202324219neil James

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A STUDY ON NUTRIENT FORAMINA IN THE SHAFT OF LONG BONES

OF UPPER AND LOWER LIMBS AT SREE MOOKAMBIKA

INSTITUTE OF MEDICAL SCIENCES

DISSERTATION SUBMITTED TO

THE TAMIL NADU DR. M.G.R. MEDICAL UNIVERSITY

IN PARTIAL FULFILMENT OF THE REGULATIONS FOR THE

AWARD OF THE DEGREE OF

M.D. ANATOMY
BRANCH - XXIII

SREE MOOKAMBIKA INSTITUTE OF MEDICAL SCIENCES,


KULASEKHARAM
THE TAMIL NADU DR. M.G.R. MEDICAL UNIVERSITY
CHENNAI - 600 032
MAY - 2019
CERTIFICATE - I

This is to certify that the dissertation entitled “A STUDY ON

NUTRIENT FORAMINA IN THE SHAFT OF LONG BONES OF

UPPER AND LOWER LIMBS AT SREE MOOKAMBIKA INSTITUTE

OF MEDICAL SCIENCES” is a bonafide work done by Dr. Neil James E.,

Sree Mookambika Institute of Medical Sciences, Kulasekharam in partial

fulfilment of the University rules and regulations for the award of Doctor of

Medicine in Anatomy (Branch XXIII) under our guidance and supervision

during the academic year 2016 – 2019.

Dr. K. Girijakumari. MS. Dr. N. Mugunthan. MS, DNB, PhD.


(Guide) (Co-guide)
Professor & Head of the Department, Professor,
Department of Anatomy, Department of Anatomy,
Sree Mookambika Institute of Sree Mookambika Institute of
Medical Sciences, Medical Sciences,
Kulasekharam, Tamil Nadu. Kulasekharam, Tamil Nadu.

Dr. Rema V. Nair. MD, DGO.


The Director,
Sree Mookambika Institute of Medical Sciences,
Kulasekharam,
Tamil Nadu.
CERTIFICATE - II

This is to certify that this dissertation work titled “A STUDY ON

NUTRIENT FORAMINA IN THE SHAFT OF LONG BONES OF

UPPER AND LOWER LIMBS AT SREE MOOKAMBIKA INSTITUTE

OF MEDICAL SCIENCES” is of the candidate Dr. Neil James E. with

registration number 201633301 for the award of Doctor of Medicine in the

branch of Anatomy. I personally verified the urkund.com website for the

purpose of plagiarism check. I found that the uploaded thesis file contains from

introduction to conclusion pages and results shows fourteen percentage of

plagiarism in the dissertation.

Guide & Supervisor sign with seal


DECLARATION BY THE CANDIDATE

I solemnly declare that the dissertation entitled “A STUDY ON

NUTRIENT FORAMINA IN THE SHAFT OF LONG BONES OF

UPPER AND LOWER LIMBS AT SREE MOOKAMBIKA INSTITUTE

OF MEDICAL SCIENCES” was prepared by me at Sree Mookambika

Institute of Medical Sciences, Kulasekharam under the guidance and

supervision of Dr. K. Girijakumari, MS., Professor & HOD, Department of

Anatomy, Sree Mookambika Institute of Medical Sciences, Kulasekharam.

This dissertation is submitted to The Tamil Nadu Dr. M.G.R. Medical

University, Chennai in partial fulfilment of the University regulations for the

award of the degree of Doctor of Medicine in Anatomy.

Place : Kulasekharam

Date : Dr. Neil James E.


ACKNOWLEDGEMENT

First of all, I thank the Lord Almighty for all the blessings that he

continues to provide me in my life.

I feel privileged in expressing my gratefulness to Dr. Rema V. Nair. MD,

DGO., Director, Sree Mookambika Institute of medical Sciences, and to

Dr. C.K. Velayudhan Nair. MS., Chairman, Sree Mookambika Institute of

Medical Sciences, for allowing to conduct the study in this institution.

I would like to put forward my sincere thanks to the Trustees of Sree

Mookambika Institute of Medical Sciences, Dr. Vinu Gopinath. MS, MCh., and

Dr. R.V. Mookambika. MD, DM., for their constant encouragement and

support throughout my studies in this institution.

I express my heartfelt thanks to Dr. Padmakumar. MS, MCh., Principal,

Sree Mookambika Institute of Medical Sciences, Kulasekharam, for his

constant support and encouragement.

I consider it a great privilege and honour to express my profound

gratitude to my guide, Dr. K. Girijakumari. MS., Professor and Head of the

Department of Anatomy, Sree Mookambika Institute of Medical Sciences for

her constant monitoring, encouragement, support and valuable guidance during

my post graduate course and this study, in this institution.


I am privileged to acknowledge the contribution of my co-guide,

Dr. N. Mugunthan, Professor, Department of Anatomy, Sree Mookambika

Institute of Medical Sciences, towards my academic career in this institution.

I would like to thank all my teachers in the Anatomy department of this

institution, Dr. Velusamy, Dr. Susie David, Dr. Rathija Sreekumar and

Dr. Lekshmy for guiding and supporting me throughout my post graduate

course.

I express my gratitude to the non-teaching staff members of the

Anatomy department of this college for their encouragement and support

during my study period.

I would like to place on record, my thanks to my better half, Dr. Daya

Pauline S., for her constant support and help throughout my post graduate

course and in completing this study.

I acknowledge the contributions of my parents and children towards my

life and career.

Dr. NEIL JAMES E.


TABLE OF CONTENTS

SL. NO. CHAPTER PAGE NO.

1 INTRODUCTION 1–3

2 AIMS AND OBJECTIVES 4

3 REVIEW OF LITERATURE 5 – 34

4 MATERIALS AND METHODS 35 – 42

5 RESULTS 43 – 68

6 DISCUSSION 69 – 90

7 CONCLUSION 91

8 BIBLIOGRAPHY

9 ANNEXURES
LIST OF ABBREVIATIONS

FI - Foraminal index

DNF - Distance of foramen form the proximal end of the bone

TL - Total length of the bone

S.D. - Standard deviation

ORIF - Open reduction internal fixation

AMS - Antero-medial surface

AS - Anterior surface

PS - Posterior surface

MC - Medial crest
INTRODUCTION
INTRODUCTION

The human body has its framework built up by a series of bones which

are supplemented by cartilages in certain regions. The bony portion of this

framework is referred to as the skeleton of the body. In an adult human skeleton,

there are a total of 206 bones which may be classified into long, short, flat and

irregular bones based on the shape or morphology. The long bones are present

in the limbs and each long bone has a shaft (also called diaphysis) and two

extremities.1

The long bones obtain their major blood supply during their period of

growth and during early stages of ossification from the nutrient arteries. The

nutrient foramina are the largest of the foramina in the shaft of long bones

through which the nutrient arteries enter the bone. These foramina lead to

nutrient canals which are cavities in the shaft of long bones that conduct the

nutrient arteries.2

The nutrient foramen is distinguished from any other foramen by the

presence of a distinct vascular groove outside the foramen. The direction of the

nutrient canal usually follows a general rule “towards the elbow and away from

knee I flee”, as per the study done by Rao and Kothapalli in the year 2014, and

this direction of the canal helps in determining the growing end of the bone.3

Harris has stated that the position of nutrient foramen is constant during

the growth of a long bone.4

1
The blood supply to bone is crucial in bone grafting and should be

preserved for promoting fracture healing.5 The blood supply is also essential

for the survival of osteocytes in cases of tumor resection, trauma and congenital

pseudoarthrosis.6 The statistical data on the distribution of nutrient foramina in

long bones helps the professional in selecting the osseous section levels of the

receptor for placing the graft without damaging the nutrient arteries, thus,

preserving the diaphyseal vasculature and the transplant consolidation.7

The relative relationship between the length of bone and the distance of

nutrient foramen from either end can be used for calculating the bone length

from a given fragment, and from the length of a long bone the height of the

individual can be calculated. This in important in medico-legal and

anthropological works. Therefore, an understanding of the number and position

of the nutrient foramina in long bones is essential for surgical procedures such

as joint replacement therapy, fracture repair bone graft and vascularized bone

microsurgery, as well as for medico-legal cases.3

The present study is a cross-sectional study aimed at creating a

generalisable pattern for the long bones of upper and lower limbs regarding the

number of nutrient foramina, position of these foramina in the various surfaces

and borders of the bones, location of the foramina based on the foraminal index,

size of the foramina, direction of the foramina and the obliquity of the nutrient

canals leading in to the medullary cavity from the nutrient foramina.

2
The study is conducted with the dry long bones available in the

Department of Anatomy of Sree Mookambika Institute of Medical Sciences,

Kulasekharam.

3
AIMS AND OBJECTIVES
AIMS AND OBJECTIVES

1) To determine the number, position and location of nutrient foramina in the

shaft of long bones.

2) To determine the size and direction of the nutrient foramina and obliquity

of the nutrient canals running from the nutrient foramina.

4
REVIEW OF LITERATURE
REVIEW OF LITERATURE

The knowledge about the number, position & location, size and direction

of the nutrient foramina may aid clinically in surgical procedures which include

fracture repair, joint replacement and vascularised bone grafting8. An idea on

the anatomy of the nutrient foramina will also aid in the diagnosis of

longitudinal stress fracture9.

The review of literature for the present study has been done under the

following headings.

1) Number of nutrient foramina

2) Position and location of nutrient foramina

3) Size of nutrient foramina

4) Direction of nutrient foramina

5) Obliquity of nutrient canals

1) NUMBER OF NUTRIENT FORAMINA

Lutken (1950) studied the number of nutrient foramina in the shaft of

humerus and femur. He found that of the 316 humeri studied, 228 had a single

nutrient foramen, 81 had double foramina and 4 had triple foramina. In femur,

of the 410 bones studied, 219 had a single foramen, 182 had double foramina

and 9 had triple foramina.10

5
According to a study done by Carroll (1963) on the number of nutrient

foramina in the diaphysis of seventy-one humeri, 48 bones had a single nutrient

foramen, 20 had double foramina and 3 bones had triple nutrient foramina.11

In the year 1967, Mysorekar studied the number of nutrient foramina in

the shaft of 180 each of the long bones of upper and lower limbs and reported

the following findings. Among the humeri, 104 bones showed a single nutrient

foramen, 68 bones had double foramina, 5 bones had triple foramina and 2

bones had four foramina each. Radii had a single foramen in all the bones

except 8 bones with double foramina and 4 bones with none. In ulnae, no

nutrient foramen was seen in 2 bones and double foramina were observed in 10

bones with the rest having a single nutrient foramen. Femur showed no foramen

in 6 of the bones, single nutrient foramen in 81 bones, double foramina in 90

bones and triple foramina in 3 bones. Tibia showed a single nutrient foramen

in all the bones except two, which had two foramina each. In the case of fibula,

7 bones didn’t show any foramen, with 6 showing double foramina and the rest

having a single nutrient foramen.12

Longia et al. (1980) in their study on the diaphyseal nutrient foramina

of 200 each of the long bones of upper and lower limbs reported the following

findings. Humerus showed a single foramen in 85%, double foramina in 13%

and no foramen in 12% of the bones studied. In radius, single and double

foramina were present respectively in 96% and 3% of the bones studied, with

1% of the bones not showing any foramen. Ulna showed a single nutrient

foramen in 95% of the bones studied, double foramina in 4% and triple

6
foramina in 1% of the bones. In femur, single, double, triple and quadruple

foramina were present in 69.5%, 26.5%, 3% and 1% of the bones respectively.

Tibia showed a single nutrient foramen in 95% and double foramina in 5% of

the bones studied. In fibula, single foramen was present in 92% and double

foramina in 8% of the bones studied.5

A study done by Guo (1981) on the nutrient foramina in fibula reported

that, of the 295 bones studied, 280 had a single nutrient foramen, 10 had double

foramina and 5 didn’t have nutrient foramen.13

The number of nutrient foramina in the upper and lower limb long bones

was studied by Campos et al. in 1987, and the following findings were reported.

Humeri showed single and double foramina in 75% and 25% of the 36 bones

studied. In the case of radius, all of the 33 studied bones showed a single

nutrient foramen. In the case of ulna, of the 33 bones studied, 91% showed a

single nutrient foramen and the rest showed double foramina. Of the 31 femora

studied, single, double and triple foramina were found in 30%, 60% and 10%

of the bones respectively. Tibia showed a single foramen in 93% and double

foramina in 7% of the total 30 bones studied. Fibula showed a single nutrient

foramen in all of the 33 bones studied.14

Sendemir and Cimen (1991) studied the number of nutrient foramina in

the shaft of femur, tibia and fibula. Of a total of 102 femora studied, they

reported single, double, triple and quadruple foramina in 26.5%, 46%, 12.7%

and 7.8% of the bones respectively. They also reported few femur bones having

6, 8 and 9 nutrient foramina. They observed a single nutrient foramen in 94.8%

7
of the tibiae and double foramina in the rest, out of the 134 bones studied. With

regard to fibula, they reported a single nutrient foramen in 73.9% of the bones

and double foramina in 7.2%, of the total 69 bones studied. The rest of the

fibulae didn’t have a dominant nutrient foramen.6

A study on the nutrient foramina in the lower limb long bones done by

Gumusburun et al. (1994) revealed that among the 103 femora studied, 40

bones had a single foramen, 44 had double foramina, 11 had three foramina, 4

had quadruple foramina and one each had five and six foramina. Nutrient

foramen was absent in two femora. Among the 106 tibiae studied, they reported

a single nutrient foramen in 84.9% of the bones, double foramina in 11.4%,

triple foramina in 2.8% and no foramen in 0.9% of the bones. With regard to

fibula, they reported that 85% of the 60 bones that they studied had a single

nutrient foramen, 12% had double foramina and 3% didn’t show any foramen.15

It was observed from a study on the number of diaphyseal nutrient

foramina in 109 femora by Bridgeman and Brookes (1996) that 48 bones had a

single foramen and 58 bones had double foramina. Three bones didn’t show

nutrient foramen.16

Out of the 305 fibulae analysed for the number of nutrient foramina by

Gumusburun et al. (1996), 281 had a single foramen and 12 had double

foramina, with the rest of the bones not having nutrient foramen.17

Kirschner et al. (1998) in their study on the arterial blood supply of

femur and tibia observed the number of nutrient foramina in these bones and

reported that out of the 200 femora studied, 35% had a single nutrient foramen,

8
57% had double foramina and 8% had triple foramina. In tibia, of the 200 bones

studied, they reported a single nutrient foramen in 93.5% of the bones, with

double foramina in the rest.18

A total of 130 femora were studied for the number of nutrient foramina

by Al-Motabagani (2002) and it was found that 3% of the bones didn’t have a

nutrient foramen. He reported that half of the remaining bones had a single

nutrient foramen and the other half had double foramina.19

Kizilkanat et al. (2006) studied the number of nutrient foramina in the

long bones of upper and lower limbs. Of the 101 humeri studied they found

single, double, triple and quadruple foramina (foramen) in 69, 22, 7 and 1

bone(s) respectively. Two humeri didn’t have nutrient foramen. They studied

93 radii of which 92 had a single foramen and one had two nutrient foramina.

Of the 102 ulnae studied, they found a single nutrient foramen in 101 bones and

double foramina in one bone. Regarding femora, they found a single foramen

in 75 bones and double foramina in 25 bones, of the total 100 studied. With

regard to tibia, they observed that out of the total 100 bones studied, 98 had a

single nutrient foramen and 2 bones had double foramina. Of the 73 fibulae

studied, they found a single nutrient foramen in 68 bones and double foramina

in 4 bones. They also reported that one fibula didn’t have nutrient foramen.8

The nutrient foramina in the upper limb long bones were studied by

Murlimanju et al. in 2011 and they found that of the 96 humeri studied, 93.8%

had a single nutrient foramen, 3.1% had double foramina and another 3.1%

didn’t show any foramen. Of the 72 radii studied, 94.4% of the bones had a

9
single foramen, 1.4% had double foramina and 4.2% didn’t show a foramen.

All of the 75 ulnae studied had a single nutrient foramen.20

In a study done in the year 2011, by Pereira et al., on the nutrient

foramina in the shaft of 174 humeri, 157 radii, 146 ulnae, 152 femora, 142

tibiae and 114 fibulae, they observed a single nutrient foramen in 88.5% of

humeri, 99.4% of radii, 98.6% of ulnae, 63.8% of femora, 98.6% of tibiae and

99.1% of fibulae. They reported double foramina in the rest of the bones except

in femur where they found that 34.9% and 1.3% had double and triple foramina

respectively.21

Ukoha et al. (2013) studied about the nutrient foramina in 150 humeri,

50 radii and 50 ulnae and reported that a single nutrient foramen was present in

66% of humeri, 68% of radii and 78% of ulnae. Double foramina were seen in

8% of the humeri. They didn’t find a nutrient foramen in the rest of the bones.22

Gupta and Kumari (2014) observed from their study on the number of

nutrient foramina in human tibia that 96.5% of the bones had a single nutrient

foramen, 0.3% had double foramina and 3.2% didn’t have any nutrient

foramen, of the total 312 bones studied.23

The number of diaphyseal nutrient foramina in femur was analysed by

Oyedun in the year 2014 and it was found that, of the 95 bones studied, single

nutrient foramen was present in 74 bones and double foramina in 21 bones.24

Out of the 200 radii studied by Shah and Saiyad (2014), 197 bones had

a single nutrient foramen with the remaining three having double foramina.25

10
The number of nutrient foramina in the shaft of 100 humeri and 80 each

of radius and ulna was studied by Solanke et al. (2014), which showed that a

single nutrient foramen was present in 92 humeri, 74 radii and 77 ulnae. Double

foramina were reported in 4 humeri and 2 radii. The rest of the bones didn’t

show a nutrient foramen.26

Bhat (2015) studied the nutrient foramina in 300 adult femora and

reported that 118 of them had a single nutrient foramen, 180 had double

foramina and 2 bones had triple nutrient foramina. They found that all of the

bones showed at least a single nutrient foramen.27

Nidhi et al. (2015) reported from their study on the dominant and

secondary nutrient foramina in fibula that, of the 160 bones studied, 141 had a

dominant single nutrient foramen, 11 bones had double foramina (one being

dominant and the other secondary) and 8 bones had only a single secondary

foramen.28

The nutrient foramina in 100 femora were studied by Poornima and

Angadi in the year 2015 and it was reported that 62 bones had a single nutrient

foramen, 37 bones and double foramina and one bone had triple nutrient

foramina.29

Roul and Goyal (2015) studied the number of nutrient foramina in thirty-

seven each of the long bones of the upper limb. They found a single nutrient

foramen in 94.6% of humeri, 97.29% of radii and 100% of the ulnae. They

reported double nutrient foramina in the remaining bones.2

11
Roul and Goyal (2015) studied the nutrient foramina in the long bones

of lower extremity which involved 37 bones each of femur, tibia and fibula.

They found that femur showed single, double and triple nutrient foramina in

27.02%, 59.4% and 13.51% of the bones respectively. Among the tibiae, 83.7%

of the bones showed a single nutrient foramen while the rest had double

foramina. In the case of fibula, 81.08% of the bones had a single nutrient

foramen with the rest having double nutrient foramina.30

Seema et al. (2015) observed from their study on the number of nutrient

foramina in the lower limb long bones that, of the 60 femora studied, 29 bones

had a single nutrient foramen and 29 bones had double foramina. Two femora

had triple nutrient foramina. Of the 60 ulnae studied, 57 had a single nutrient

foramen and 3 had double foramina. In the case of fibulae, 50 had a single

nutrient foramen and 10 had double foramina, of the total 60 bones studied.31

The nutrient foramina in a total of 120 humeri were studied by Asharani

and Ningaiah (2016) who found that 87% of the bones had a single foramen,

11% had double foramina and 2% of the bones had none.32

A single nutrient foramen was found in all of the 50 tibiae studied by

Jayaprakash in the year 2016.33

The study on the nutrient foramina of 253 femora by Mansur et al.

(2016) revealed that 154 bones had a single nutrient foramen, 73 bones had

double foramina, 16 had triple foramina and a few bones showed quadruple

foramina. Five of the bones didn’t show any nutrient foramen.34

12
Out of the 100 fibulae analysed by Sinha et al. (2016), 78 bones had a

single nutrient foramen with the rest having double foramina.35

In the year 2017, Kumar et al. carried out a study on the nutrient

foramina in 151 tibiae and reported that 131 bones had a single nutrient

foramen, 18 bones had double foramina and 2 bones had triple foramina.36

Kumar et al. (2017) reported from their study on the nutrient foramina

in 110 radii that 108 of them had a single nutrient foramen with the remaining

two bones having double foramina.37

Priya and Janaki (2017) studied the number of nutrient foramina in 100

femora and found that 70% of the bones had a single nutrient foramen, 24%

had double foramina and 6% of the bones had triple foramina. They have

further conducted a study on the nutrient foramina of 92 tibiae in the same year

and reported that 89.2% of the bones had a single nutrient foramen and 10.8%

had double nutrient foramina.38,39

A study on the number of nutrient foramina in long bones of human

upper extremity by Veeramuthu et al. (2017) revealed that, of the total of 55

humeri, 46 had a single nutrient foramen, 8 bones had double foramina and 1

bone had none. Of the 59 radii studied, 57 bones had a single nutrient foramen

and 2 bones had none. Ulnae showed a single nutrient foramen in 57 bones,

double foramina in 1 bone and no foramen in 1 bone, of the total 59 bones

studied.40

13
2) POSITION AND LOCATION OF NUTRIENT FORAMINA

The study conducted by Mysorekar in 1967 on the position of nutrient

foramina in 180 bones each of humerus, radius, ulna, femur, tibia and fibula

revealed the following findings. Femora had foraminal index ranging between

16.55 and 67.5 with the majority of the foramina lying in the linea aspera and

its lips, in the third-sixth and fourth-sixth of the bones. Tibiae had most of the

foramina in the upper third of the bones lateral to the vertical line in the

posterior surface, with foraminal index ranging between 23.5 and 44.63. The

foraminal index in fibulae ranged from 27.08 to 70.65, with the majority of

foramina in the middle third of the bones, in the medial crest and between the

medial crest and posterior border. Humeri had foraminal index ranging between

26.51 and 74.46, with the majority of the foramina lying in the third and fourth-

sixth of the bones, in the antero-medial surface and medial border. Radii had

the most foramina in the middle third of the bones followed by the proximal

third, in the anterior surface of the bones, with foraminal index ranging between

27 and 48. In ulnae, he found similar distribution of foramina as that of radii,

with foraminal index ranging between 23.63 and 59.51.12

Longia et al. (1980) reported the location of nutrient foramina in the long

bones of upper and lower limbs as follows. Humeri had most of the foramina

in the antero-medial surface in the middle third of the shaft. Radii also had the

majority of foramina in the middle third of the shaft in the anterior surface. In

ulnae, anterior surface had the greatest number of foramina, with 55.66% of the

14
foramina being found in the upper-third and 43.4% in the middle-third of the

shaft. Femora had 56.09% and 42.8% of the foramina in the middle and upper

third of the shaft respectively. The majority were present in the linea aspera and

its lips. Tibiae had the greatest number of nutrient foramina in the proximal

third of the shaft below the soleal line in the posterior surface. Fibulae had

nearly 85% of their foramen in the middle third of the shaft.5

Campos et al. (1987) in their study on the position of nutrient foramina

in human long bones found that the foramina in the upper limb long bones were

located nearer to the elbow than to the shoulder or wrist. Radii and ulnae had

their foramina constantly in the anterior surface. Almost all the humeri had a

dominant foramen in the anteromedial surface, with a secondary foramen

occasionally present in the antero-lateral or posterior aspect of the bone. In

femora, the majority of the foramina were found closer to the hip, in the linea

aspera and its lips. Tibiae had the greatest number of foramina near the junction

of the proximal and the middle thirds of the bone, below the soleal line in the

posterior surface. In fibulae, the foramina were found most in the middle third

of the bones, distributed almost equally between the posterior and medial

surfaces, with foraminal index ranging between 35 and 67.14

Sendemir and Cimen (1991) analysed the situation of nutrient foramina

in the shaft of long bones of lower limbs and reported that 86.6% of the

foramina in the 102 femora studied were in the linea aspera and its lips with

7.1% of the foramina lying in the anterior aspect of the femur. Foraminal index

ranged between 26.7 and 82.1 with the majority of the foramina being found in

15
the middle third of the bone. In the 134 tibiae studied, 90.8% of the foramina

were present in the posterior surface with 5.7% in the lateral surface. Foraminal

index for the foramina in the posterior surface of tibia was 32.3 ± 3.5 with

majority of the foramina in the upper two-third of the bone. In the 69 fibulae

studied, 88.5% of the foramina were seen in the medial surface, 9.8% in the

posterior surface and 1.6% in the lateral surface. Most of the foramina in fibulae

were present near the midpoint of the shaft having foraminal index between

29.8 and 67.8 with a mean foraminal index of around 46.6

The position of nutrient foramina in 103 femora, 106 tibiae and 60

fibulae was studied by Gumusburun et al. in the year 1994, which showed that

the majority of the femoral foramina were present in the linea aspera and its

lips confined to the third-sixth and fourth-sixth of the bone. The mean foraminal

index was 48.82. Tibia had the majority of the foramina in the posterior surface.

The mean foraminal index was 33.17 with the upper-third having the most

foramina followed by the middle-third. No foramen was reported in the lower-

third of tibia. In fibula also, the posterior surface had the most foramina in the

medial crest of the bone. The mean foraminal index for fibula was 47.82 with

majority of the foramina lying in the middle third of the bone.15

Gumusburun et al. (1996) studied the diaphyseal nutrient foramina of

fibula (305 bones) and reported that, of the 305 foramina, 298 were present in

the middle third of the bone with a mean foramen index of 48.13 ± 0.46 (range

from 23 to 70). They also found that 48.36% of the foramina were present in

the posterior surface and 19.74% in the medial crest of the bone.17

16
Malukar and Joshi (2011) reported the following findings from their

observation on the position of nutrient foramina in 100 bones each of humerus,

radius, ulna, femur, tibia and fibula. Radius, ulna and tibia had the majority of

foramina in the upper thirds of their length. Humerus and fibula had their

majority in the middle third. Of the 167 foramina found in femur, 86 were

present in upper third, 59 in the middle third and 22 in the lower third. With

regard to the distribution of foramina in the various surfaces of the bones,

humerus had the majority in the antero-medial surface, radius and ulna in the

anterior surface, femur in and around the linea aspera, tibia in the postero-

lateral surface and fibula in the posterior surface.41

In 2011, Murlimanju et al. analysed the position of nutrient foramina in

the upper limb long bones and observed that, of the 96 humeri studied, 58 had

their foramina in the antero-medial surface, 32 in the medial surface and 3 each

in the anterior border and posterior surface. Of the 72 radii studied, 52 had their

foramina in the anterior surface, 10 bones in the interosseous border, four in the

anterior border and four bones in the posterior surface. In the case of ulna, of

the 75 bones studied, 65 bones had their foramina in the anterior surface, eight

in the anterior border and two bones in the interosseous border.20

Pereira et al. (2011) in their study on nutrient foramina in long bones of

upper and lower limbs found that most of the foramina were present in the

anterior aspect of the bones of upper limb and in the posterior and lateral aspects

of the bones of lower limb. They also reported that the majority of foramina in

the upper limb bones were present in the anteromedial surface of humerus

17
(89.7%) and in the anterior surfaces of radius (82.2%) and ulna (73.2%). In the

lower limb bones, most of the foramina were present in the linea aspera of

femur (93.4%), posterior surface of tibia (93.7%) and lateral surface of fibula

(98.2%).21

The study on the nutrient foramina in 101 femora by Kumar et al. (2013)

showed that 52% of the bones had their nutrient foramina in the middle third

and the rest in their upper third. They also reported that more than 50% of the

foramina were located in relation to the linea aspera and around 35% were

present in the posteromedial surface.42

Ukoha et al. (2013) studied the position of nutrient foramina in 150

humeri, 50 radii and 50 ulnae and inferred that the mean foraminal indices for

the three bones respectively were 56.28 ± 4.90, 33.74 ± 4.94 and 36.70 ± 4.56,

with the majority of humeri having the foramina in the middle third of the

bones, radii in the proximal third followed by the middle third and ulnae in the

middle third followed by the proximal third. The greatest number of nutrient

foramina were present in the antero-medial surface of humeri and anterior

surface of radii and ulnae.22

The position of nutrient foramina in 189 fibulae was worked out by

Bilodi and Reddy in 2014 and they that 29.62% of the foramina were present

in the posterior surface, 22.23% in the lateral surface, 21.16% in the medial

surface, 8.99% in the medial crest, 7.93% in the interosseous border and 2.11%

in the posterior border of the shaft of the bones. They also reported an increased

distribution of foramina in the middle third of the shaft.43

18
Gupta and Kumari (2014) conducted a study on the nutrient foramina of

312 tibia and concluded that 299 of them had their foramina in the posterior

surface. The foraminal index ranged between 28.09 and 37.57 with a mean of

32.86, indicating that most of the foramina were present in the lower part of

upper third and upper part of middle third of the bones.23

Oyedun (2014) analysed the nutrient foramina in 95 femora and arrived

at a conclusion that the majority of the foramina were located in the posterior

aspect. He also observed that most of the bones (78.94%) with a single nutrient

foramen had their foramina in the linea aspera and its lips. In the case of bones

with double nutrient foramina, the most common site was in the medial surface

followed by linea aspera, with the proximal foramen lying in the medial surface

of the bone. The mean foramen index in this study of 42.46 with a standard

deviation of 9.18 showed that majority of the foramina were present in the

middle third of the bone.24

The architecture of diaphyseal nutrient foramina in the bones of upper

and lower limbs was studied by Rao and Kothapalli (2014) and they found that

most of the humeri had their foramina in the proximal part of lower half of the

bone whereas almost all radii had theirs in the proximal third of the bone. In

ulnae, the foramina were distributed most in the proximal and middle thirds of

the bones. In the lower limb long bones, they reported that most femora had

their foramina in the middle portion of upper half of the bone followed by few

in the proximal portion of the lower half of the bone. In tibiae they reported that

19
all the foramina were present in the upper one-third of the bones, while in

fibulae almost all the foramina were present in the middle third of the bones.3

Shah and Saiyad (2014) worked out the nutrient foramina in 200 radii

and concluded that the mean foraminal index was around 36 and that the

majority of the foramina were present in the anterior aspect of the bones closer

to the upper end than that to the lower end.25

The study conducted by Solanke et al. (2014) on the position of nutrient

foramina in 100 humeri, 80 radii and 80 ulnae revealed that the majority of the

foramina were present in the antero-medial surface in humeri (67%) and in the

anterior surface in radii and ulnae (66.25% and 76.62% respectively). They also

found that the radii had a significant number of foramina (21.25%) in the

medial border.26

Bhat (2015) deduced from her study on the position of nutrient foramina

in femur, that 52% of the foramina were present in the medial lip of linea aspera

followed by 41% in the lateral lip and the majority of the remaining in the

medial surface of the bones. She also found that 48% of the foramina were

present in the junction of upper and middle thirds of the shaft and 38% in the

junction of middle and lower thirds of the shaft of the bones, with the remaining

foramina being present in the middle third of the shaft.27

Mazengenya and Fasemore (2015) studied the location of nutrient

foramina in the long bones of lower limb and found that the majority of the

femora had their nutrient foramina in the middle third of the bones in the linea

aspera and its lips. In tibia, the majority of the foramina (around 75%) were

20
found in the upper third of the posterior surface. Fibulae had most of the

nutrient foramina in the posterior surface followed by medial surface and were

present mostly in the middle third of the bones.44

The study conducted by Nidhi et al. (2015) on the nutrient foramina in

fibulae revealed that out of the 171 foramina found in 160 bones, almost 90%

of the foramina were present in the posterior surface in the middle third of the

shaft of the bones.28

A study on the position of nutrient foramina in 100 femora was

performed by Poornima and Angadi (2015) and they reported that 56.1% of the

foramina were present at the junction of the upper and middle third of the shaft,

18.7% at the junction of middle and lower third of the shaft and 23% of the

foramina in the middle one-third of the shaft of the bones.29

Roul and Goyal (2015) carried out a study on the nutrient foramina of

long bones of upper extremity and found that of the 37 humeri studied, 36 had

their foramina in the middle one-third of the bone and one humerus had the

foramen in its lower third. Among the thirty-seven radii, 28 bones had their

foramina in the middle third while 9 bones had them in the upper third of their

length. Ulna showed almost similar numbers with 25 bones having the nutrient

foramina in their middle third and 12 bones in their upper third, of a total of 37

bones studied. In the same year, the authors also studied the nutrient foramina

in 37 bones each of femur, tibia and fibula and found that 17 and 19 femora

respectively had their nutrient foramina in the upper and middle thirds of the

shaft. One bone had its foramen in the lower third of the shaft. With respect to

21
tibiae, 34 bones had their foramina in the upper third of the shaft and 3 bones

in the middle third. Fibula had its foramina in the middle third of the shaft in

27 bones and in the proximal third of the shaft in 10 bones.2,30

Seema et al. (2015) explored the position of nutrient foramina in the long

bones of lower limb (60 bones each) and revealed that most of the bones had

their foramina in the posterior aspect, with femur having 76.5% of the foramina

in the linea aspera, tibia with 95.5% of the foramina below the soleal line and

fibula having 65% of the foramina in the posterior surface. They also found that

fibula had 15% of the nutrient foramina in the medial surface.31

A study on the nutrient foramina in 120 adult humeri was done by

Asharani and Ningaiah in 2016. They reported that the majority of the bones

had their nutrient foramina in the middle third of the shaft, distributed most in

the medial border followed by the anteromedial surface.32

Jayaprakash (2016) studied the position of nutrient foramina in 50 tibiae

and reported that 18% of the foramina were present in the middle third of the

shaft while the rest were found in the upper third of the shaft, with the foraminal

index ranging between 31.12 and 40.60. Most of the foramina were distributed

lateral to the vertical line in the posterior surface of the bones.33

An investigation on the nutrient foramina in humeri by Mansur et al.

(2016) established the following findings. A total of 368 foramina were found

in the 253 bones studied and 88.86% of the foramina were found in the antero-

medial aspect of the shaft. Antero-lateral surface had 6.52% of the foramina

and the posterior surface of the shaft had 4.62% of the foramina. They also

22
observed that 94.84% of the foramina were present in the middle one-third of

the shaft, 4.62% in the lower third and the rest in the upper third of the bone.34

Sinha et al. (2016) carried out a study on the nutrient foramina in 100

fibulae and found that all of the dominant foramina were present in the middle

third of the shaft with a mean foraminal index of around 46. They also reported

that almost all the foramina were present in the posterior aspect of the bones.35

The study on the nutrient foramina in radius and ulna by Ashwini et al.

(2017) outlined that the majority of the foramina were present in the middle

one-third of the shaft in the anterior surface of the bones.45

Kumar et al. (2017) established from their study on the nutrient foramina

in 151 tibiae that 79% of the foramina were situated below the soleal line in the

posterior surface of the bones and that the foramina were found predominantly

in the upper third of the shaft of the bones with the foraminal index ranging

between 28.33 and 35.85.36

Investigations on the position of nutrient foramina in 100 femora and 92

tibiae were carried out by Priya and Janaki in 2017. The results are outlined

below. Among the femora, 56% of the bones had their nutrient foramina in the

middle third of the bones, 42% in the upper third and 2% in the lower third.

Almost all the foramina were present in the linea aspera and its lips. In case of

double and triple nutrient foramina, most were present in the middle third of

the shaft in and around the linea aspera, with a few foramina in the lower third

of the shaft. Among the 92 tibiae, 86 bones had their foramina in the posterior

surface and 6 bones in the medial surface. All the bones had their foramina in

23
the upper third of the shaft. In the bones with double nutrient foramina, the

second foramen was found most and equally distributed in the upper and middle

thirds of the bone, with a few in the lower third of the shaft.38,39

Veeramuthu et al. (2017) reported from their study on 55 humeri, 59

radii and 59 ulnae that 89% of the humeral foramina were present in the middle

third of the shaft, with a mean foraminal index of 58.95 ± 5.63. Radii had 59%

and 41% of the foramina respectively in the middle third and proximal third of

the shaft, with a mean foraminal index of 33.78 ± 4.64. In ulnae, 68% of the

foramina were present in the middle third of the shaft and 32% in the proximal

third, with a mean foraminal index of 36.39 ± 5.61. They also reported that

humeri had the majority of the foramina in the antero-medial surface, radii in

the anterior surface and ulna also in the anterior surface.40

3) SIZE OF NUTRIENT FORAMINA

Longia et al. (1980) studied the diaphyseal nutrient foramina of 200 each

of the human long bones and found that of the 222 humeral foramina, 20.29%

were large (more than 2 mm in diameter), 62.32% medium sized (diameter

between 1 mm and 2 mm) and 17.39% were small (diameter less than 1 mm).

Of the 204 radial foramina found, 1.8% were large, 80.18% were medium sized

and 18.02% were small. The percentages of large, medium and small sized

foramina in ulnae were 1.96, 73.53 and 24.51 respectively. Of the 271 femoral

foramina, 66.98% were medium sized and 33.02% were small. In the case of

24
tibiae, 7.01% of the foramina were large, 59.41% were medium sized and

33.58% were small. Fibulae showed a total of 216 foramina of which 8.57%

were large, 79.52% medium and 11.91% small in size.5

Guo (1981) from his observations on the blood supply of fibula reported

that besides the nutrient foramina, many minute foramina were found on the

surface of fibula, through which the muscular branches of the peroneal artery

may enter the bone piercing the periosteum and supply it. He stated that in this

way the bones without a nutrient foramen get their blood supply from the

musculo-periosteal vessels.13

Campos et al. (1987) from their study on nutrient foramina of human

long bones observed that in the case of humeri with double foramina, the

dominant foramen was always present in the antero-medial surface of the bones

whereas the secondary foramen was present either in the posterior surface or

rarely in the antero-lateral surface.14

The nutrient foramina in the shaft of long bones of lower limb was

analysed by Sendemir and Cimen (1991) and they reported that all of the 102

femora studied had at least one dominant nutrient foramen with two bones

among them showing eight and nine dominant nutrient foramina respectively.6

Bridgeman and Brookes (1996) from their study on human femoral

diaphysis reported that in the case of bones with multiple nutrient foramina,

they were not always of the same size and that either the upper or the lower

foramen could be smaller.16

25
The study carried out on the arterial supply of diaphysis of femur by Al-

Motabagani (2002) revealed that in the bones with double nutrient foramina,

the two foramina were not necessarily equal in size.19

Kizilkanat et al. (2007) analysed the nutrient foramina in the long bones

of upper and lower limbs and recorded the following observations. A dominant

nutrient foramen was present in all the bones which showed a single nutrient

foramen. In the bones which had double, triple and quadruple foramina, the

proportion of dominant and secondary foramina was almost the same.8

Kumar et al. (2013) studied the nutrient foramina in 101 femora and

reported that, of the total of 150 foramina found in 99 bones, 102 (68%) were

dominant foramina and the remaining 48 (32%) were secondary foramina. Of

all the secondary nutrient foramina, one foramen was found in a femur with a

single nutrient foramen and the rest were found in bones with double nutrient

foramina.42

Gupta and Kumari (2014) observed the size of nutrient foramina in 312

tibiae and found that all of the 302 foramina present were of the dominant type

of which 293 foramina were large, admitting a 20-gauge needle through them

comfortably.23

A study carried out by Bhat (2015) on 300 femora established that the

majority of the foramina were of the dominant type.27

Nidhi et al. (2015) observed in their study on the nutrient foramina in

160 fibulae that 141 bones had a single dominant nutrient foramen (≥0.56mm

in diameter) and 8 bones (5%) had a single secondary nutrient foramen. Also,

26
they found that 11 bones had double nutrient foramina of which one was

dominant and the other secondary.28

Poornima and Angadi (2015) studied the size of nutrient foramina in 100

femora and reported 7.2% of the foramina to be large (diameter ≥ 1.27mm),

64.7% of the foramina medium sized (diameter ≥ 0.90mm to < 1.27mm), 16.5%

of the foramina small (diameter ≥ 0.71mm to < 0.90mm) and 11.5% of the

foramina to be very small (diameter ≥ 0.55mm < 0.71mm).29

Sinha et al. (2016) studied the size of nutrient foramina in 100 fibulae

and found that, of the 122 foramina present, 104 were of the dominant type

(≥0.56mm diameter) and 18 were of the secondary type.35

Kumar et al. (2017) measured the size of nutrient foramina in 151 tibiae

and graded the size of the foramina based on their diameters, using hypodermic

needle. Of the 173 foramina found, 116 foramina had a diameter of 1.27 mm

or more (18G needle), 18 foramina had diameter between 0.9 mm and 1.27 mm

(20G needle), 18 foramina had diameter between 0.71 mm and 0.9 mm (22G

needle) and 21 foramina had diameter between 0.55 mm and 0.71 mm (24G

needle).36

Veeramuthu et al. (2017) studied the nutrient foramina in the upper limb

bones and reported that of the 55 humeri studied, 31 bones had a small foramen

(0.5 to 0.7 mm diameter), 21 bones had a medium sized foramen (0.7 to 1.1

mm diameter) and 3 bones had a large foramen (greater than 1.1 mm diameter).

Of the 59 radii studied, 50 bones had a small foramen, 8 bones had a medium

27
sized foramen and 1 bone had a large nutrient foramen. Of the 59 ulnae studied,

42, 14 and 3 bones had small, medium and large sized foramina respectively.40

4) DIRECTION OF NUTRIENT FORAMINA

A study on the nutrient foramen in humerus and femur was conducted

by Lutken (1950) and the following findings were published. In the 316 humeri

observed, 402 foramina were present and all were directed distally towards the

elbow. In the case of femur, 610 nutrient foramina were found in the 410 bones

studied, of which 597 were directed proximally away from the knee, 7 foramina

distally towards the knee and 6 foramina directed anteriorly.10

The investigations on the nutrient foramina in 164 bones each of radius

and ulna carried out by Shulman (1959) suggested that all of the bones with

nutrient foramina had them directed towards the elbow, obeying the general

concept of nutrient foramen being directed towards the elbow in the long bones

of upper limb.46

Mysorekar (1967) studied the nutrient foramina in 180 bones each of the

long bones of upper and lower limbs and reported that all of the bones except

9 fibulae had their foramina directed normally (towards the elbow and away

from the knee). Of the exceptions, six fibulae had a single foramen each which

were directed upwards towards the knee and 3 fibulae had double nutrient

foramina, one foramen being directed upwards and the other foramen

downwards.12

28
Longia et al. (1980) in their study on the nutrient foramina in 200 bones

each of humerus, radius, ulna, femur, tibia and fibula observed that all of the

bones with nutrient foramina except one femur, 7 tibiae and 19 fibulae had their

foramina directed away from the growing end, that is towards the elbow in

upper limb bones and away from the knee in lower limb bones. Among the

exceptions mentioned above, 3 fibulae had a single nutrient foramen in them

which was directed upwards and the rest of the bones had double foramina,

with one directed upwards and the other downwards.5

The study on the nutrient foramina in 100 each of the longs bones of

upper and lower limbs by Malukar and Joshi (2011) revealed that all except

1.3% of the bones followed the theory of nutrient foramina being directed away

from the growing end, that is towards the knee in lower limb bones and away

from the knee in lower limb bones.41

Kumar et al. (2013) studied the direction of nutrient foramina in 101

femora and reported that of the 150 foramina found, 148 were directed

proximally and 2 were directed distally.42

The nutrient foramina in the shaft of long bones of the upper limb was

studied by Ukoha et al. (2013) and the following findings were recorded. Of

the 150 humeri, 50 radii and 50 ulnae studied, only one radius had its foramen

directed distally (away from the elbow) and all the other bones had their

foramina directed towards the elbow away from the growing end.22

29
Studies on the direction of nutrient canals in 189 fibulae carried out by

Bilodi et al. (2014) revealed that all the bones had their foramina directed away

from the knee towards the lower ends of the bones.43

Gupta and Kumari (2014) in their study on nutrient foramina in 312

tibiae found that 300 bones had their foramina directed downwards following

the general rule of foramina of lower limb bones being directed away from the

knee. Three bones had their nutrient foramina directed upwards, towards the

knee.23

Oyedun (2014) reported that all but one of the 95 femora studied had

their foramina directed towards the proximal end. One bone had its foramen

directed anteriorly from the posterior surface of the bone.24

The architecture of nutrient foramina and the nutrient canals in the long

bones of upper and lower limbs analysed by Rao and Kothapalli (2014)

revealed that the direction of nutrient canal conformed to the general rule that

the nutrient canal runs towards the knee and away from the elbow and the

foramina were directed away from the growing end of the bone. The canals

which were directed upwards were more frequently seen in the lower half of

the shaft. They also reported that there was no change in the obliquity of the

canal with regard to position of the foramen in the shaft and that tibiae had

almost vertical nutrient canals.3

Shah and Saiyad (2014) reported that all the foramina in 200 radii were

directed towards the elbow, which confirmed the lower end of radius being its

growing end.25

30
Solanke et al. (2014) observed the direction of nutrient foramina in 100

humeri and 80 bones each of radii and ulnae and reported that all of the

foramina in these bones were directed towards the elbow without any

exception.26

Mazengenya and Fasemore (2015) studied the nutrient foramina in 360

bones each of femur, tibia and fibula and reported that all the femoral foramina

pointed away from the growing end. In the majority of the tibiae, the nutrient

foramina pointed away from the growing end while in 4 bones, they pointed

towards the growing end. They also reported one tibia with double foramina,

each one pointing away from each other. Among the fibulae studied, 15 bones

had foramina pointing towards the growing end and 9 bones had double

foramina, each pointing towards the opposite ends.44

Nidhi et al. (2015) reported from their study on the nutrient foramina in

160 fibulae that 88.88% were directed distally as per the growing end theory

and the rest were directed proximally towards the knee. They attributed this

variation to the change in the type of lower epiphysis of fibula after birth from

traction to pressure type.28

Poornima and Angadi (2015) observed in their study that all of the

foramina in the 100 femora that they studied were directed towards the upper

end of the bones, as per the growing end theory.29

Roul and Goyal (2015) studied the nutrient foramina in the longs bones

of upper limb and reported that the foramina were directed away from the elbow

31
and the nutrient canals were directed away from the growing end due to the

unequal growth of one end of the bone.2

Studies on the nutrient foramina in 188 tibiae by Vadhel et al. (2015)

revealed that all the foramina found in the bones were directed downwards

away from the knee.47

Asharani and Ningaiah (2016) from their study on the direction of

nutrient foramina in 120 humeri reported that all the foramina obeyed the

growing end theory in that all were directed towards the elbow away from the

growing end.32

Studies on the nutrient foramina of humeri carried out by Mansur et al.

(2016) showed that all of the foramina were directed towards the lower end of

the bone confirming the general proposition that nutrient foramina in the upper

limb long bones are directed towards the elbow joint.34

Sinha et al. (2016) studied the nutrient foramina in 100 fibulae and found

that all the foramina found in the bones were directed away from the knee

joint.35

Ashwini et al. (2017) reported from their study on the nutrient foramina

in 69 radii and 84 ulnae that all the foramina were directed towards the upper

ends of the bones (towards the elbow) thereby confirming the lower end of

radius and ulna to be the growing end.45

A study on the nutrient foramina in 151 tibiae by Kumar et al. (2017)

revealed that all bones had their foramina directed away from the knee towards

32
the lower end of the bones, except five bones, which had the foramina directed

upwards towards the knee.36

Priya and Janaki (2017) studied the nutrient foramina of 100 femora and

reported that all the foramina were directed upwards away from their knee

indicating the lower end of femur to be the growing end. Also, they studied the

nutrient foramina in 92 tibiae and found that all the bones with a single nutrient

foramen had their foramina directed downwards away from the knee. Ten of

the bones had double nutrient foramina, of which 40% of the foramina were

directed upwards towards the knee.38,39

Veeramuthu et al. (2017) in their study on the nutrient foramina in 55

humeri, 59 radii and 59 ulnae reported that all of the bones had their foramina

directed away from the growing end, towards the elbow, thereby obeying the

growing end theory.40

5) OBLIQUITY OF NUTRIENT CANALS

Humphry (1861) explained the reasons for the unequal growth at the two

ends of a long bone and has reported that the obliquity of the nutrient canal in

the bones is due to this unequal growth.48

Digby (1916) observed that though the bone growth was faster at one

end, the blood vessel which gives off the nutrient artery grows uniformly

throughout its length and that the nutrient canal was directed towards the older

part of the shaft of the bone.49

33
Payton (1934) stated that the obliquity of the nutrient canal decreases

with the advancing age of the bone and the change in the obliquity is associated

with the lengthening rather than shortening of the nutrient canal.50

Mysorekar (1967) reported from his study on the obliquity of nutrient

foramina in long bones that the obliquity of the nutrient canal remained fairly

constant irrespective of the nutrient foramen being in the centre or near the ends

of the bone.12 In 1980, Longia et al. also observed similar findings in their

study.5

34
MATERIALS AND METHODS
MATERIALS AND METHODS

A) Source of data

The present study was done on dry long bones of upper limb and lower

limb available in the Department of Anatomy, Sree Mookambika

Institute of Medical Sciences, Kulasekharam, Kanyakumari District.

B) Study duration

One and a half years - From January 2017 to June 2018.

C) Study design

Cross sectional study.

D) Study sample

Sample size and groups

210 dry long bones consisting of 105 bones each from upper and lower

limbs, divided into 6 groups having 35 bones in each group.

1st group - 35 humeri

2nd group - 35 radii

3rd group - 35 ulnae

4th group - 35 femora

5th group - 35 tibiae

6th group - 35 fibulae

35
Sample size calculation
4pq
Sample size was calculated using the following formula. n =
d2

where, p = percentage of foramina with foraminal index < 33.33,

in tibia = 80, as per the study “Diaphyseal nutrient foramina in human

long bones” done by Mysorekar in 1967.12

q = 100-p = 100-80 = 20

d = 20% of p = 16

n = 25

Minimum required sample size for each group was 25. I took a sample

size of 35 for each group.

E) Study Population

i) Inclusion criteria

Long bones of upper limb and lower limb of all ages belonging

to either sex and both sides (right and left).

ii) Exclusion criteria

Bones with gross deformity.

F) Study Variables

To study the

a) Number of nutrient foramina.

36
b) Position of the nutrient foramina in the various surfaces and borders

of the shaft of the bone and the location of the foramina based on the

foraminal index.

c) Size of the nutrient foramina.

d) Direction of the nutrient foramina and obliquity of the nutrient

canals.

G) Data Collection

i) Materials used (fig. 1)

a) Hand lens

b) Osteometric board

c) Sliding caliper

d) 24-gauge hypodermic needle

e) A fine stiff wire

ii) Procedure in detail

Bones were collected from the Department of Anatomy, Sree

Mookambika Institute of Medical Sciences, Kulasekharam. All the

bones selected were intact with no gross deformities. The side of the

bones (right or left) was determined. The data regarding age and sex of

the bones were not available.

37
A hand lens was used to identify the nutrient foramina. They were

identified by the raised margins surrounding the foramina and by the

distinct groove leading to them.5

Only those foramina which were well defined and present in the shaft

of the bones were taken for the study. Those that were present at the ends

of the bone were ignored. In case of a doubt regarding the identification

of a foramen, a fine stiff wire was used to confirm the foramen leading

into the medullary cavity.12

All the parameters mentioned above were studied in each bone as

mentioned below.

a) Number of Nutrient Foramina (fig. 2)

The number of nutrient foramina present in each bone was identified

using a hand lens.5

b) Position of Nutrient Foramina

The position of the nutrient foramina with respect to the different

aspects of the shaft of the bone as given in Gray’s Anatomy textbook

was examined.1 The foramina lying within 1mm from a border of a bone

was taken to be lying on that border.12,15

The distribution of the foramina with respect to the upper, middle

and lower thirds of different aspects of the shaft of the bones was arrived

38
Fig. 1 – Materials used.

Fig. 2 – Identifying and counting the nutrient foramina.


at by calculating the foramina index (FI) using the formula given

below.46,51

FI = (DNF/TL) × 100

where, DNF = the distance of the nutrient foramen from the proximal

end of the bone, measured with an Inox Sliding caliper.14 (fig. 4)

TL = total length of the bone.

In case of presence of multiple foramina in the same aspect of the

shaft, the distance of the proximal dominant foramen (proximal

secondary foramen in case of no dominant foramen) from the proximal

end of the bone was used for calculating the foraminal index.24

Determination of the total length of the bone (fig. 3)

This was done using an Osteometric board and the bony points used for

measuring the length of bones in each group are mentioned below.8,14

i) Humerus - Superior aspect of head

Most distal aspect of trochlea

ii) Radius - Most proximal aspect of head

Tip of radial styloid process

iii) Ulna - Most proximal aspect of olecranon

Tip of ulnar styloid process

iv) Femur - Superior aspect of head

Most distal aspect of medial condyle

39
Fig. 3 – Measuring the length of the bone for calculating FI.

Fig. 4 – Measuring the distance of nutrient foramen from the proximal end of bone for
calculating FI.
v) Tibia - Superior margin of medial condyle

Distal aspect of medial malleolus

vi) Fibula - Apex of head

Distal aspect of lateral malleolus

Distribution of nutrient foramina according to FI

The position of nutrient foramina was grouped into three according to

the foraminal index as follows.12,40,52

Type I : FI ≤ 33.33 → foramen in proximal third of shaft

Type II : FI > 33.33 & ≤ 66.66 → foramen in middle third of shaft

Type III : FI > 66.66 → foramen in distal third of shaft

c) Size of Nutrient Foramina (fig. 5)

A 24-gauge hypodermic needle (0.56 mm in diameter) was used to

classify the nutrient foramina into dominant and secondary foramina.

The foramina through which this needle could be passed were classified

as dominant foramina while those through which this needle could not

be passed were classified as secondary foramina.6,8

d) Direction of Nutrient Foramina and Obliquity of Nutrient

Canals (fig. 6)

A fine stiff wire was used to find the direction of nutrient foramina

and the obliquity of the nutrient canals running from the foramina.53

40
Dominant Foramen

Secondary Foramen

Fig. 5 – Dominant and secondary foramina classified using a 24-gauge needle.

Fig. 6 – Finding the direction of nutrient foramen and obliquity of nutrient canal using
a fine stiff wire.
The direction was categorised as one of the below:3,12

i) Upwards

ii) Downwards

The obliquity of the canals was grossly examined and described with

respect to the difference between obliquity of the nutrient canals present

near the middle of the shaft of the bones and the obliquity of canals

present near the ends of the bones.5,12

e) Photographs

A Nikon digital camera (16 mega pixels) was used to take the

photographs.

f) Statistical Analysis

The results were tabulated and analysed using Microsoft Excel

software for windows. The range, mean and standard deviation of the FI

were calculated. The difference in the length wise distribution of the

foramina on the shaft of the bones between the right and left sides was

analysed for each group using the Student’s t-test for unequal variances

with a level of significance 0.05. The association between the size of the

foramina and the side of the bones was tested using the chi-square test,

the level of significance being taken as 0.05. The dependence of the size

of the foramina, on the bone being part of the upper or lower extremity,

41
was also analysed using the chi-square test, taking 0.05 as the level of

significance.

H) Ethical Issues

The study was conducted after obtaining the certificate for ethical

clearance from the Institutional Human Ethics Committee, Sree

Mookambika Institute of Medical Sciences, Kulasekharam.

42
RESULTS
RESULTS

Measurements were made on adult long bones from both right & left sides

and irrespective of age and sex. The observations of the present study are

documented under the following headings.

1) Number of nutrient foramina

2) Position of the nutrient foramina on the different surfaces and borders

of the shaft of long bones

3) Location of the nutrient foramina based on the foraminal index

4) Size of the nutrient foramina

5) Direction of the nutrient foramina

6) Obliquity of the nutrient canals

7) Statistical Tests

1) Number of nutrient foramina

Humerus (Table 1)

Out of 35 bones studied, single foramen was found in maximum number of

bones (60%). Double foramina were seen in 37.14% of the bones. A maximum

of 3 (2.86%) nutrient foramina were observed in one humerus. (fig. 7)

Radius (Table 1)

Three bones out of the 35 studied no nutrient foramen on the surface of

shaft. The rest of the bones had a single foramen each. (fig. 8)

43
AMS

Fig. 7 – Humeri showing single, double and triple foramina. The bone with the single
foramen has a dominant foramen in the anteromedial surface, in the middle third of the
shaft. The bone with triple foramina shows two secondary foramina.
AS

Fig. 8 – Radius showing a single dominant nutrient foramen in the middle third of the
anterior surface of the shaft.

AS

Fig. 9 – Ulnae showing single and double nutrient foramina. The bone with double
foramina has two secondary foramina in the anterior surface, one in the upper third and
the other in the middle third of the bone. The bone with the single foramen has a
dominant foramen.
Ulna (Table 1)

The majority of the bones (94.29%) showed a single nutrient foramen. In

two cases, double foramina were observed. (fig. 9)

Table 1

Number of nutrient foramina observed in the long bones of upper limb

Number of Number of Percentage (%)


Bone
Bones Foramina of bones

21 Single 60

Humerus (n=35) 13 Double 37.14

1 Triple 2.86

32 Single 91.43
Radius (n=35)
3 Absent 8.57

33 Single 94.29

Ulna (n=35)
2 Double 5.71

Femur (Table 2)

Two of the femora studied showed triple foramina whereas the rest had

single foramen in 45.72% and double foramina in 48.57% of bones.

(figs. 12 & 13)

44
Fig. 10 – Radius showing a secondary foramen in its anterior surface.

Humerus

Radius

Ulna

Fig. 11 – Direction of nutrient foramen and obliquity of nutrient canal in upper limb
long bones. The foramina are directed downwards in the humerus, upwards in the radius
and ulna, all directed towards the elbow. The radius has its foramen in the upper third
of the shaft.
LA

Fig. 12 – Femora having single, double and triple foramina. The first bone has a single,
dominant foramen in the linea aspera in the upper third of the shaft. The second bone
has double foramina in the middle third of the shaft, the upper one secondary in size
and the lower foramen present in the medial lip of linea aspera. The third bone shows
triple foramina. All the foramina are directed towards the upper end of the bones, away
from the knee.

Fig. 13 – Femur showing a single secondary foramen in the linea aspera.


Tibia (Table 2)

All the 35 tibiae studied had a single nutrient foramen. (fig. 14)

Fibula (Table 2)

Nutrient foramen was absent in only one fibula and the remaining 34 fibulae

had single foramen. (fig. 16)

Table 2

Number of nutrient foramina observed in the long bones of lower limb

Number of Number of Percentage (%)


Bone
Bones Foramina of bones

16 Single 45.72

Femur (n=35) 17 Double 48.57

2 Triple 5.71

Tibia (n=35) 35 Single 100

29 Single 82.86

Fibula (n=35) 5 Double 14.28

1 Absent 2.86

45
PS

Fig. 14 – Tibiae showing single dominant and secondary foramina in the first & second
bones respectively. The dominant foramen is present in the upper third of the bone in
the posterior surface, directed downwards. The secondary foramen is present in the
middle third of the bone.

Fig. 15 – A variant tibia with an anteriorly directed single secondary nutrient foramen.
MC

PS

Fig. 16 – Fibulae showing single dominant foramen, single secondary foramen and
double foramina in the first, second and third bones respectively. The first bone has the
foramen in the lower third of the bone and the second bone has the foramen in the upper
third of the bone. The third bone has both the foramina in the middle third of the bone,
the proximal secondary foramen in medial crest of posterior surface directed
downwards and the distal dominant foramen directed upwards.
2) Position of the nutrient foramina on the different surfaces and borders

of the shaft of long bones

Humerus (Table 3)

The majority of the foramina (64%) were present on the antero-medial

surface of the shaft of the humerus (fig. 7). The next higher proportion of

foramina (14%) was found in the medial border of the shaft. Five foramina were

present in the posterior surface of the shaft of numerus. It was found that, in

majority of bones, the position of nutrient foramen was closer to or at medial

border, rather than lateral border or closer to it.

Table 3

Position of nutrient foramina on different surfaces and borders of the shaft of


humeri

Number of Percentage
Position
Foramina (%)
Medial border 7 14

Lateral border 5 10
Antero-medial surface – near medial
26 52
border
Antero-medial surface – near anterior
2 4
border
Antero-medial surface – midway
4 8
between anterior and medial borders
Antero-lateral surface – near lateral
1 2
border
Posterior surface – near medial border 1 2

Posterior surface – near lateral border 3 6


Posterior surface – in the spiral groove,
1 2
near the lateral border

46
Radius (Table 4)

All the foramina were present on the anterior aspect of the shaft of the bones.

Anterior surface, specifically midway between anterior and interosseous

borders showed maximum number of foramina (34.8%). Anterior surface, close

to anterior border showed foramina in 28.12% of the bones and close to

interosseous border in 25%. Anterior and interosseous borders each had

foramina in 6.25% of the bones. (fig. 10)

Table 4

Position of nutrient foramina on different surfaces and borders of the shaft of


radii

Number of Percentage
Position
Foramina (%)

Anterior border 2 6.25

Interosseous border 2 6.25

Anterior surface – near anterior border 9 28.12

Anterior surface – near interosseous


8 25
border

Anterior surface – midway between


11 34.38
anterior and interosseous borders

47
Ulna (Table 5)

Almost all the foramina (97.3%) were present in the anterior aspect of the

shaft of the ulna, the majority of which were present near the anterior border.

(fig. 9)

Table 5

Position of nutrient foramina on different surfaces and borders of the shaft of


ulnae

Number of Percentage
Position
Foramina (%)

Interosseous border 1 2.7

Anterior surface – near anterior border 15 40.54

Anterior surface – near interosseous border 12 32.43

Anterior surface – midway between anterior


9 24.33
and interosseous borders

48
Femur (Table 6)

Femora had all the foramina on the posterior aspect of the bones. Linea

aspera showed the greatest number (68%) of nutrient foramina distributed

among its medial and lateral lips, and the area between them. (fig. 12)

Table 6

Position of nutrient foramina in different surfaces of the shaft of femora

Number of Percentage
Position
Foramina (%)

Posterior border – medial lip of linea


16 28.57
aspera

Posterior border – lateral lip of linea


6 10.71
aspera

Posterior border – between the lips of


16 28.57
linea aspera

Medial Surface 15 26.79

Lateral Surface 3 5.36

49
Tibia (Table 7)

In tibiae, the posterior surface had the maximum number of foramina (97%).

The majority of the nutrient foramina on the posterior surface were present near

the lateral border (37.14%), and between the lateral border and the soleal line

(37.14%). (fig. 14)

Table 7

Position of nutrient foramina in different surfaces of the shaft of tibiae

Number of Percentage
Position
Foramina (%)

Lateral Border 1 2.86

Posterior surface – near lateral border 13 37.14

Posterior surface – near medial border 2 5.71

Posterior surface – between lateral


13 37.14
border and soleal line

Posterior surface – near soleal line,


4 11.44
lateral to it

Posterior surface – on the soleal line 2 5.71

50
Fibula (Table 8)

Fibulae had 92% of the foramina on the posterior surface, the majority of

which were on the medial crest. The rest of the foramina were present on the

interosseous border of fibula. (fig. 16)

Table 8

Position of nutrient foramina in different surfaces of the shaft of fibulae

Number of Percentage
Position
Foramina (%)

Interosseous border 3 7.69

Posterior surface – on the medial crest 22 56.41

Posterior surface – between medial crest and


7 17.95
posterior border – near medial crest

Posterior surface – midway between medial


2 5.2
crest and interosseous border

Posterior surface – between medial crest and


1 2.55
interosseous border – near medial crest

Posterior surface - between medial crest and


1 2.55
interosseous border – near interosseous border

Posterior surface – midway between


1 2.55
interosseous and posterior borders

Lateral surface 1 2.55

Medial surface 1 2.55

51
3) Location of the nutrient foramina based on the foraminal index

The shaft of a long bones was divided into three parts (upper third,

middle third and lower third) based on the foraminal index, and the distribution

of foramina in these three parts was noted.

Humerus (Tables 9 & 10)

All the bones had their foramina in the middle third of the shaft (Type II)

with foraminal index ranging from 38.96 to 65.73. The mean foraminal index

was 52.63. (fig. 7)

Radius (Tables 9 & 10)

Among radii, 54.29% (Type I) and 37.14% (Type II) of the bones had their

foramina in the upper and middle thirds of the bones respectively. The

foraminal index ranged between 26.38 and 46.33, with a mean FI of 33.33.

(figs. 8 & 11)

Ulna (Tables 9 & 10)

The greatest number of bones (21) had their foramina in the middle third of

the shaft of the bones. The foramina index ranged between 27.13 and 45.49,

with a mean foraminal index of 35.14. (fig. 9)

The range and mean foraminal index with standard deviation for different

surface and borders of the upper limb long bones are given in the tables 11, 12

and 13.

52
Table 9

Location of nutrient foramina in the long bones of upper limb based on


foraminal index

Position (% of bones)
Bone
Type I Type II Type III
(Upper third) (Middle third) (Lower third)

Humerus - 100 -

Radius 54.29 37.14 -

Ulna 40 60 -

Table 10

Range and mean with standard deviation of the foraminal indices of the upper
limb long bones

Foraminal Index
Bone
Range Mean ± S.D.

Humerus 38.96 – 65.73 52.63 ± 6.27

Radius 26.38 – 46.33 33.33 ± 4.74

Ulna 27.13 – 45.49 35.14 ± 4.86

53
Table 11

Range and mean with standard deviation of foraminal indices of humeri with
respect to individual surfaces and borders of the shaft of the bones

Position Range Mean ± S.D.

Medial border 49.69 – 72.15 60.62 ± 8.09

Lateral border 39.44 – 53.27 44.19 ± 5.50

Antero-medial surface – near


50.87 – 66.37 56.90 ± 4.37
medial border

Antero-medial surface – near 54.23


54.77 ± 0.76
anterior border 55.31

Antero-medial surface –
midway between anterior and 55.48 – 62.06 58.79 ± 2.69
medial borders

Antero-lateral surface – near


15 -
lateral border

Posterior surface – near


9.6 -
medial border

Posterior surface – near lateral


43.38 – 46.44 44.47 ± 1.71
border

Posterior surface – in the


spiral groove, near the lateral 12.7 -
border

54
Table 12

Range and mean with standard deviation of foraminal indices of radii with
respect to individual surfaces and borders of the shaft of the bones

Position Range Mean ± S.D.

29.87
Anterior border 32.52 ± 3.75
35.17
36.07
Interosseous border 38.60 ± 3.58
41.13
Anterior surface – near anterior
26.38 – 37.44 31.25 ± 3.45
border
Anterior surface – near
30.68 – 42.23 35.53 ± 4.25
interosseous border
Anterior surface – midway
between anterior and interosseous 28.4 – 46.33 32.61 ± 5.54
borders

Table 13

Range and mean with standard deviation of foraminal indices of ulnae with
respect to individual surfaces and borders of the shaft of the bones

Position Range Mean ± S.D.

Interosseous border 37.75 -

Anterior surface – near


27.13 – 38.66 31.81 ± 3.07
anterior border
Anterior surface – near
34.60 – 47.24 40.03 ± 3.73
interosseous border
Anterior surface – midway
between anterior and 28.91 – 42.59 35.65 ± 5.20
interosseous borders

55
Femur (Tables 14 & 15)

Among the femora, 86% of the bones had their foramina in the middle third

of the shaft of the bone, while the rest had them in their upper third. The

foraminal index range between 27.29 and 60, with a mean of 40.78. (fig. 12)

Tibia (Tables 14 & 15)

Eighty percent of the bones had their foramina in the upper third of the shaft

of the bone and the rest had them in the lower third. The range of the foraminal

index was between 26.75 and 50.35. The mean foraminal index was found to

be 31.95. (fig. 14)

Fibula (Tables 14 & 15)

The majority of the fibulae had their foramina in the middle third of the

shaft of the bone, with a few bones having them in the upper and lower thirds.

The mean foraminal index was found to be 43.95 with a range between 28.86

and 67.12. (fig. 16)

The range and mean foraminal index with standard deviation for different

surface and borders of the lower limb long bones are given in the tables 16, 17

and 18.

56
Table 14

Location of nutrient foramina in the long bones of lower limb based on


foraminal index

Position (% of bones)
Bone
Type I Type II Type III
(Upper third) (Middle third) (Lower third)

Femur 14.29 85.71 -

Tibia 80 20 -

Fibula 8.57 85.71 2.86

Table 15

Range and mean with standard deviation of the foraminal indices of the lower
limb long bones

Foraminal Index
Bone
Range Mean ± S.D.

Femur 27.29 – 60 40.78 ± 9.08

Tibia 26.75 – 50.35 31.95 ± 5.24

Fibula 28.86 – 67.12 43.95 ± 10.09

57
Table 16

Range and mean with standard deviation of foraminal indices of femora with
respect to individual surfaces and borders of the shaft of the bones

Position Range Mean ± S.D.

Medial lip of linea aspera 32.70 – 64.77 49.07 ± 10.23

Lateral lip of linea aspera 31.63 – 48.83 37.72 ± 5.79

Between the lips of linea


27.29 – 48 35.52 ± 4.40
aspera

Medial Surface 27.37 – 66.53 51.37 ± 10.21

Lateral Surface 41.92 – 45.68 44.38 ± 2.13

58
Table 17

Range and mean with standard deviation of foraminal indices of tibiae with
respect to individual surfaces and borders of the shaft of the bones

Position Range Mean ± S.D.

Lateral Border 48.5 -

Posterior surface – near


26.75 – 41.94 31.89 ± 3.76
lateral border

Posterior surface – near 29.6


39.97 ± 14.67
medial border 50.35

Posterior surface – between


lateral border and soleal 27.73 – 33 30.80 ± 1.45
line

Posterior surface – near


26.82 – 35.25 30.20 ± 3.60
soleal line, lateral to it

Posterior surface – on the 26.75


26.89 ± 0.20
soleal line 27.03

59
Table 18

Range and mean with standard deviation of foraminal indices of fibulae with
respect to individual surfaces and borders of the shaft of the bones

Position Range Mean ± S.D.

Interosseous border 64.60 – 67.12 66.02 ± 1.29

Posterior surface – on the


31.48 – 61.54 40.38 ± 6.89
medial crest

Posterior surface – between


medial crest and posterior 36.95 – 56.41 47.65 ± 7.66
border – near medial crest

Posterior surface – midway


51.99
between medial crest and 57.12 ± 7.26
62.26
interosseous border
Posterior surface – between
medial crest and
50.98 -
interosseous border – near
medial crest
Posterior surface - between
medial crest and
28.86 -
interosseous border – near
interosseous border
Posterior surface – midway
between interosseous and 59.61 -
posterior borders

Lateral surface 56.45 -

Medial surface 63.35 -

60
4) Size of the nutrient foramina

Humerus (Table 19)

The majority of the foramina in humeri were secondary foramina (size <

0.56mm diameter) and a sole secondary foramen was found in 8 bones. Ten out

of the thirteen bones with double foramina had only secondary foramina. In one

of the bones with double foramina, both were of the dominant type (size ≥

0.56mm diameter) and in two bones with double foramina, one was dominant

and the other was secondary. In the humerus with triple foramina, one foramen

was of the dominant type and the other two were of secondary type. Thirteen

bones had a single dominant nutrient foramen. (fig. 7)

Radius (Table 19)

Among the 35 radii studied, 19 bones had a single dominant foramen and

13 bones had a single secondary foramen, with the remaining three not showing

any nutrient foramen. (figs. 8 & 10)

Ulna (Table 19)

Among the 37 nutrient foramina, 20 were of the dominant type and the

remaining foramina were of secondary type. In the two bones with double

foramina, all the foramina were secondary in size. (fig. 9)

61
Table 19

Size of nutrient foramina of the upper limb long bones

Size of Foramen

Bone Dominant Secondary


Percentage Percentage
Number Number
(%) (%)

Humerus 18 36 32 64

Radius 19 59.38 13 40.62

Ulna 20 54.05 17 45.95

Femur (Table 20)

In femora, 44 of the 56 nutrient foramina were dominant and the rest were

secondary in size. Among the bones with a single nutrient foramen, only one

had a secondary foramen (in the medial lip of linea aspera). Seventeen bones

had double foramina of which 9 bones had double dominant foramina and the

rest had one dominant and one secondary foramen each. Of the two bones with

triple foramina, one bone had two dominant and one secondary foramen and

the other bone had one dominant and two secondary foramina. (figs. 12 & 13)

62
Tibia (Table 20)

Tibiae showed a single dominant nutrient foramen in 31 bones and a single

secondary nutrient foramen in 4 bones. (fig. 14)

Fibula (Table 20)

Among the 29 fibulae having single nutrient foramen each, a dominant

foramen was observed in 7 bones and the rest had secondary foramina. Out of

the five bones which showed double foramina, 4 bones had double secondary

foramina and one bone had one dominant and one secondary foramina. (fig. 16)

Table 20

Size of nutrient foramina of the lower limb long bones

Size of Foramen

Bone Dominant Secondary


Percentage Percentage
Number Number
(%) (%)

Femur 44 78.57 12 21.43

Tibia 31 88.57 4 11.43

Fibula 8 20.51 31 79.49

63
5) Direction of the nutrient foramina

The direction of the nutrient foramina in the long bones of upper and limbs

are given in tables 21 & 22 respectively, and shown in figs. 11, 12, 14 & 16.

In tibiae one bone had its foramen directed anteriorly, from the posterior

aspect (fig. 15). In fibulae, 8 bones had foramina which were directed upwards

and 26 bones had them directed downwards.

6) Obliquity of the nutrient canals

The observations noted about the obliquity of the nutrient canals in the long

bones of upper and lower limbs are given in tables 21 & 22 respectively and in

figures 11, 12, 14 & 16. All the bones studied had nutrient canals which were

uniformly oblique irrespective of the part of the bone where they were found

except one foramen in the tibia which was nearly horizontal (fig. 15).

Table 21

Direction of nutrient foramina and obliquity of nutrient canals of the upper limb
long bones

Bone Direction Obliquity

Humerus Downward Uniformly oblique

Radius Upward Uniformly oblique

Ulna Upward Uniformly oblique

64
Table 22

Direction of nutrient foramina and obliquity of nutrient canals of the lower limb
long bones

Bone Direction Obliquity

Femur Upward Uniformly oblique

Uniformly oblique
except one canal
Tibia Downward
which was nearly
horizontal

Downward – 31 foramina
Fibula Uniformly oblique
Upward – 8 foramina

7) Statistical tests

A significant difference between the two sides of bones was not noted in the

length-wise location of nutrient foramina, in the student’s t-test done on the

foraminal indices of the bones. The ‘t’ and ‘p’ values of the test are given in

table 23.

65
Table 23

Results of the Student’s t-test – ‘t’ & ‘p’ values, and inference

Bone t-value p-value Inference

No difference
in location of
Humerus -1.37 0.09 foramina
between the
two sides
No difference
in location of
Radius 0.96 0.17 foramina
between the
two sides
No difference
in location of
Ulna 0.58 0.28 foramina
between the
two sides
No difference
in location of
Femur 1.13 0.13 foramina
between the
two sides
No difference
in location of
Tibia 0.32 0.37 foramina
between the
two sides
No difference
in location of
Fibula 0.07 0.47 foramina
between the
two sides
Level of significance is p < 0.05

66
The association of the size of the foramina with the side of the bones was

tested with the chi-square test and it was found that there was no significant

association between the two, the p-value being 0.33. The chi-square statistic

obtained was 0.94. The contingency table for the test is given as table 24.

Table 24

Contingency table for the chi-square test to test association between the size of
the foramina and the side of the bones

Marginal row
Right side Left side
totals

Dominant foramina 78 62 140

Secondary foramina 54 55 109

Marginal column
132 117 249 (Grand total)
totals

The chi-square test was used again to check if the size of the nutrient

foramen was influenced by the bone being a part of the upper extremity or the

lower extremity and the test results showed that there was a dependence of the

size of the nutrient foramina on the nature of the bones being present in the

upper limb or lower limb. Dominant foramina were more common in the lower

limb long bones, while secondary foramina were more frequent in the upper

limb long bones. The chi-square statistic obtained was 6.42 with a p-value of

0.01. The contingency table for this test is given as table 25.

67
Table 25

Contingency table for the chi-square test to test association between the size of
the foramina and bones being present in the upper or lower limbs

Marginal row
Upper Limb Lower Limb
totals

Dominant foramina 57 83 140

Secondary foramina 62 47 109

Marginal column
119 130 249 (Grand total)
totals

68
DISCUSSION
DISCUSSION

The results of this study are discussed under the following headings

1) Number of nutrient foramina

2) Position of the nutrient foramina in the various surfaces and borders of the

bones and the location of the foramina based on the foraminal indices

3) Size of the nutrient foramina

4) Direction of the nutrient foramina and Obliquity of the nutrient canals

5) Clinical importance

1) Number of nutrient foramina

Humerus

In the present study done on 35 humeri, a single nutrient foramen was

the commonest (60%) and triple foramina in least number (2.86%). This

distribution is in confirmation with previous studies. Double foramina were

seen in 13 bones (37.14%). These have been found in other studies as shown in

review of literature.

Carroll in his study on 71 humeri had found that 48 bones (67.6%) had

a single nutrient foramen, 20 bones (28.2%) had double foramina and 3 bones

(4.2%) had triple foramina.11 Mysorekar had reported from his study on 180

humeri that 104 bones (57.8%) had a single nutrient foramen, 68 bones (37.8%)

had double foramina, 5 bones (2.8%) had triple foramina and 2 bones (1.1%)

69
had quadruple foramina.12 Kizilkanat et al. had reported 69 bones (68.3%) with

a single foramen, 22 bones (21.8%) with double foramina, 7 bones (6.9%) with

triple foramina and 1 bone (0.99%) with quadruple foramina, out of a total 101

humeri that they studied.8 The present study did not find any bones with

quadruple foramina.

A higher percentage of bones with single nutrient foramen was found by

Longia et al. (85% of 200 bones), Murlimanju et al. (93.8% of 96 bones),

Pereira et al. (88.5% of 174 bones), Solanke et al. (92 out of 100 bones), Roul

and Goyal (94.6% of 37 bones), Asharani and Ningaiah (87% of 120 bones)

and Veeramuthu et al. (83.6% of 55 bones).2,5,20,21,26,32,40

Humerus without a nutrient foramen was not observed in the present

study but it was reported by previous authors, and the authors stated that the

periosteal blood vessels contributed entirely to the blood supply of the

bones.5,20,22,26,32

Radius

Absence of nutrient foramen was noted in 8.57% on the 35 radii in the

present study. This observation was similar to previous authors. Mysorekar

noted 2.2% and Murlimanju et al. observed 4.2% bones without a nutrient

foramen.12,20 Solanke et al. and Ukoha et al. also reported absence of nutrient

foramina in the radii under their study.22,26 Single nutrient foramen was the

commonest in radii also in the present study, in confirmation with previous

studies. Campos et al. had found that all of the 37 radii they studied had a single

70
nutrient foramen.14 A quite different observation in the present study was the

absence of double foramina.

Ulna

In agreement with previous studies, majority of ulnae presenting with a

single nutrient foramen (94.29%) was observed in present study, with

remaining bones having double foramina.

Mysorekar in his study on 180 ulnae had found that 168 bones (93.3%)

had a single nutrient foramen.12 Longia et al. had reported that 95% of the 200

bones had a single foramen.5 Campos et al. had observed a single nutrient

foramen in 91% of the 33 bones studied.14 Solanke et al. reported a single

nutrient foramen in 77 (96.25%) of the 80 ulnae studied and Veeramuthu et al.

found a single foramen in 57 bones (96.6%) of the total 59 ulnae studied.26,40

Kizilkanat et al. reported a single nutrient foramen in all except one of the 102

ulnae studied.8 Murlimanju et al. and Roul & Goyal had found that all of the 75

and 37 ulnae they had studied respectively displayed a single nutrient

foramen.2,20 Ukoha et al. reported 78% of the 50 ulnae they had studied to have

a single nutrient foramen and the rest not showing any foramen.22

Ulnae without a nutrient foramen have also been reported in their

respective studies by Mysorekar (2 bones), Solanke et al. (3 bones) and

Veeramuthu et al. (1 bone).12,26,40 The present study revealed at least one

foramen in all the bones studied.

71
Regarding bones with double nutrient foramina, the present study found

2 bones (5.71%) with double foramina. Mysorekar in his study had found 10

bones (5.56%) with double foramina, with Campos et al. finding 9% in their

study.12,14 Longia et al. reported 4% of the bones in their study to have double

foramina.5

Absence of foramen and presence of triple foramina were not noted in

the present study. This observation is similar to previous studies except in the

study of Longia et al. who noticed triple foramina in 1% of the bones.5

Femur

The present study found at least one nutrient foramen in all of the bones

studied. Many authors reported that a maximum of three nutrient foramina were

present in femora.10,12,14,16,18,19,38 The present study results were similar in

finding a maximum of three foramina in femora.

Quadruple foramina were reported by a few studies.5,6,15 The present

study did not find any. However, Sendemir and Cimen reported from their

study on 102 femora that three bones respectively had 6, 8 and 9 foramina,

while Gumusburun et al. reported two bones having 5 and 6 foramina

respectively, out of a total of 103 femora that they studied.6,15

As with the long bones of upper limb, predominant occurrence of single

foramen was not observed in present study and most of the previous studies in

literature.

72
In the present study comprising of 35 femora, single, double and triple

nutrient foramina were found in 16 bones (45.7%), 17 bones (48.6%) and 2

bones (5.7%) respectively. Seema et al. in their study on 60 femora found

single, double and triple foramina in 29 (48.33%), 29 (48.33%) and 2 bones

(3.33%) respectively.31 Kirchner et al. reported from their study on 200 femora

that 35% of the bones had a single nutrient foramen, 57% had double foramina

and 8% had triple foramina.18 Longia et al. observed from their study on 200

femora that 69.5% of the bones had a single nutrient foramen, 26.5% had

double foramina and 3% had triple foramina.5

Femora without a nutrient foramen were reported by Mysorekar (6 out

of 180 bones studied), Bridgeman & Brookes (3 out of 109 femora studied),

Al-Motabagani (3% of 130 bones studied) and Mansur et al. (5 out of 253

femora studied),12,16,19,34 while the present study didn’t find any.

Tibia

All of the 35 tibiae analysed in this study showed a single nutrient

foramen.

This observation corresponded with that of the study by Jayaprakash (on

50 tibiae), which reported 100% of the bones having a single nutrient

foramen.33

Mysorekar in his study on 180 tibiae had found 178 bones (98.9%) to

have a single foramen and 2 bones (1.1%) with double foramina.12 Pereira et

al. had reported 98.6% of the 142 tibiae that they studied to have a single

73
nutrient foramen and 1.4% of bones having double foramina.21 Kizilkanat et al.

confirmed the presence of a single nutrient foramen in 98 of the 100 tibiae that

they studied, with the rest having double foramina.8 Tibiae with triple nutrient

foramina were reported by Gumusburun et al. who found 2.8% of the 106 tibiae

that they studied to have triple foramina, and Kumar et al. finding triple

foramina in 2 out of the total 151 bones that they studied.15,42 Tibiae without a

nutrient foramen were reported by Gupta & Kumari (3.2% of 312 bones) and

Gumusburun et al. (in 0.9% of the bones).15,23

Fibula

In the present study a single nutrient foramen was the most frequent in

fibulae (82.86%). Fibulae had double foramina in 5 bones (14.28%), with no

foramen seen in 1 bone (2.86%).

Gumusburun et al. reported from their study on 60 fibulae found that

85% of the bones had a single nutrient foramen, 12% had double foramina and

3% had triple foramina.15 Roul & Goyal in their study on 37 fibulae observed

that 81.08% of the bones had a single nutrient foramen and 18.92% had double

foramina.30 Seema et al. observed that 50 (83.33%) of the 60 bones they studied

had a single nutrient foramen with the rest showing double foramina.31 Sinha

et al. had reported that 78 of the 100 fibulae that they studied had a single

nutrient foramen and the remaining 22 bones had double foramina.35 Campos

et al. in their study on 33 fibulae reported all of the bones to have a single

nutrient foramen.14 Mysorekar found 3.9% of the 180 fibulae studied with no

74
Humerus
100

Percentage of bones
80
60
40
20
0
Present study (35 Carroll (71 bones) Mysorekar (180 Kizilkanat et al.
bones) bones) (101 bones)
Studies

Single foramen Double foramina Triple Foramina

Radius
100
Percentage of bones

98
96
94
92
90
88
86
Present study (35 Mysorekar (180 Murlimanju et al. Solanke et al. (80
bones) bones) (72 bones) bones)
Studies

Single foramen Double foramina None

Ulna
100
Percentage of bones

98
96
94
92
90
88
86
Present study (35 Mysorekar (180 Longia et al. (200 Campos et al. (33
bones) bones) bones) bones)
Studies

Single foramen Double foramina None

Fig. 17 – Bar chart showing comparison of number of nutrient foramina in


upper limb long bones between different studies.
Femur
100

Percentage of bones
80
60
40
20
0
Present study (35 Seema et al. (60 Kirschner et al. Longia et al. (200
bones) bones) (200 bones) bones)
Studies

Single foramen Double foramina Triple Foramina

Tibia
100
Percentage of bones

99.5
99
98.5
98
97.5
Present study (35 Jayaprakash (50 Mysorekar (180 Pereira et al. (142
bones) bones) bones) bones)
Studies

Single foramen Double foramina

Fibula
100
Percentage of bones

80
60
40
20
0
Present study (35 Roul & Goyal (37 Seema et al. (60 Sinha et al. (100
bones) bones) bones) bones)
Studies

Single foramen Double foramina None

Fig. 18 – Bar chart showing comparison of number of nutrient foramina in


lower limb long bones between different studies.
nutrient foramen and Kizilkanat et al. found that only one bone (1.37%) out of

the 73 fibulae they studied was without nutrient foramen.8,12

A graphical comparison of the number of nutrient foramina in the long

bones of upper and lower limbs between different studies is given in figs. 17 &

18.

2) Position of the foramina on the various surfaces and borders of the

bones and the location of the foramina based on the foraminal indices

The knowledge of the accurate position of nutrient foramina in long

bones definitely helps to prevent intraoperative injuries in orthopaedic,

plastic and reconstructive surgeries.

Humerus

In the present study, all the 35 humeri had their foramina in the middle

third of the shaft. Among the foramina found, 64% were in the antero-medial

surface, 14% in the medial border, 10% in the lateral border, 10% in the

posterior surface and 2% in the antero-lateral surface.

Mysorekar in his study on 180 humeri found 96% of the foramina were

present in the middle third of the shaft, 3% in the lower third and 1% in the

upper third. He also reported that 41% of the 263 foramina were present in the

antero-medial surface, 38% in the medial border, 19% in the spiral groove, and

1% each in the anterior border & posterior surface.12 Longia et al. had reported

75
in his study on 200 humeri that 91% of the 222 foramina were present in the

middle third of the shaft, 5.4% in the lower third and 3.6% in the upper third.5

The maximum number of foramina being present in the antero-medial

surface was reported by Longia et al. (82.9%), Campos et al. (81.8% of 44

foramina, in 36 humeri), Murlimanju et al. (in 58 of the 96 bones studied) and

Pereira et al. (88.8% of 214 foramina, in 174 humeri).5,14,20,21 Asharani &

Ningaiah in their study on 120 humeri had found that the majority (52.3%) of

the 130 foramina were present in the medial border of the bones followed by

40% in the antero-medial surface, and the rest were distributed equally among

the lateral border, anterior border and posterior surface of the bones.32 A

significant proportion (6.5%) of foramina in the antero-lateral surface was

reported in the study by Mansur et al. on 253 humeri, which found a total of

368 foramina.34

Regarding the length-wise distribution of foramina in humeri, most

studies (Longia, Malukar & Joshi, Ukoha, Rao & Kothapalli, Asharani &

Ningaiah, Mansur et al., Veeramuthu) reported the maximum number of

foramina in humeri to be present in the middle third of the shaft of the

bones.3,5,22,32,34,40,41

Nagel had stated that the nutrient artery of the humerus is prone to

damage during the exposure and plating of the medial column in supra-condylar

fractures of the humerus, and hence it had been advocated for the plating to be

done both medially and laterally, with the fixation extending into the

diaphysis.54

76
Radius

Nutrient foramina were located in the anterior surface of majority of

radii in the present study.

In 35 radii studied, 87.5% of the foramina were present on the anterior

surface with the rest on the anterior (6.25%) and interosseous (6.25%) borders.

Analysis of the length-wise distribution of the foramina in the bones showed

that 54.3% of them were in the upper third of the bones and 37.1% in the middle

third.

Malukar & Joshi had reported that 83 (94.3%) of the 88 foramina in 100

radii were present in the anterior surface and the rest of the foramina were

present in the posterior surface, while also finding that 86.4% of the foramina

were present in the upper third of the shaft of the bones and the remaining in

the middle third.41 Ukoha et al. found in their study on 50 radii that 20 bones

(40%) had their foramina in the upper third and 15 bones (30%) had them in

the lower third of the bones. They had further reported that 32 bones (64%) had

their foramina in the anterior surface of the bones and 3 bones (6%) had them

in the posterior surface.22 Studies done by various authors reported that most of

the foramina in radii were found in the anterior surface of the

bones.5,12,14,20,21,25,40,45

In contrast to this study, Mysorekar in his study on 180 radii had

observed that 62% of the 184 foramina were present in the middle third of the

shaft and 36.4% were present in the upper third.12 Similar findings of a greater

number of foramina in the middle third of the shaft of radii were found in their

77
studies by Longia et al. (86.3% of 204 foramina, in 200 bones), Roul & Goyal

(75.7% of 37 foramina, in 37 bones) and Veeramuthu et al. (59% of 59

foramina, in 59 bones).5,30,40

Ulna

The present study on 35 bones revealed that 97.3% of the foramina were

present on the anterior surface of the bones, with the remaining on the

interosseous border. Also, 60% of the foramina were in the middle third of the

bones, with the rest in the upper third. Presence of major number of foramina

on the anterior surface was noted in the studies of Veeramuthu et al. (76%) and

Murlimanju et al. (86.7%).20,40

Veeramuthu et al. had found in their study on 59 ulnae that 45 foramina

(76%) out of the total 59 were present on the anterior surface, 15% on the

anterior border, 2% on the posterior surface and 5% on the lateral border. They

also reported that 68% of the foramina were present in the middle third of the

shaft and 32% in the upper third.40 Murlimanju et al. had reported that 65 of the

75 ulnae studied had their foramina in the anterior surface, 8 bones in the

anterior border and 2 in the interosseous border.20

Mysorekar had reported from his study on 180 ulnae that 62% of the 188

foramina were present in the middle third of the shaft of ulnae and 35% were

present in the upper third, while the remaining were present at the junction of

upper and middle thirds of the bones.12 In contrast to the present study, Longia

et al. reported in their study that the majority of the foramina were present in

78
the upper third of the bones (56% of 212 foramina, in 200 bones) followed by

the middle third (43%).5

The regions of muscular attachments to the proximal half of the radius

and ulna are reinforced by the blood supply from the nutrient arteries. However,

the distal part of these bones lack in nutrient foramina and thereby nutrient

arteries probably due to the lack of muscular attachments in that part. This may

be the reason for the delayed and non-union of fractures, common in the lower

half of these bones (Kizilkanat).8 Giebel et al. have stated that dorsal

localisation of plates is preferred in radius and ulna due to the lack of nutrient

foramina and arteries in the posterior aspect of these bones.55

Femur

The observations of the present study on the position of nutrient

foramina on femur were found to be similar with previous studies.

In the present study on 35 femora, it was found that 85.71% of the

foramina were present in the middle third and 14.29% in the upper third of the

bones. Further, 67.85% of the foramina were found in the linea aspera and its

lips, 26.79% in the medial surface and 5.36% in the lateral surface.

Gumusburun et al. in their study on 103 femora had reported that 65%

of the 188 foramina were present in the linea aspera and its lips, 24% in the

medial surface, 3% in the anterior surface and 3.7% each in the lateral &

popliteal surfaces. They also reported that 79% of the foramina were present in

the middle third of the shaft of the bones, 12% in the upper third and 9% in the

79
lower third.15 Oyedun had found in his study on 95 femora that 79% of the

foramina were present in the linea aspera & its lips, 19% in the medial surface

and 2% in the lateral surface.24 Sendemir & Cimen, in their study on 102 femora

had reported that 86.6% of the foramina were present in the linea aspera & its

lips and 7.1% of the foramina in the anterior aspect of the bones.6

All of the studies mentioned above confirmed that the majority of the

foramina were present in the linea aspera and its lips, followed by the medial

surface of bone.

Bhat in her study on 300 adult femora had reported that 48% of the

nutrient foramina were present at the junction of the upper & middle thirds of

the bones, 38% at the junction of middle & lower thirds, and 14% in the middle

third of the shaft of the bones.27 Poornima & Angadi who did a study on 100

femora had found 56.1% of the foramina to be at the junction of the upper &

middle thirds 18.7% at the junction of middle & lower thirds, and 23% of the

foramina in the middle third of the shafts of the bones.29 Malukar & Joshi in

their study on 100 femora had reported that 22 of the 167 foramina found were

present in the lower third of the shaft.41 Priya & Janaki had also reported from

their study on 100 femora that 2 bones had their foramina in the lower third of

the shaft.38 In the present study, foramen in the lower third of the shaft of femur

was not observed.

80
Tibia

The location of nutrient foramina in tibia is on the posterior surface and

in the upper third in majority of the studies done earlier.

Jayaprakash in his study on 50 tibiae had reported that 82% of the

foramina were present in the upper third of the shaft and 18% in the middle

third.33 Gupta & Kumari in their study on 312 tibiae had reported 190 of the

302 foramina to be present in the upper third and the remaining 112 foramina

to be present in the middle third of the shaft of the bones.23

With regard to the tibia, the present study found that 80% of the nutrient

foramina were present in the upper third of the bones and 20% were present in

the middle third. No foramen was found in the lower third of the bones.

Further, 97.14% of the foramina found in this study were present in the

posterior surface, the majority (85.7%) among which were present between the

lateral border and the soleal & vertical lines. The lateral border had 2.86% of

the foramina.

Malukar & Joshi had found from their study on 100 tibiae that 98% of

the foramina were present in the posterior surface and 1.9% in the lateral

surface.41 Priya & Janaki had report that 86 of the 92 tibiae studied had the

nutrient foramina in the posterior surface and 6 bones had them in the medial

surface.39 Sendemir & Cimen had found 90.8% of the foramina in the 134 tibiae

studied to be present in the posterior surface of the shaft, with the lateral surface

showing 5.7% of the foramina.6 Gupta & Kumari in their study had found the

81
majority of the foramina (299 out of 302) were present in the posterior surface

and 3 foramina were present in the interosseous border.23

According to Trueta, the rate of fracture healing is directly related to the

vascularity of the site and those areas with a good blood supply heal faster than

those areas with a poor blood supply. Tibia is one of the examples for this

phenomenon wherein delayed union and mal-union are common in the distal

part of the bone due to the relative absence of nutrient foramina in this part.56

Fibula

The fibulae analysed in the present study showed that 87.21% of the

foramina were present in the posterior surface of the bones, the majority of

which were found on the medial crest (56.41%), and between the medial crest

& posterior border (17.95%).

Mysorekar in his study on 180 fibulae found 179 foramina of which 100

(55.87%) were on the medial crest and 59 (33%) foramina were present

between the medial crest & the posterior border.12 The next higher proportion

of foramina (7.69%) was seen in the interosseous border followed by a few in

the medial (2.55%) and lateral (2.55%) surfaces of the bones. Sendemir &

Cimen found 88.5% of the foramina in the medial surface, in the 69 fibulae that

they studied.6 Bilodi and Reddy in their study on 189 fibulae found an almost

equal proportion of foramina in the posterior (29.62%), medial (21.16%) and

lateral surface (22.23%).43 Pereira et al. have reported from their study on 114

fibulae that a majority of foramina (98.2%) were seen in the lateral surface.21

82
Regarding the length wise distribution of foramina, in the present study,

the greatest number of foramina (85.71%) were seen in the middle third of the

shaft of the bones, with a few foramina in the upper (8.57%) and lower thirds

(2.86%). Mysorekar had reported that 96% of the foramina in fibulae were in

the middle third of the shaft, 2.2% in the lower third and 1.7% in the upper

third.12 Gumusburun et al. had reported that 60 (92.3%) of the 65 foramina that

they found in the 60 fibulae were in the middle third of the shaft and the rest

were in the lower third.15

Pre-operative knowledge of the variations in the position and location of

the nutrient foramina is especially important in the fibula which is commonly

used for bone grafting. If it’s desirable for the transplant to have endosteal and

peripheral vascularisations, then the graft must be taken from the middle third

of the shaft, where the nutrient foramen is more likely to be present.57,58 For the

osteocytes and osteoblasts in the free vascularised bone graft to survive, it is

essential to preserve the nutrient blood supply, which also helps in the

acceptance of the graft by the recipient bone through graft healing that takes

place by the process of creeping substitution.17

A graphical comparison of the position, location of nutrient foramina in

the long bones of upper and lower limbs between different studies is given in

figs. 19, 20 & 21.

83
Humerus
90

Percentage of foramina
80
70
60
50
40
30
20
10
0
Present study (35 Mysorekar (180 Asharani & Mansur et al. (253
bones) bones) Ningaiah (120 bones)
bones)
Studies

AMS Medial border Lateral border


PS Anterior border Antero-lateral surface

Radius
100
Percentage of foramina

80
60
40
20
0
Present study (35 Malukar & Joshi Ukoha et al. (50 Veeramuthu et al.
bones) (100 bones) bones) (59 bones)
Studies

AS Anterior border Interosseous border PS

Ulna
100
Percentage of foramina

80
60
40
20
0
Present study (35 Veeramuthu et al. Murlimanju et al. Mysorekar (180
bones) (59 bones) (75 bones) bones)
Studies

AS Interosseous border Anterior border PS

Fig. 19 – Bar chart showing comparison of position of nutrient foramina in


upper limb long bones between different studies.
Femur
90
80

Percentage of foramina
70
60
50
40
30
20
10
0
Present study (35 Gumusburun et al. Oyedun (95 bones) Sendemir & Cimen
bones) (103 bones) (102 bones)
Studies

LA & its lips Medial surface Lateral surface AS Popliteal surface

Tibia
100
Percentage of foramina

80
60
40
20
0
Present study (35 Malukar & Joshi Priya & Janaki (92 Sendemir & Cimen
bones) (100 bones) bones) (134 bones)
Studies

PS Lateral border Lateral surface Medial surface

Fibula
100
Percentage of foramina

80
60
40
20
0
Present study (35 Mysorekar (180 Sendemir & Cimen Bilodi & Reddy
bones) bones) (69 bones) (189 bones)
Studies

PS Interosseous border Medial surface Lateral surface

Fig. 20 – Bar chart showing comparison of position of nutrient foramina in


lower limb long bones between different studies.
It was observed in the present study that most of the nutrient foramina

were present in the flexor aspects of the bones, that is, in the anterior aspect in

upper limb long bones and in the posterior aspect in lower limb long bones. The

reason for this distribution may be due to the higher requirement of blood

supply by the bulky, stronger and more active flexor muscle of the limbs, when

compared to the extensors.8

Furthermore, the results of the student’s t-test, comparing the length

wise location of the foramina between the right sided and left sided bones were

insignificant for each of the individual group of bones, thus showing that there

was no statistically significant difference in the location of foramina between

bones of both sides. Further studies with a larger sample size are required to

ascertain this observation.

3) Size of the nutrient foramina

The present study revealed that the majority of the foramina were of the

dominant type in radius (59.38%), ulna (54.05%), femur (78.57%) and tibia

(88.57%).

Kizilkanat et al. have stated that whenever a single nutrient foramen was

observed in a bone, it was always dominant.8 But this study found many bones

with a single secondary foramen. Gupta & Kumari had reported that all of the

302 foramina in 312 tibiae that they studied were dominant.23

It was documented by Bhat (88.12% of 480 foramina, in 300 bones) and

Kumar et al. (68% of 150 foramina, in 99 bones) that the majority of the femoral

84
nutrient foramina were dominant was also established by.27,42 Further,

Bridgeman & Brookes and Al-Motabagani in their study on femora, had

reported that in case of multiple foramina being present in a bone, they need

not be of the same size.16,19 The present study confirmed this finding.

In the present study, all of the femora studied had at least one dominant

foramen except one femur which had a single secondary foramen.

Kumar et al. in their study had reported one femur out of the 101 femora

they studied to have a single secondary foramen.42 Sendemir and Cimen had

reported in their study that all the 102 femora studied had at least one dominant

foramen. They also found two femora having 8 and 9 dominant nutrient

foramina respectively.6

Nidhi et al. in their study on 160 fibulae found that 141 bones had a

dominant foramen and 8 bones had a secondary foramen, with the rest of the

bones having double foramina (one dominant and the other secondary).28 Sinha

et al. had found from their study on 100 fibulae that 104 (85.2%) of the 122

foramina present were of the dominant type and the rest were secondary in

size.35 However, the present study observed that the majority (64% and 79.49%

respectively) of the foramina in humeri and fibulae were secondary.

Guo in his study had reported that fibulae had many minute foramina on

their surface apart from the nutrient foramina, and that the muscular branches

of the peroneal artery may enter the bone through these minute foramina. He

inferred that by this way, the bones without a nutrient foramen may get the

blood supply from the musculo-periosteal vessels.13

85
The proportions of dominant and secondary foramina found by this

study in the different groups of long bones are graphically represented in fig.

22.

Statistical testing in the present by chi-square test to find any association

between the size of the foramina and the side (right or left) of the bones returned

an insignificant p-value (p = 0.33 > 0.05), indicating that the size of the nutrient

foramina was independent of the side of the bone. But, Carroll in the year 1963,

using Fisher’s “t” table, had demonstrated a statistically significant higher

proportion of larger foramina in the right sided humeri that he studied.11

The chi-square test of independence returned a significant p-value (p =

0.01 < 0.05) while testing the association between the size of the foramina and

the property of the bone belonging either to the upper or the lower limb. Thus,

this study found that the dominant foramina occurred more frequently in the

lower limbs than in the upper limbs, and the secondary foramina were more

common in the upper limbs, which were statistically significant. The reason for

this occurrence may be due to the higher force and stress transmitted to the

lower limbs than to the upper limbs in view of the weight bearing & locomotive

functions of the lower limbs and the relatively finer functions of the upper

limbs, thereby warranting a more robust blood supply for the lower limb bones,

resulting in a larger size of the nutrient foramina. This finding however has to

be confirmed by more extensive studies and with a larger sample size.

86
0
Upper end of bone

10

20
26.38 27.13 27.29 26.75
28.86
30
38.96
40
Foraminal index

50 46.33 45.49
50.35
60
60
70 65.73 67.12

80

90

Lower end of bone


100
Humerus Radius Ulna Femur Tibia Fibula
Bone

Fig. 21 – Graphical representation of the length-wise location of foramina in


the shaft of the long bones based on the range of foraminal index

Humerus Radius Ulna

36 40.62 45.95
64 59.38 54.05

Dominant Secondary Dominant Secondary Dominant Secondary

Femur Tibia Fibula

11.43
21.43 20.51

78.57 79.49
88.57

Dominant Secondary Dominant Secondary Dominant Secondary

Fig. 22 – Percentage of dominant and secondary foramina in the six groups of


bone in the present study
4) Direction of the nutrient foramina and Obliquity of the nutrient canals

The present study revealed that all the upper limb bones had nutrient

foramina which were directed towards the elbow, and all the lower limb bones

except 8 fibulae had their foramina directed away from the knee. Among the 8

fibulae with variation in the direction of foramina, 5 bones had a single nutrient

foramen and the rest had double foramina, one directed upward and the other

downwards. Mysorekar in his study on 180 bones each of the long bones of

upper and lower limbs found that all of the upper limb bones had their foramina

directed towards the elbow and all the lower limb long bones except 9 fibulae

had their foramina directed away from the knee. Of the nine fibulae with

foramina directed towards the knee, he had reported that six fibulae had single

nutrient foramen and the remaining 3 bones had double foramina (one directed

towards the knee and the other directed away from the knee).12

The findings of this study except in a few fibulae obeyed the ‘growing

end theory’ of the direction of nutrient foramina being away from the growing

end of the bone which is “towards the elbow and away from the knee I flee”,

confirmed by many authors (Mysorekar, Shulman, Bilodi, Shah & Saiyad,

Solanke, Poornima & Angadi, Roul & Goyal, Vadhel, Asharani & Ningaiah,

Mansur, Ashwini, Veeramuthu).12,25,46,47,26,29,30,32,34,40,43,45 Sinha et al. had

reported in their study that all the nutrient foramina in the 100 fibulae that they

studied were directed downwards (away from the knee).35 Longia et al,

Mazengenya & Fasemore and Nidhi et al. have stated that variations in the

direction of the nutrient foramina were more frequent in fibulae.5,28,44

87
Nutrient foramina in femora, which pointed downwards towards the

growing end were reported by Kumar et al. (2 out of 150 foramina, in 101

bones) and Lutken (7 out of 610 foramina, in 410 bones).10,42 Hughes in his

study had stated that anomalies in the direction of nutrient foramina in femur

were common in lower animals and that they were less frequent in humans due

the presence of an axis artery in the thigh, the profunda femoris artery, which

runs near the femur and is always present.51

Variations in the direction of the foramina in tibia, them being directed

upwards towards the knee, were found by Longia et al. (in 19 out of the 200

bones that they studied), Gupta & Kumari (in 3 of the 312 bones they studied),

Mazengenya & Fasemore (in 5 bones of the total 360 studied) and Kumar et al.

(in 5 of the 151 bones they studied).5,23,42,44 In a study by Ukoha et al. on 50

human radii, they found a single bone which had its nutrient foramen directed

downwards, towards its growing end and away from the elbow.22

With regard to the obliquity of the nutrient canals, the present study

found that all the bones except one tibia had uniformly oblique foramina

irrespective of the site of the foramina. This uniformity in the obliquity of the

nutrient canals has been confirmed by Mysorekar.12 The variant tibia had its

nutrient canal which was directed anteriorly from the posterior aspect. A similar

finding in fibula was not found in any of the studies mentioned here. However,

Lutken (6 foramina out of 610, in 410 bones) and Oyedun (in 1 of the 95 bones

studied) have both reported femora having horizontal nutrient canals in their

respective studies.10,24

88
There are a few theories which account for the general constancy in the

direction of the canals and their anomalies, and these theories include the

‘periosteal slip theory’ by Schwalbe, the ‘vascular theory’ by Hughes and the

‘muscular theory’ by Lacroix, out of which the vascular theory offered the most

comprehensive explanation for the direction of the nutrient canals.51,59,60

However, the different factors mentioned in the different theories may be

appropriately and proportionally contribute to the direction and obliquity of the

nutrient canals.

5) Clinical importance

Orthopaedic surgeries including joint replacement, fracture repair and

vascularised bone grafting require a sound understanding of the number and

position of nutrient foramina in the long bones (Kizilkanat).8

Longitudinal stress fracture occurs frequently in tibia and less

commonly in femur and fibula. These fractures may initiate from the sites of

the nutrient foramina, them being a potential area of weakness in the bones.

Under increased stress and with decreased quality of the bones due to any

reason, the foramen may develop a fracture. Position of the fracture and the

pattern of edema with relation to the nutrient foramen may secondarily aid in

the diagnosis of this type of fracture (Craig).9

The exposure and stripping of the periosteum in treating diaphyseal

fractures by open reduction internal fixation (ORIF) may add insult to the

already existing bony injury. A knowledge of the anatomy of the nutrient

89
foramina may aid in adjusting and manipulating the bony exposure and

dissection in these surgeries, so as to avoid further injury to the region of the

nutrient foramina (Nagel).54

Healing of fractures like that of other wounds depends on the blood

supply of the bones. Damage to the nutrient artery either during the injury or

during the subsequent manipulation may impede the fracture healing. An idea

on the positional anatomy of the nutrient foramina and arteries can help to avoid

injury to those sites, thereby promoting an efficient fracture healing (Carroll).11

A knowledge of the vascular anatomy of the lower limb long bones may

help in deciding the level of resection of femur and tibia, done in allogenic

vascularised femoral diaphyseal transplantation and knee joint replacement

surgeries (Kirschner).18 According to Wavreille et al., a similar knowledge on

the upper limb long bones may help in the successful outcome of free

vascularised elbow allografts.7

90
CONCLUSION
CONCLUSION

A knowledge of the number and position of nutrient foramina in the

shaft of long bones of upper and lower limbs is necessary during surgical

procedures to avoid injury to the nutrient artery. The present study has reported

information regarding the number, position, location, size and direction of the

nutrient foramina in the shaft of long bones of upper and lower limbs. The

findings of this study may help to reinforce the information on the morphology

of nutrient foramina which are already available in literature.

There was a statistically significant difference in the size of the nutrient

foramina between the bones of the upper and lower extremity. Further studies

with a larger sample size are warranted to confirm this finding and its

significance.

91
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ANNEXURES
LIST OF TABLES

Table No.

1 - Number of nutrient foramina observed in the long bones of upper


limb
2 - Number of nutrient foramina observed in the long bones of lower
limb
3 - Position of nutrient foramina in different surfaces of the shaft of
humeri
4 - Position of nutrient foramina in different surfaces of the shaft of
radii
5 - Position of nutrient foramina in different surfaces of the shaft of
ulnae
6 - Position of nutrient foramina in different surfaces of the shaft of
femora
7 - Position of nutrient foramina in different surfaces of the shaft of
tibiae
8 - Position of nutrient foramina in different surfaces of the shaft of
fibulae
9 - Location of nutrient foramina in the long bones of upper limb based
on foraminal index
10 - Range and mean with standard deviation of the foraminal indices of
the upper limb long bones
11 - Range and mean with standard deviation of foraminal indices of
humeri with respect to individual surfaces and borders of the shaft
of the bones
12 - Range and mean with standard deviation of foraminal indices of
radii with respect to individual surfaces and borders of the shaft of
the bones
13 - Range and mean with standard deviation of foraminal indices of
ulnae with respect to individual surfaces and borders of the shaft of
the bones
14 - Location of nutrient foramina in the long bones of lower limb based
on foraminal index
15 - Range and mean with standard deviation of the foraminal indices of
the lower limb long bones
16 - Range and mean with standard deviation of foraminal indices of
femora with respect to individual surfaces and borders of the shaft
of the bones
17 - Range and mean with standard deviation of foraminal indices of
tibiae with respect to individual surfaces and borders of the shaft of
the bones
Table No.

18 - Range and mean with standard deviation of foraminal indices of


fibulae with respect to individual surfaces and borders of the shaft
of the bones
19 - Size of nutrient foramina of the upper limb long bones
20 - Size of nutrient foramina of the lower limb long bones
21 - Direction of nutrient foramina and obliquity of nutrient canals of the
upper limb long bones
22 - Direction of nutrient foramina and obliquity of nutrient canals of the
lower limb long bones
23 - Results of the Student’s t-test – ‘t’ & ‘p’ values, and inference
24 - Contingency table for the chi-square test to test association between
the size of the foramina and the side of the bones
25 - Contingency table for the chi-square test to test association between
the size of the foramina and bones being present in the upper or
lower limbs
LIST OF FIGURES

Fig. No.

1 - Materials used
2 - Identifying and counting the nutrient foramina
3 - Measuring the length of the bone for calculating FI
4 - Measuring the distance of nutrient foramen from the proximal end
of bone for calculating FI
5 - Dominant and secondary foramina classified using a 24-gauge
needle
6 - Finding the direction of nutrient foramen and obliquity of nutrient
canal using a fine stiff wire
7 - Nutrient foramina in humeri
8 - Radius showing a single dominant nutrient foramen in the middle
third of the anterior surface of the shaft
9 - Nutrient foramina in ulnae
10 - Radius showing a secondary foramen in its anterior surface
11 - Direction of nutrient foramen and obliquity of nutrient canal in
upper limb long bones
12 - Nutrient foramina in femora
13 - Femur showing a single secondary foramen in the linea aspera
14 - Nutrient foramina in tibiae
15 - A variant tibia with an anteriorly directed single secondary nutrient
foramen
16 - Nutrient foramina in fibulae
17 - Bar chart showing comparison of number of nutrient foramina in
upper limb long bones between different studies
18 - Bar chart showing comparison of number of nutrient foramina in
lower limb long bones between different studies
19 - Bar chart showing comparison of position of nutrient foramina in
upper limb long bones between different studies
20 - Bar chart showing comparison of position of nutrient foramina in
lower limb long bones between different studies
21 - Graphical representation of the length-wise location of foramina in
the shaft of the long bones based on the range of foraminal index
22 - Percentage of dominant and secondary foramina in the six groups of
bone in the present study
Length of bones and distance of the foramen from the proximal end
of the bones for calculating FI in humerus and radius

Humerus Radius
Bone TL DNF Bone TL DNF
No. (cm) (cm) No. (cm) (cm)
1 32.2 16.4 1 25.3 8.1
2 29.8 12.9 2 26.2 10.2
3 32.1 21.1 3 26.9 8.2
4 32.9 19.1 4 25 7.1
5 30.3 16.7 5 23.1 6.9
6 31.9 16.6 6 24.8 10.2
7 32.3 15 7 26.9 8.3
8 33.6 19.7 8 25.4 7.8
9 28.2 17.5 9 26.6 7.9
10 31.5 12.7 10 23.3 7.9
11 28.3 15.7 11 24.8 7.2
12 33.3 18.5 12 21.9 7.9
13 29.8 16.8 13 21.1 7.9
14 33.5 18.8 14 23.2 7.9
15 32.6 12.7 15 23.6 8.3
16 28.9 15.8 16 26.4 8.6
17 31.5 17.9 17 23 6.6
18 29.9 15.7 18 25.9 9.8
19 29.6 18.9 19 23.8 8
20 32.4 16.1 20 24.1 8
21 28.9 14.7 21 26.4 8.1
22 31.9 17.3 22 25.4 6.7
23 32 17.7 23 22.6 7.2
24 31.8 16.9 24 25 7.1
25 33.5 17.1 25 24.1 7.1
26 29.6 12.9 26 25.1 10.6
27 30.6 16.3 27 24.5 8
28 29.6 15.3 28 24.8 7.6
29 34.4 20.3 29 25 9.6
30 32.5 14.5 30 25.9 12
31 32.4 18.4 31 23.1 6.3
32 30.4 16 32 20.8 8
33 31.9 15
34 32.5 14.1
35 29.6 15.6
Length of bones and distance of the foramen from the proximal end
of the bones for calculating FI in ulna and femur

Ulna Femur
Bone TL DNF Bone TL DNF
No. (cm) (cm) No. (cm) (cm)
1 28 10.7 1 48.7 20
2 26.9 10.4 2 41.8 23.4
3 26 9.6 3 41.1 13
4 27.6 9.2 4 42.7 15.6
5 27.4 10.7 5 41.4 21.1
6 26.3 9.1 6 44 15.6
7 23.5 9.2 7 46.3 25
8 27.7 10.9 8 44.8 24.6
9 27.4 7.7 9 46.6 16.3
10 25.2 10.2 10 44 24.6
11 26.8 9.7 11 45.8 19.2
12 25.8 7 12 45.7 15.3
13 26.9 11.9 13 43.9 25
14 26.4 10.5 14 42.8 20.9
15 26 7.9 15 42.8 15.6
16 27.3 8.1 16 41.4 15.2
17 26.3 11.2 17 40 14.5
18 27.8 9 18 44 15.2
19 25.3 8.1 19 47.4 15.5
20 26.5 8.9 20 45.1 14.3
21 25.4 7.8 21 46.6 15.3
22 24.9 9.4 22 41.5 18.9
23 23.7 9.3 23 46.7 15.7
24 25.6 7.4 24 48 13.1
25 23.4 7.6 25 47.5 28.5
26 27.4 9.2 26 43.3 21.9
27 25.7 7.9 27 41.8 14.9
28 26.5 9.6 28 47.4 23.8
29 25.2 10 29 42.6 15.3
30 26.9 7.7 30 49.3 17.2
31 26.6 10.2 31 38.9 13.2
32 27.7 12.6 32 45.8 17
33 23.9 7.6 33 47.2 17.3
34 23.1 7 34 40.9 14.7
35 28.4 8.6 35 46.8 17
Length of bones and distance of the foramen from the proximal end
of the bones for calculating FI in tibia and fibula

Tibia Fibula
Bone TL DNF Bone TL DNF
No. (cm) (cm) No. (cm) (cm)
1 33.6 9.7 1 38.9 16.9
2 36.4 10.7 2 38.6 14.3
3 40 14.1 3 33.4 11
4 37.6 13.2 4 36.3 22.6
5 40.2 12 5 38.7 25
6 40.3 11.5 6 34.7 12.4
7 40.8 12.9 7 33.3 12.4
8 42.9 21.6 8 39.5 22
9 40 10.7 9 36.3 13.2
10 40 19.4 10 36.8 15
11 40.1 12.5 11 39.3 14.2
12 40 10.7 12 37.3 14.5
13 37.5 11.1 13 39 15.2
14 41 13 14 38.7 14.3
15 39.3 13.1 15 36.9 15.3
16 37.5 10.4 16 37.8 11.9
17 38.6 12.2 17 36.2 14.2
18 33.3 9 18 37.2 16.9
19 35.2 10.7 19 35.2 16.2
20 38.1 11.8 20 30.7 18.3
21 39.6 12.8 21 36.9 15.8
22 33.7 10.1 22 35 16.8
23 37.5 11.1 23 34.2 13.1
24 39.8 12 24 34.9 18.5
25 35.1 12 25 30.6 11.1
26 35.4 11 26 35.2 18.3
27 40 12.4 27 35.1 13.6
28 39.7 13.1 28 33.1 16.3
29 38.4 10.3 29 34.5 13.4
30 38.1 11.4 30 34.8 15.8
31 37.2 15.6 31 35 10.1
32 40.3 13.2 32 36.5 24.5
33 37.1 11.2 33 36.4 22.4
34 37.7 11.7 34 36.5 12.4
35 33.2 9.9

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