diagnostics

Article
Osteo-Proliferative Lesions of the Phalanges on Radiography:
Associations with Sex, Age, and Osteoarthritis
Sandra Hermann 1 , Iris Eshed 2 , Iván Sáenz 3 , Niclas Doepner 4 , Katharina Ziegeler 4,†
and Kay Geert A. Hermann 4, *,†

1 Department of Rheumatology and Clinical Immunology, Charité—Universitätsmedizin Berlin,

Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, 10117 Berlin, Germany;
sandra.hermann@charite.de
2 Sheba Medical Center, Department of Radiology, Sackler Faculty of Medicine, Tel Aviv University,
Tel Aviv 6997801, Israel; iriseshed@gmail.com
3 Departamento de Anatomía, Facultad de Medicina, Universidad de Barcelona, 08007 Barcelona, Spain;
dr.ivan.saenz@gmail.com
4 Department of Radiology, Charité—Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin
and Humboldt-Universität zu Berlin, 10117 Berlin, Germany; niclas.doepner@charite.de (N.D.);
katharina.ziegeler@charite.de (K.Z.)
* Correspondence: kghermann@gmail.com
† These authors contributed equally to this work.

Abstract: Objectives: The effects of aging such as osteophyte formation, acral shape changes, cortical
tunneling, and bone porosity as well as enthesophytes can be studied in the X-rays of hands. However,
during the interpretation of radiographs of the hands, misinterpretation and false-positive findings
for psoriatic arthritis often occur because periosteal proliferations of the phalanges are overinterpreted



and too little is known about enthesophytes of the phalanges in this area. Method: It included a

 total of 1153 patients (577 men, 576 women) who presented themselves to the emergency department
Citation: Hermann, S.; Eshed, I.; and received a radiography of their right hand to exclude fractures. The Osseographic Scoring
Sáenz, I.; Doepner, N.; Ziegeler, K.; System was used in a modified form to record osteophytes and enthesophytes. A linear regression
Hermann, K.G.A. Osteo-Proliferative model for periosteal lesions was computed with age, sex, osteophytes, and global diagnosis as
Lesions of the Phalanges on
covariables. The inter-reader agreement was assessed using ICC (two-way mixed model) on the
Radiography: Associations with Sex,
sum scores of osteophytes and periosteal lesions. Results: Overall, men exhibited more periosteal
Age, and Osteoarthritis. Diagnostics
lesions, demonstrated by a higher mean sum score of 4.14 vs. 3.21 in women (p = 0.008). In both
2022, 12, 618. https://doi.org/
sexes, the second and third proximal phalanx were most frequently affected by periosteal lesions, but
10.3390/diagnostics12030618
the frequencies were significantly higher in men. The female sex was negatively associated with an
Academic Editor: Antonio Barile extent of periosteal lesions with a standardized beta of −0.082 (p = 0.003), while age and osteophytes
Received: 5 December 2021 were positively associated with betas of 0.347 (p < 0.001) and 0.156 (p < 0.001), respectively. The
Accepted: 28 February 2022 distribution of osteophytes per location did not differ between men and women (p > 0.05). The
Published: 2 March 2022 inter-reader agreement was excellent for periosteal lesions with ICC of 0.982 (95%CI 0.973–0.989,
p < 0.001). Conclusions: Special care should be taken not to confuse normal periosteal changes in
Publisher’s Note: MDPI stays neutral
aging with periosteal apposition in psoriatic arthritis.
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Keywords: radiography; peripheral joints; periosteum; arthritis; osteoarthritis

Copyright: © 2022 by the authors. 1. Introduction

Licensee MDPI, Basel, Switzerland. The hand is more available than any other body region for detailed analyses of its
This article is an open access article
skeletal elements. The hand was not only the first human object to be X-rayed, but also the
distributed under the terms and
foundation of musculoskeletal radiology [1,2]. The effects of aging such as osteophyte for-
conditions of the Creative Commons
mation, acral shape changes, cortical tunneling and bone porosity as well as enthesophytes
Attribution (CC BY) license (https://
can be studied. However, a number of inflammatory and metabolic diseases also manifest
creativecommons.org/licenses/by/
in the joints and phalanges of the fingers, most notably rheumatoid arthritis (RA) and
4.0/).

Diagnostics 2022, 12, 618. https://doi.org/10.3390/diagnostics12030618 https://www.mdpi.com/journal/diagnostics

Diagnostics 2022, 12, 618 2 of 9

psoriatic arthritis (PsA), but also hyperparathyroidism. However, while osteo-proliferative

changes are uncommon in RA and hyperparathyroidism, they are considered the diagnos-
tic hallmark in PsA, in addition to characteristic erosions [3–5]. These osteo-proliferative
changes are typically located directly adjacent to the affected joint and are included in the
classification criteria for PsA (CASPAR criteria) [6].
As a general rule, osteophytes are sharply demarcated bony prominences that occur
at the edge of the articular surfaces. In contrast to this, periosteal attachments in psoriatic
arthritis are ill-defined in the early stage, but are also localized at the edge of the joints [7].
Only later in the course of the disease it may smooth out and then look strikingly similar
to osteophytes. Periosteal changes in psoriatic arthritis are also described on the shaft of
the phalanges as so-called periostitis. These are initially fuzzy calcified lamellae on the
diaphyses, which can be transformed into more solid proliferations in the course of the
disease. However, enthesophytes also tend to develop in the same location along the shaft
during life, which may be due to mechanical stress applied on the hands.
Although computed tomography (CT) has been used in clinical studies to depict
osteo-proliferative changes [8], radiography remains the main imaging modality for their
detection [9].
Since little is known about enthesophytes of the phalanges, periosteal proliferations of
the phalanges are commonly misinterpreted into false-positive findings for psoriatic arthritis.
The Osteographic Score (OSS) is a composite scale for evaluating age-related changes
in the skeleton of the hands [10,11]. It uses a combination of osteoporosis and osteoarthritis
parameters such as bone porosity, bone proliferation including enthesis ossification, scle-
rosis, and joint space narrowing [11]. As such, it is well suited as a basis for a modified
assessment score in this study, particularly because of its rating of bone proliferation.
In order to increase the body of knowledge regarding osteo-proliferative lesions of the
phalanges and to provide a basis for differentiating these changes from psoriatic arthritis,
we aimed in the current study to define the frequency, localization, and gender dependence
of periosteal attachments of the fingers’ phalanges in the general population and to relate
them to degenerative changes of the finger joints.

2. Materials and Methods

2.1. Patients and Sample Size Estimation
Included in this retrospective cross-sectional study were patients reporting with trau-
matic pain to the emergency department that underwent a radiography of the right hand
to exclude fractures. In order to describe the effects of sex and age on the lesions studied,
men and women from different age groups were included in equal proportions. A sample
size estimation was calculated by the institute of biometry and clinical epidemiology of
our university using a dedicated software (nQuery Version 7.0). Under the assumption
of a prevalence of 25% of target lesions in the general population, a sample size of 1153
was held sufficient to measure 95% Confidence interval with a width of 5%. The local
ethics committee approved of this study (ID EA2/138/20) prior to data acquisition and
individual informed written consent was waived because of the retrospective nature of
the investigation.

2.2. Anatomical Studies

The analysis of the X-ray changes was accompanied by a careful analysis of the
underlying anatomy. For this purpose, the cadaver of one finger was dissected in layers.
Briefly, after removing the skin from the palmar and incising the palmar aponeurosis,
incisions were made along the midline of the fingers as deep as the tendon sheaths. The
fatty and connective tissue of the fingers and palm as well as the tendon sheaths were
removed while preserving the annular ligaments A1 to A5 and the cruciate ligaments C1
to C3. Special attention was paid to the annular ligaments A2 and A4, according to the
research question of this study (Figure 1).
Diagnostics 2022, 12, x FOR PEER REVIEW 3 of 9

Diagnostics 2022, 12, 618 3 of 9

to C3. Special attention was paid to the annular ligaments A2 and A4, according to the
research question of this study (Figure 1).

Figure 1. Preparation of the flexor tendons of the 3rd finger and their pulleys with view from oblique
Figure 1. Preparation of the flexor tendons of the 3rd finger and their pulleys with view from oblique
palmar. The A2 and A4 annular ligaments (arrows), which insert into the diaphyses of the proximal
palmar. The A2 and A4 annular ligaments (arrows), which insert into the diaphyses of the proximal
phalanx and middle phalanx, respectively, can be seen as very delicate structures.
phalanx and middle phalanx, respectively, can be seen as very delicate structures.
2.3. Imaging
2.3. Imaging and
and Scoring
Scoring System
System
X-ray images of the
X-ray images of the right right hand
hand were
were assessed
assessed in in two
two planes
planes (anterior-posterior
(anterior-posterior and and
oblique) by one primary reader, a rheumatologist (S. H.) skilled in scoring
oblique) by one primary reader, a rheumatologist (S.H.) skilled in scoring hands and feet hands and feet
with 12 years of experience. A random sample of 100 patients was
with 12 years of experience. A random sample of 100 patients was also scored to assessalso scored to assess
inter-reader agreement
inter-reader agreement by by aa second
second reader,
reader, aa radiologist
radiologist with
with six
six years
years ofof experience
experience in in
skeletal imaging (K. Z.). Prior to image scoring, a consensus reading of
skeletal imaging (K.Z.). Prior to image scoring, a consensus reading of 20 test patients 20 test patients not
included
not in the
included analysis
in the analysiswas performed
was performed bybythethetwo
tworeaders
readerstogether
togetherwithwithanan expert in
expert in
musculoskeletal imaging
musculoskeletal imaging (K.G.H.).(K. G. H.).
The Osseographic
The Osseographic Score Score (OSS)
(OSS)[10]
[10]was
wasused
usedin inaamodified
modifiedform
formtotorecord
recordthe thealtera-
alter-
tions ofofage
ations ageininthe
theskeleton
skeletonwithwithreference
referencetotothe
the research
research question
question [12]. As the analyses of
project presented
project presentedhereheredid
didfocus
focusonon enthesophytic
enthesophytic phalangeal
phalangeal change,
change, thisthis domain
domain waswasfur-
further
ther refined.
refined. For For
this this purpose,
purpose, a detailed
a detailed description
description of the various
of the various grades ofgrades of enthe-
enthesophytes
sophytes
(0–3) was (0–3) was formulated
formulated (Table 1) and (Table 1) and pictorially
pictorially represented represented
in an atlasin(Figure
an atlas2).(Figure 2).
In each subject, the proximal, middle, and distal phalanges were scored for the pres-
ence of enthesophytes. A sum score was then calculated for each subject. The osteoarthritis
of the metacarpophalangeal and interphalangeal joints was also recorded using the Kellgren
and Lawrence score adapted for small joints [13], with a scale from 0 (absent) to 4 (severe).
Examples are given in Figure 3. In addition, a global imaging diagnosis was made by
the expert reader, distinguishing between degenerative, inflammatory, or neither. The
degenerative category included all cases with evidence of either osteophytes, joint space
narrowing, sclerosis, or a combination thereof on the hand at any joint. Inflammatory status
was assigned if erosions of the joints were apparent, again at any joints of the hand. Single
joints and entheseal sites in a fractured bone were excluded.
 Diagnostics
Diagnostics 12,12,
2022,
2022, 618 PEER REVIEW
x FOR 4 of
4 9of 9

Table 1. Refined definition of enthesophytic growth at digital phalanges, modified from

Table 1. Refined definition of enthesophytic growth at digital phalanges, modified from Karasik et
Karasik et al. [12].
al. [12].
Grade Definition of Enthesophytic Phalangeal Change
Grade Definition of Enthesophytic Phalangeal Change
0 Cortical bone smooth without prominences
0 Cortical bone smooth without prominences
Irregular cortical bone, possibly with fluffing,
1Irregular cortical bone, possibly with fluffing,
1 possibly with smallest, flattened periosteal proliferations
possibly
2
with smallest, flattened
Cortical bone withperiosteal proliferations
well-defined enthesophytic protuberance, not more
2 than 1
Cortical bone with well-defined enthesophytic protuberance, not more mm of substance increase
than 1 mm of substance increase
Cortical bone with clearly recognizable enthesophytic
3
Cortical bone with clearly recognizable enthesophytic
proliferation of 1 mm or more
3
proliferation of 1 mm or more

Figure 2. Anterior-posterior X-ray examples of the different grades of enthesophytic growth. Pa-
Figure 2. Anterior-posterior X-ray examples of the different grades of enthesophytic growth. Patients’
tients’ characteristics from left to right: 53 y/o female, 59 y/o male, 57 y/o female, 82 y/o male.
characteristics from left to right: 53 y/o female, 59 y/o male, 57 y/o female, 82 y/o male.

2.4. In each subject,

Statistical the proximal, middle, and distal phalanges were scored for the pres-
Analysis
ence ofAllenthesophytes. A sum
statistical analyses score
were was then
performed calculated
using for each
SPSS version 27 subject. The osteoarthritis
with a significance level
ofofthe
p < 0.05. All analyses were primarily performed for men and women separately,using
metacarpophalangeal and interphalangeal joints was also recorded and inthe
Kellgren
the case and Lawrence
of sex, score
differences adapted
were for small
also reported joints [13],
separately. with a scale
Frequencies from per
of lesions 0 (absent)
region to
4 were
(severe). Examples
compared usingare 2 tests. in
Chigiven Figure 3. rho
Spearman’s In addition,
was computeda global imaging
to assess diagnosis of
the correlation was
age with
made periosteal
by the expert lesions
reader,and OA. A linearbetween
distinguishing regression model for periosteal
degenerative, lesions or
inflammatory, wasnei-
computed
ther. with age, sex,category
The degenerative OA (sumincluded
score), and
all radiographic diagnosisofaseither
cases with evidence covariables. The
osteophytes,
inter-reader
joint agreementsclerosis,
space narrowing, was assessedor a using ICC (two-way
combination thereofmixed
on themodel) onany
hand at the sum
joint.scores
Inflam-
of OA and periosteal lesions.
matory status was assigned if erosions of the joints were apparent, again at any joints of
the hand. Single joints and entheseal sites in a fractured bone were excluded.
Diagnostics 2022, 12, 618 5 of 9
Diagnostics 2022, 12, x FOR PEER REVIEW 5 of 9

Figure 3. The different degrees of osteoarthritis formation at the distal interphalangeal joints. 0—
Figure 3. The different degrees of osteoarthritis formation at the distal interphalangeal joints. 0—
normal shape; 1—minimal de-rounding (arrowhead) and minute cystic changes; 2—gross osteo-
normal
phytes shape;
and cyst 1—minimal
formation de-rounding
(arrowhead),(arrowhead) and
joint space yet minute
well cystic changes;
preserved; 3—marked 2—gross osteophytes
asymmetric joint
and cyst formation (arrowhead), joint space yet well preserved; 3—marked
space narrowing (arrowhead); 4—complete joint space narrowing and marked osteophyteasymmetric joint space
for-
narrowing (arrowhead);
mation. Patients’ 4—complete
characteristics joint
from left space 46
to right: narrowing
y/o male, and marked
59 y/o osteophyte
female, formation.
62 y/o male, 63 y/o
female, 69characteristics
Patients’ y/o female. from left to right: 46 y/o male, 59 y/o female, 62 y/o male, 63 y/o female,
69 y/o female.
2.4. Statistical Analysis
3. Results
All statistical analyses were performed using SPSS version 27 with a significance
3.1.
levelPatients
of p < 0.05. All analyses were primarily performed for men and women separately,
and As determined
in the bydifferences
case of sex, the sampleweresize also
estimation,
reported1153 patientsFrequencies
separately. were included in this
of lesions
retrospective
per region were compared using Chi tests. Spearman’s rho was computed to assess 576).
analysis, with equal proportions
2 of men (n = 577) and women (n = the
A global imaging
correlation diagnosis
of age with of degenerative
periosteal lesions and OA. disease was
A linear assignedmodel
regression in 352for(30.5%) and
periosteal
inflammatory disease was
lesions was computed withseen
age,in 59 OA
sex, (5.1%) of score),
(sum the patients. In 152 patients,
and radiographic one or
diagnosis asmore
co-
locations
variables.were excluded from
The inter-reader the analysis,
agreement due to ausing
was assessed fracture.
ICC (two-way mixed model) on
the sum scores of OA and periosteal lesions.
3.2. Osteoarthritis
The distribution of osteoarthritis per location did not differ between men and women
3. Results
(p > 0.05). A complete table of frequencies of OA (Kellgren and Lawrence Grade 2 or higher)
3.1. Patients
at all locations and for different age groups is given as Table 2. In all fingers, the DIP joints
As determined by the sample size estimation, 1153 patients were included in this
were most frequently affected, followed by the PIP joints. The second and third fingers
retrospective analysis, with equal proportions of men (n = 577) and women (n = 576). A
were more affected than the fourth and fifth; as expected, OA was much more prevalent in
global imaging diagnosis of degenerative disease was assigned in 352 (30.5%) and inflam-
older patients. Correlation analyses showed a strong association of extent of OA (expressed
matory disease was seen in 59 (5.1%) of the patients. In 152 patients, one or more locations
as sum scores) and patient’s age with a Spearman’s rho of 0.660 (p < 0.001).
were excluded from the analysis, due to a fracture.

3.2. Osteoarthritis
The distribution of osteoarthritis per location did not differ between men and women
(p > 0.05). A complete table of frequencies of OA (Kellgren and Lawrence Grade 2 or
higher) at all locations and for different age groups is given as Table 2. In all fingers, the
DIP joints were most frequently affected, followed by the PIP joints. The second and third
 prevalent in older patients. Correlation analyses showed a strong association of extent of
OA (expressed as sum scores) and patient’s age with a Spearman’s rho of 0.660 (p < 0.001).

Table 2. Frequency of OA. Frequencies given as relative (%) and absolute numbers.

<3012,
Diagnostics 2022, Years
618 30–39 Years 40–49 Years 50–59 Years 60–69 Years 70–79 Years ≥80 Years
6 of 9
(%, n) (%, n) (%, n) (%, n) (%, n) (%, n) (%, n)
DIP-II 2.0 (5/252) 2.4 (4/168) 10.6 (18/170) 16.4 (26/159) 34.1 (60/176) 50.3 (75/149) 49.4 (39/79)
PIP-II 0.0 (0/252) 1.2 (2/168) 0.0 (0/170)
Table 2. Frequency 4.4 (7/159)
of OA. Frequencies 7.4 (13/176)
given as relative 16.8 numbers.
(%) and absolute (25/149) 21.5 (17/79)
MCP-II 0.0 (0/252) 0.0 (0/168) 0.6 (1/170) 2.5 (4/159) 2.8 (5/176) 4.7 (7/149) 12.7 (10/79)
<30 Years 30–39 Years 40–49 Years 50–59 Years 60–69 Years 70–79 Years ≥80 Years
DIP-III 1.6 (4/252)(%, n) 4.3 (7/168) (%, n) 5.9 (10/170)
(%, n) 16.4 (26/159)
(%, n) 31.8 (%,
(56/176)
n) 55.7
(%,(83/149)
n) 48.1
(%, n)(38/79)
PIP-III
DIP-II0.4 (1/252) 0.0 (0/168)
2.0 (5/252) 2.4 (4/168)1.8 (3/170)
10.6 (18/170) 3.816.4(6/159)
(26/159) 6.334.1(11/176)
(60/176) 14.8(75/149)
50.3 (22/149) 20.3
49.4 (16/79)
(39/79)
0.0 (0/252)
PIP-II0.0 (0/252)
MCP-III 1.2 (2/168)1.2 (2/170)
0.0 (0/168) 0.0 (0/170) 1.9 4.4 (7/159)
(3/159) 7.4 (4/176)
2.3 (13/176) 16.8
6.7(25/149)
(10/149) 21.5 (17/79)
13.9 (11/79)
MCP-II 0.0 (0/252) 0.0 (0/168) 0.6 (1/170) 2.5 (4/159) 2.8 (5/176) 4.7 (7/149) 12.7 (10/79)
DIP-IV
DIP-III
0.4 (1/252) 4.2
1.6 (4/252)
(7/168) 6.5
4.3 (7/168)
(11/170)
5.9 (10/170)
13.2 (21/159)
16.4 (26/159)
22.7 (40/176)
31.8 (56/176)
39.6 (59/149)
55.7 (83/149)
36.7 (29/79)
48.1 (38/79)
PIP-IVPIP-III0.0 (0/252) 1.2 (2/168)
0.4 (1/252) 0.0 (0/168)2.9 (5/170)
1.8 (3/170) 5.7 3.8(9/159)
(6/159) 7.4
6.3(13/176)
(11/176) 22.8(22/149)
14.8 (34/149) 22.8
20.3 (18/79)
(16/79)
MCP-III
MCP-IV 0.0 (0/252)
0.0 (0/252) 0.0 (0/168)0.0 (0/170)
0.0 (0/168) 1.2 (2/170) 0.0 1.9 (3/159)
(0/159) 2.3(0/176)
0.0 (4/176) 6.7
2.7(10/149)
(4/149) 13.91.3
(11/79)
(1/79)
0.4 (1/252) 4.2 (7/168) 6.5 (11/170)
DIP-VDIP-IV
0.4 (1/252) 3.0 (5/168) 5.9 (10/170) 8.2 13.2 (21/159)
(13/159) 22.7 (40/176)
21.0 (37/176) 39.6 34.2(59/149)
(51/149) 36.7 (29/79)
43.0 (34/79)
PIP-IV 0.0 (0/252) 1.2 (2/168) 2.9 (5/170) 5.7 (9/159) 7.4 (13/176) 22.8 (34/149) 22.8 (18/79)
PIP-V
MCP-IV 0.0 (0/252) 0.6 (1/168)
0.0 (0/252) 0.0 (0/168)0.0 (0/170)
0.0 (0/170) 3.1 0.0(5/159)
(0/159) 10.8 0.0(19/176)
(0/176) 20.1 (30/149)
2.7 (4/149) 24.1
1.3 (19/79)
(1/79)
MCP-V DIP-V0.0 (0/252) 0.0 (0/168)
0.4 (1/252) 3.0 (5/168)0.0 (0/170)
5.9 (10/170) 0.08.2 (0/159)
(13/159) 0.6
21.0(1/176)
(37/176) 1.3(51/149)
34.2 (2/149) 43.03.8 (3/79)
(34/79)
PIP-V 0.0 (0/252) 0.6 (1/168) 0.0 (0/170) 3.1 (5/159) 10.8 (19/176) 20.1 (30/149) 24.1 (19/79)
MCP-V 0.0 (0/252) 0.0 (0/168) 0.0 (0/170) 0.0 (0/159) 0.6 (1/176) 1.3 (2/149) 3.8 (3/79)
3.3. Periosteal Lesions
Overall, men exhibited more periosteal lesions, with a higher mean sum score of 4.14
3.3. Periosteal Lesions
vs. 3.21 in women (p = 0.008). A graphical illustration of lesions per region is given as
FigureOverall, menmen
4. In both exhibited more periosteal
and women, lesions,
the second and with
thirdaproximal
higher mean sum were
phalanx score most
of
4.14 vs. 3.21 in women (p = 0.008). A graphical illustration of lesions per region is given
frequently affected by periosteal lesions, but frequencies were significantly higher in men.
as Figure 4. In both men and women, the second and third proximal phalanx were most
frequently affected by periosteal lesions, but frequencies were significantly higher in men.

Figure 4. Distribution of periosteal lesions at phalanges. Relative frequencies (%) per region. Signifi-
Figure
cantly4. Distribution
higher of periosteal
frequencies are markedlesions at phalanges.
with an asterisk (*); Relative frequencies
p-values derived from(%)
Chiper region. Signif-
2 tests.

icantly higher frequencies are marked with an asterisk (*); p-values derived from Chi2 tests.
In both men and women, the extent of periosteal lesions correlated with age and
OA with Spearman’s rho of 0.586 (p < 0.001) and 0.535 (p < 0.001) in men and 0.575
(p < 0.001) and 0.562 (p < 0.001) in women. The regression analysis yielded a corrected
R2 of 0.265 for the model including sex, age, sum score for OA, and global category
(none/degenerative/inflammatory) as covariables. The female sex was negatively associ-
ated with an extent of periosteal lesions with a standardized beta of −0.082 (p = 0.003), while
age, extent of OA and the degenerative/inflammatory category were positively associated
with betas of 0.347 (p < 0.001), 0.156 (p < 0.001), and 0.078 (p = 0.041), respectively.
Diagnostics 2022, 12, 618 7 of 9

3.4. Inter-Reader Agreement

The inter-reader agreement was excellent for both periosteal lesions and osteoarthri-
tis with ICCs of 0.982 (95%CI 0.973–0.989, p < 0.001) and 0.989 (95%CI 0.984–0.993,
p < 0.001), respectively.

4. Discussion
This study adds to the body of knowledge on the natural history of skeletal aging of
the hand, demonstrating osteophyte and periosteal enthesophytes of the phalanges in a
central-European patient population. We found a high frequency of osteo-proliferative
lesions at the proximal phalanx of the second and third finger. Furthermore, the extent of
these lesions correlated with both the age and grade of the osteoarthritis of the finger joints.
Our investigation revealed that males exhibited osteo-proliferative lesions more fre-
quently than females, while the distribution of finger OA did not differ between the sexes.
These findings are in line with those of Kalichman et al., who studied the association
of midshaft enthesophytes and osteophytes and found that age corresponded to 45% of
enthesophyte variation in males but only 25% in females [14]. This finding may result from
a stronger grip of males compared to females [15] resulting in a more developed pulley
system at the fingers and also possibly higher mechanic strain on their insertions.

4.1. Anatomical Considerations

Given the unclear data on enthesophytes of the fingers, we preceded the radiographic
examinations with a precise anatomical dissection. It was found that there are normally no
roughnesses or calcareous protrusions on the lateral and medial sides of the proximal and
middle phalanges. Periosteal appositions were particularly frequent at the attachments
of the A2 annular ligament and the C1 cruciate ligament (frequency in females 6.7–38.8%
and in males10.4–49.3%) at the basal phalanges. Periosteal lesions were rare at the middle
and distal phalanges. Anatomically, the A2 and A4 annular ligaments are of particular
importance, as they prevent the superficial and deep flexor tendons from snapping out of
their sheaths during finger flexion. The lumbrical muscles play no role in the development
of phalangeal enthesophytes because both their origin and insertion are on the flexor and
extensor tendons, respectively [16], and thus have no bony contact. Periosteal lesions were
rare at the middle and distal phalanges. The work of Meng et al. deals with a similar aspect,
namely the palmar ridges of the phalanges [17]. These are particularly visible on oblique
images of the fingers, in contrast to the lesions in the focus of our study, which are clearly
visible on anterior-posterior projections. The histological analyses by Meng and colleagues
show a fibrocartilaginous layer between the attachments of the annular ligaments and the
palmar edges of the phalanges, which clearly identifies these regions as entheses [17,18].

4.2. Psoriatic Arthritis

Periosteal changes on the hands are the typical sign of psoriatic arthritis and some
forms of peripheral spondyloarthritis [19]. These are known to be spiculated in appearance
and often localized to the acral and articular sites. However, it has also been postulated
that periosteal proliferations occur diaphyseally in the setting of periostitis. However, their
frequency on radiographs has not been well studied. To complicate matters, diaphyseal
periosteal attachments also occur in the form of physiologic enthesophytes, leading to
diagnostic uncertainty. Our data underlines the limited specificity of diaphyseal periosteal
attachments, especially in the proximal phalanges and in men more than in women. In pa-
tients with suspected psoriatic arthritis, changes in these localizations should be interpreted
with care. Conversely, there is also a diagnostic dilemma when patients with the clear
clinical condition of psoriatic arthritis are presented as normal in the radiological report,
either because the periosteal changes have been inadequately analyzed or the early-stage
disease does not yet make these visible on X-rays.
Diagnostics 2022, 12, 618 8 of 9

4.3. Limitations
The study was planned with a long lead time, but some limitations need to be dis-
cussed. The X-ray examinations of the right hand from the emergency room were selected
for the analysis on the assumption that the acute traumatic changes, if any, do not cause
dependence on chronic ossification of the cruciate and annular ligament structures of the
fingers. Likewise, conclusions about mechanical loads should be drawn with caution
because, due to the nature of this study, we were unable to collect data on previously
known hand osteoarthritis or on occupational or recreational loads on the finger joints.
Purely theoretically, however, there is a risk of confusion of an acute osseous avulsion of
the annular ligament avulsion with a chronic enthesophyte. However, this influence can be
discarded as relevant due to the rarity of osseous avulsions at the phalanges.

5. Conclusions
Enthesophytes that can be reliably detected by conventional radiography represent a
form of ageing and correlate with the degree of osteoarthritis of the finger joints. Due to the
significantly lower manifestation in the female sex, mechanical causes can be postulated as
the cause of the changes. In the diagnostic process, the physiological periosteal changes
should not be confused with those of diseases such as hyperparathyroidism or psoriatic
arthritis. In our future projects, we will target patients with known psoriatic arthritis and
also analyze the association of entheseal bone proliferations with laboratory biomarkers of
bone metabolism.

Author Contributions: Conceptualization, K.Z. and K.G.A.H.; methodology, S.H., K.Z. and K.G.A.H.;
formal analysis, S.H., I.S., K.Z. and K.G.A.H.; investigation, S.H., I.S., N.D., K.Z. and K.G.A.H.;
resources, N.D. and K.Z.; data curation, N.D. and K.Z.; writing—original draft preparation, K.Z.;
writing—review and editing, S.H., I.E., N.D., K.Z. and K.G.A.H.; visualization, K.Z., I.S. and K.G.A.H.;
supervision, K.G.A.H.; project administration, K.G.A.H. All authors have read and agreed to the
published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: The study was conducted in accordance with the Decla-
ration of Helsinki, and approved by the Ethics Committee of Charité Universitätsmedizin Berlin
(ID EA2/138/20).
Informed Consent Statement: Not applicable.
Data Availability Statement: The data presented in this study are available on request from the
corresponding author.
Acknowledgments: The authors thank Robert Roehle for assistance with sample size estimation and
statistical analysis. They also thank the Berlin Institute of Health for essential infrastructure for data
collection and curation.
Conflicts of Interest: The authors declare no conflict of interest.

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