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Original papers Med Ultrason 2019, Vol. 21, no.

3, 225-231
DOI: 10.11152/mu-1940

Is the presence of echo-rich periportal cuffing in the liver indicator


for abdominal inflammation in pediatric patients?
Nurdan Fidan1, Esra Ummuhan Mermi Yetis2, Muammer Murat1, Cuneyt Yucesoy3, Ebru
Turgal4, Mehmet Metin5

1Department of Radiology, Hitit University Erol Olcok Training and Research Hospital, Corum, 2Department of
Radiology, Maltepe University Faculty of Medicine, Istanbul, 3Department of Radiology, Hitit University Faculty of
Medicine, Corum, 4Department of Biostatistics, Hitit University Faculty of Medicine, Corum, 5Department of Pediatric
Surgery, Hitit University Erol Olcok Training and Research Hospital, Corum, Turkey

Abstract
Aims: Hyperechoic/echo-rich periportal cuffing (ErPC) is defined as an increase in echogenicity relative to the adjacent
liver parenchyma. Thickening in the periportal area may occur with proliferation of bile ducts, hemorrhage, oedema, fibrosis,
inflammatory changes or a combination of these. The aim of this study is to determine which intraabdominal inflammatory dis-
eases are associated with the presence of ErPC in the pediatric population and to calculate the sensitivity and specificity of this
finding. Material and methods: In this prospective study 200 consecutive children who underwent abdominal ultrasonogra-
phy (US) were included: group 1, the patient group (100 children with appendicitis, gastroenteritis, mesenteric lymphadenitis,
intestinal infection, terminal ileitis and invagination as cause of intra-abdominal inflammation) and group 2, the control group
(100 children). Results: The ErPC was positive in 74 (74%) cases in the patient group and in 3 (3%) in the control group.
According to final diagnoses, we found ErPC in most of patients with gastroenteritis (16/17), perforated appendicitis (10/11),
mesenteric lymphadenitis (5/6) and acute appendicitis (27/37). The sensitivity of ErPC in indicating intra-abdominal inflam-
mation was 0.80 and its specificity was 0.87. No significant correlation between ErPC and age, gender and CRP was found but
a moderate and significant positive correlation between ErPC and WBC (p=0,010; r=0.255) was detected. Very good concord-
ance between observers in terms of the presence of ErPC on abdominal US was found (concordance 97% and kappa 0.93).
Conclusions: We consider that the presence of ErPC in pediatric patients, when evaluated alongside clinical and laboratory
findings, has a high sensitivity and specificity for inflammatory intra-abdominal pathology.
Keywords: periportal cuffing; inflammation; acute abdomen; ultrasound; children

Introduction ic artery, bile duct, nerves, lymph ducts and potentially


empty areas. Periportal pathology occurs when any of
The periportal area is the anatomical area around the these structures are affected. The periportal area may
portal vein in the liver, including branches of the hepat- become wider due to inflammatory processes, tumor in-
filtration, bile duct proliferation, hemorrhage or oedema
Received 04.03.2019  Accepted 02.07.2019 and this appearance is radiologically defined as a peri-
Med Ultrason
2019, Vol. 21, No 3, 225-231
portal halo. Periportal halo is also referred as periportal
Corresponding author: Nurdan Fidan, MD cuffing (PC) in ultrasonography (US) and may appear as
Department of Radiology, Hitit University an increase or decrease of echogenicity in the periportal
Erol Olcok Training and Research Hospital, area. Hyperechoic/ echo-rich periportal cuffing (ErPC)
19200, Corum, Turkey
E-mail: kocak_nurdan@yahoo.com
is defined as an increase in echogenicity relative to the
Phone: +90 364 219 30 00 adjacent liver parenchyma and is termed “starry sky” or
Fax:0 364 223 30 30 “stars and stripes”’ [1-5]. It generally appears with acute
226 Nurdan Fidan et al Echo-rich periportal cuffing & abdominal inflammation in pediatric patients

hepatitis, cholecystitis, pancreatitis, primary sclerosing 100 pediatric patients presented for abdominal US with
cholangitis, pericolangitis, hepatic trauma, primary bil- pre-diagnosis of chronic abdominal pain (more than 3
iary cirrhosis and inflammatory bowel disease [6-11]. weeks), urinary tract infection, hepatic steatosis/obesity,
In previous studies, it has been mentioned that PC is hematuria, dyspepsia, urolithiasis, enuresis, chronic epi-
a very rare ultrasonographic finding (0.95%) [10,11]. The gastric pain, hepatosplenomegaly and hydronephrosis.
pathogenesis of ErPC is not completely known and his- WBC was determinated in all patients. No hospitaliza-
tological findings have not been reported [10]. Thicken- tion was needed in this group.
ing in the periportal area may occur due to proliferation The patients referred with a pre-diagnosis known to
of the bile ducts, hemorrhage, oedema, fibrosis, inflam- modify the periportal area such as trauma, viral hepatitis,
matory changes, or a combination of these [9,12]. It has pancreatitis, pyelonephritis, gallbladder/biliary tract pa-
been hypothesized that abnormal cells in inflammatory thology were excluded. In addition, we excluded patients
bowel disease emerge due to the transition of enterohe- with FMF (familial mediterranean fever) attack, ovarian
patic circulation from the intestinal mucosa into the por- torsion or ovarian cyst rupture, alterated liver tests or el-
tal system and inflammation of the liver [11]. evated serum amylase.
We planned this study to answer the question of The demographic data (age, gender) and pre-diagno-
whether this finding may be related or not to intra-ab- sis were collected. The patients were followed up until
dominal inflammation, because in our radiology unit we the final diagnosis and treatment was established.
frequently observed periportal echogenicity in pediatric US evaluation
patients presenting with acute abdominal findings. In US examinations were performed by a radiologist
adult patients the association between periportal echo- with 5 years of experience in pediatric US using Philips
genicity and inflammatory diseases, such as inflamma- HD15  and Philips Affiniti 70G (Philips  Healthcare,
tory bowel diseases, hepatitis, pancreatitis, biliary tract Amsterdam, the Netherlands) with a 3-5 MHz / 3-12 MHz
diseases, parasitic disease or pyelonephritis, has been frequency transducer. A second radiologist was consult-
already described [10,11]. In the pediatric population, ed regarding the presence of ErPC in the liver without
the association has been reported in patients with cystic knowing the patient’s pre-diagnosis and US results. The
fibrosis, hemophagocytic lymphohistiocytosis and ap- periportal echogenicity was compared with the posterior
pendicitis [12-18] but no primary study regarding spe- diaphragm echogenicity. ErPC was considered positive
cific inflammatory diseases related to ErPC in pediatric when there was an increase in echogenicity in the peri-
patients was published. The aim of this study is to de- portal area up to the diaphragm echo, diffuse (central and
termine which intra-abdominal inflammatory diseases peripheric) and in both lobes [12] (fig 1-5).
are associated with the presence of ErPC in the pediatric In the US examination, if the anterior-posterior di-
population and to calculate the sensitivity and specificity ameter of the appendix with a blind-ending, tubular and
of this finding for acute intra-abdominal pathologies. nonperistaltic segment of bowel that arises from the ce-
cum was less than 6 mm, it was interpreted as normal. If
Materials and methods the appendix diameter was greater than 6 mm and non-

Study population
The study was conducted prospectively with the ap-
proval of the local Ethics Committee at the Radiology
Department of Corum Training and Research Hospital,
between 2015-2017. The study included 200 consecutive
pediatric patients aged between 2 and 18 years old who
were divided into two groups. In Group 1 (patient group)
100 patients referred by the emergency department for
an abdominal US with pre-diagnosis of acute abdomi-
nal pain, acute abdomen, acute appendicitis, nausea,
vomiting, diarrhea and invagination were enrolled. All
these patients were hospitalized, followed up and treated.
White blood cell count (WBC) in all patients and C-reac-
tive protein (CRP) in 71 patients were measured. Values Fig 1. A 9-year-old boy with upper respiratory tract infection:
of >10x109/L for WBC and >5 mg/L for CRP were con- a-c) US images with convex transducer of the normal liver;
sidered to be high. Group 2 (control group) consisted of d) US image with high frequency linear-array transducer.
Med Ultrason 2019; 21(3): 225-231 227
compressible, it was interpreted as acute appendicitis Statistical analysis
[19,20]. The wall thickness of the bowels greater than 2 The data were summarized with descriptive statis-
mm was interpreted as edema and dilatation of the bow- tics. Continuous quantitative variables are expressed in
el loops more than 2.5 cm in diameter was considered terms of mean and standard deviation values, and quali-
pathologic [21-23]. The presence of free fluid between tative variables are expressed in terms of the minimum
the bowel loops and mesenteric lymph nodes (the size of and maximum values. Categorical data were compared
the largest lymph node was measured) in the right lower with chi-square and Fisher’s exact tests. A point-biserial
quadrant of the abdomen were recorded. If the number correlation coefficient  was  used  to determine the rela-
of lymph nodes were ≥5, with dimensions over 10/5 mm tionship between binary and continuous variables. Phi
or clusters, the findings were considered to be positive in coefficient  was used for the association of two binary
terms of mesenteric lymphadenitis [20,24,25]. variables. Sensitivity and specificity for PC were calcu-

Fig 2. A 7-year-old girl with a history of acute abdomi- Fig 3. An 8-year-old girl with a history of acute abdominal pain
nal pain: a-c) US images with convex transducer of the liver and nausea: a,b) US images with convex transducer of the liver
demonstrate increased periportal echogenicity in the central demonstrate increased periportal echogenicity in the central and
and peripheral parenchyma; d) US image with linear-array peripheral parenchyma; c) US image with high frequency line-
transducer of the right lower quadrant shows distended, non- ar-array transducer of the liver shows “starry sky appearance” of
compressible, abnormal appendix with thickened appendiceal increased periportal echogenicity; d)US image of the right lower
wall due to inflammation. Final diagnosis was acute appendi- quadrant shows an abnormal appendix with adjacent increased
citis. echogenicity. Final diagnosis was perforated appendicitis.

Fig 4. A 10-year-old boy with a history of acute abdominal Fig 5. A 6-year-old boy with a history of acute abdominal pain,
pain: a,b) US images of the liver demonstrate increased peri- nausea and diarrhea: a) US image of the liver demonstrate in-
portal echogenicity; c, d) US images with linear-array trans- creased periportal echogenicity; b-d) US images with linear-ar-
ducer of the right lower quadrant shows clustered, enlarged and ray transducer of the right lower quadrant shows the distended
tender mesenteric lymph nodes in the right lower quadrant with bowel loop(arrow), presence of free intraabdominal fluid (ar-
a long-axis diameter of 1.5 cm. The final diagnosis was mesen- row) and the appendix is normal size (arrow). Final diagnosis
teric lymphadenitis. was gastroenteritis.
228 Nurdan Fidan et al Echo-rich periportal cuffing & abdominal inflammation in pediatric patients
Table I. Summary of the demographic data and pre-diagnosis of the referred patients for abdominal ultrasonography
Patient group (n:100) Control group (n:100) p value
Age (years) 9.72±4.30 8.5±3.79 p=0.066
Sex (M/F) 67/33 35/65 <0.001
WBC (x109/L) 14.87±6.13 7.74±1.89 <0.001
CRP (mg/L) 41.62±62.97 –
Pre-diagnosis – number of cases Acute appendicitis – 49 Chronic abdominal pain – 42
Acute abdomen – 28 Urinary tract infection – 24
Acute abdominal pain – 15 Hematuria – 7
Invagination – 3 Dyspepsia – 7
Nausea, vomiting – 3 Urolithiasis – 6
Diarrhea – 2 Other* – 11
WBC, white blood cell; CRP, C-reactive protein; *Other pre-diagnosis: enuresis nocturna, chronic epigastric pain, hepatosplenomegaly,
hydronephrosis

Table II. The number (n) and percentage (%) of ultrasongraphic lated. Kappa (K) was interpreted as an indication of poor
findings in patient group agreement when less than 0.2 and as fair agreement when
US findings n (%) 0.20. All tests were conducted at the two-sided 5% sig-
Acute appendicitis 47(47) nificance level using SPSS 20.
Mesenteric lymph nodes 12 (12)
Invagination 3(3) Results
Perforated appendicitis 3 (3)
Thickening of the terminal ileum + 3 (3) The demographic data and the presentation reasons
Mesenteric lymph nodes for US examination in both groups are detailed in Table I.
Acute appendicitis + 2 (2) In Table II the US findings in group 1 are listed. US was
Mesenteric lymph nodes reported as normal in 27 patients of group 1, and in 3 of
Perforated appendicitis + 1 (1) these patients, the abdominal computer tomography (CT)
Mesenteric lymph nodes investigation was realized because of continued clinical
Dilated bowel 1(1) suspicion. In 2 cases CT was normal while in one case
Fluid in the right lower quadrant 19 (19) acute appendicitis was diagnosed. The mesenteric lymph
Normal 27 (27) nodes detected in US examination were between 33x15
Increased periportal echogenicity 74 (74) mm and 13x7 mm.

Table III. Final diagnosis and treatment methods in patient and control groups


Patient group Control group
Final diagnosis n Final diagnosis n
Surgery 56 Medical treatment 100
Acute appendicitis 37 Normal 20
Perforated appendicitis 11 Disorders of urinary system 19
Reactive lymphoid hyperplasia 7 Upper respiratory tract infection 14
Invagination 1 Irritable bowel syndrome 11
Medical treatment 44 Gastroesophageal reflux 9
Non-specific diagnosis 17 Vitamin deficiency / malabsorption 7
Gastroenteritis 17 Non-specific functional bowel disorder 7
Mesenteric lymphadenitis 6 Endocrine disorders 5
Invagination 2 Dyspepsia 5
Terminal ileitis 1 Lower respiratory tract infection 3
Intestinal infection 1
Total 100 100
n, number of patients
Med Ultrason 2019; 21(3): 225-231 229
Table III detailed the final diagnoses and the thera-
peutic approach in both groups.
The presence/absence of ErPC according to the final
diagnosesis presented in Table IV and fig 6. The diagno-
sis of appendicitis, gastroenteritis, mesenteric lymphade-
nitis, intestinal infection, terminal ileitis and invagination
were accepted as causes of intra-abdominal inflamma-
tion. The sensitivity of ErPC for intra-abdominal inflam-
mation was calculated to be 80% and its specificity was
87%.
In Group 2, ErPC was positive only in 3 patients (3%)
with the final diagnoses of lower respiratory tract infec-
tion, functional bowel disorder and other disorders of the
urinary tract. While WBC level was higher in patients
with functional bowel disorder (11.35x109/L), it was
within the normal limits in the other 2 patients. Fig 6. Ranking list of the final diagnoses associated with peri-
portal cuffing in both groups. Horizontal line demonstrates
No significant correlation between the presence of number of the patients. ErPC, echo-rich periportal cuffing;
ErPC and age (p=0.103; r=0,164) sex (p=0.097; r=0.166) n, number of patients.
and CRP (p=0.063; r=0.222) could be established. There
was a moderate and significant positive correlation be- perforated appendicitis, mesenteric lymphadenitis and
tween ErPC and WBC (p=0.010; r=0.255). In both acute appendicitis. ErPC was negative in 6 of 7 patients
groups a very good concordance between observers in operated on for suspected acute appendicitis and whose
terms of the presence of ErPC on abdominal US was pathology results were reported as reactive lymphoid hy-
found (concordance 97% and kappa 0.93). perplasia, as well as in 97 of 100 patients of the control
group. According to our results, ErPC it is highly predict-
Discussions able for an abdominal acute inflammatory process. ErPC
was positive in each patient diagnosed with invagination,
ErPC is a rare US finding that manifests itself with terminal ileitis, and bowel infection but studies with large
the thickening of the periportal area. It is a non-specific case series are required since we had very few cases with
US observation and its relation with the underling dis- these pathologies.
eases is relatively unknown. Recognition of this phe- Ringler et al retrospectively evaluated US examina-
nomenon, the pathophysiology of which is not proven, tions of 1853 patients and Neesse et al retrospectively
is important because it should be considered as a sign evaluated US examinations of 10500 patients. The au-
of pathological liver. In our study, we found that the thors reported the presence of hyperechoic PC in 12
presence of ErPC was frequently diagnosed in patients (0.65%) and 91 patients (0.86%), respectively [4,10].
with gastroenteritis, followed by cases diagnosed with We detected ErPC in 3% of patients in the control group.
This higher frequency could be related especially to the
Table IV. Echo-rich periportal cuffing frequency according to pediatric population enrolled in this study compared with
final diagnoses in group 1 adult patients enrolled in the aforementioned study.We
Final diagnoses ErPC ErPC found no significant correlation between ErPC and the
negative positive children’s age.The prominent relationship between acute
Non-specific diagnosis 5 (19.2) 12 (16.2) appendicitis, gastroenteritis and mesenteric lymphadeni-
Mesenteric lymphadenitis 1 (3.8) 5 (6.8) tis and the presence of ErCP, as we found in our pediatric
Acute and perforated appendicitis 11(42.3) 37 (50) group, was not described in adult patients.Therefore, we
Gastroenteritis 1(3.8) 16(21.6) think that ErPC is more common in children and may be
Intestinal infection 0 1(1.4) negatively correlated with age.
Terminal ileitis 0 1(1.4) Neese et al found that all 14 cases of inflammatory
Reactive lymphoid hyperplasia 6(23.1) 1(1.4) bowel disease displayed ErPC positivity and 12 of them
Invagination 2(7.7) 1(1.4) showed significantly higher CRP levels [10]. Similar to
Total cases 26 74 the literature, in our study, the mean CRP and WBC lev-
The results are expressed as number(%). ErPC, Echo-rich Periportal els in the patient group was higher than normal. Particu-
Cuffing larly, CRP levels were increased in 27/37 patients with
230 Nurdan Fidan et al Echo-rich periportal cuffing & abdominal inflammation in pediatric patients

appendicitis, 9/ 10 patients with gastroenteritis, all of the In conclusion, ErPCappears especially in diseases
4 patients with mesenteric lymphadenitis,1 patient with associated with abdominal inflammation such as gastro-
terminal ileitis and in 1 patient with a bowel infection. enteritis, acute appendicitis, perforated appendicitis and
However, although there was a positive and significant mesenteric lymphadenitis. When evaluated with adequate
correlation between the presence of ErPC and WBC lev- clinical information, the presence of ErPC is a finding of
els, no correlation was found with CRP levels. This could high sensitivity and specificity in pediatric patients. This
be related to the low number of cases in some subgroups could have a significant contribution to correct diagnoses
and the lack of CRP determination in some of our pa- by directing the radiologists or clinicians to further ex-
tients. We think that a positive correlation may become aminations or follow-ups.
apparent in studies carried out with a larger series.
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