ORIGINAL ARTICLE: HEPATOLOGY

Interobserver Agreement on Endoscopic Classification of

Oesophageal Varices in Children


Lorenzo DAntiga, yPietro Betalli, zPaola De Angelis, Mark Davenport,
Angelo Di Giorgio,
jj
Patrick J. McKiernan, Valerie McLin, #Paolo Ravelli,

Ozlem Durmaz, yyCecile Talbotec,
zz
Ekkehard Sturm, Marek Woynarowski, and jjjjAndrew K. Burroughsy

ABSTRACT
training of paediatric endoscopists may improve the agreement in grading
Objectives: Data regarding agreement on endoscopic features of oesopha-
severity of varices in this setting.
geal varices in children with portal hypertension (PH) are scant. The aim of
this study was to evaluate endoscopic visualisation and classification of Key Words: children, endoscopy, interobserver agreement, oesophageal
oesophageal varices in children by several European clinicians, to build a varices, portal hypertension
rational basis for future multicentre trials.
Methods: Endoscopic pictures of the distal oesophagus of 100 children with (JPGN 2015;61: 176181)
a clinical diagnosis of PH were distributed to 10 endoscopists. Observers
were requested to classify variceal size according to a 3-degree scale (small,
medium, and large, class A), a 2-degree scale (small and large, class B), and
to recognise red wales (presence or absence, class Red). Overall agreement What Is Known
was considered fair if Fleiss and Cohen k test was 0.30, good if 0.40,
excellent if 0.60, and perfect if 0.80.  The natural history and response to treatment for
Results: Agreement between observers was fair with class A (k 0.34) and
oesophageal varices in children is not completely
class B (k 0.38), and good with class Red (k 0.49). The agreement was
understood.
good on presence versus absence of varices (class A 0.53, class B 0.48).  Prospective studies need to be multicentric to
The agreement among the observers was good in class A when endoscopic
achieve sufficient statistical power.
features of severe PH (medium and large sizes, red marks) were grouped and  There are few data regarding agreement on classifi-
compared with mild features (absent and small varices) (k 0.58).
cation of varices in children.
Conclusions: Experts working in different centres show a fairly good
agreement on endoscopic features of PH in children, although a better
What Is New

 There is fairly good agreement between endoscopists

Received October 31, 2014; accepted April 7, 2015.
From the
Paediatric Hepatology, Gastroenterology and Transplantation,
Hospital Papa Giovanni XXIII, Bergamo, the yPaediatric Surgery,
Hospital Niguarda Ca Granda, Milan, the zPaediatric Gastrointestinal
Surgery and Endoscopy, Ospedale Pediatrico Bambino Gesu, Rome,
Italy, the Department of Paediatric Surgery, Kings College Hospital,
London, the jjLiver Unit, Birmingham Childrens Hospital, Birming-
ham, UK, the Gastroenterology Unit, Department of Paediatrics,
University Hospitals, Geneva, Switzerland, the #Gastrointestinal Endo-
scopy, Hospital Papa Giovanni XXIII, Bergamo, Italy, the

Pediatric
Gastroenterology, Hepatology and Nutrition, Istanbul University and
School of Medicine, the yyDepartment of Pediatric Gastroenterology,
Hepatology and Nutrition, Hospital Necker-Enfants Malades, University
of Paris-Rene Descartes, Paris, France, the zzPaediatric Gastroenterol-
ogy and Hepatology, University Hospital for Children and Adolescents,
University of Tuebingen, Germany, the Gastroenterology Diagnostics
Unit, Childrens Health Memorial Institute, Warsaw, Poland, and the
jjjjLiver Transplantation and Hepatobiliary Medicine, Royal Free Hos-
pital, London, UK.
Address correspondence and reprint requests to Lorenzo DAntiga,
Paediatric Hepatology, Gastroenterology and Transplantation, Hospital
Papa Giovanni XXIII, Piazza Oms 1, 24127 Bergamo, Italy (e-mail:
ldantiga@hpg23.it).
yDeceased.
The authors report no conflicts of interest.
Copyright # 2015 by European Society for Pediatric Gastroenterology,
Hepatology, and Nutrition and North American Society for Pediatric
Gastroenterology, Hepatology, and Nutrition
DOI: 10.1097/MPG.0000000000000822
grading varices in children.

The agreement is weaker on mild disease, whereas it
is excellent for medium- and large-sized varices.
 This study addresses an important aspect related to
the success of future studies in children with
oesophageal varices.
P ortal hypertension (PH) is a common problem in children
with liver disease, and its most threatening complication,
variceal bleeding, is a major cause of morbidity (1). Although
the outcome of bleeding in young patients is not as poor as in adults
with chronic liver disease, variceal haemorrhage is still a life-
threatening event in childhood, especially in children with cirrhotic
PH (2).
There is lack of data on paediatric PH, and therefore these
patients are managed according to guidelines developed in adults,
despite widely differing aetiologies and physiological responses.
(3). Likewise, there is little paediatric data evaluating the effec-
tiveness of primary prophylaxis of variceal bleeding in children,
either by nonselective b-blockers or by endoscopic variceal
treatment (4). In addition, no scoring system for endoscopic
diagnosis and grading of varices has been validated or standar-
dised in children, and this surely should be the first step toward
reliable assessment of endoscopic findings among different
observers (5). Prospective and interventional studies on

176 JPGN  Volume 61, Number 2, August 2015

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 JPGN  Volume 61, Number 2, August 2015
paediatric PH will need to be multicentric if they are to have
sufficient power (6), and good agreement between endoscopists
in different tertiary care centres will be fundamental to such
studies (7). Therefore, our aim was to investigate interobserver
agreement amongst endoscopists working in different settings in
assessing the presence and severity of oesophageal varices in
children with PH.
METHODS
Endoscopic pictures of 100 children with a clinical diagnosis
of PH were collected and distributed to 9 endoscopists working in
tertiary care centres with a paediatric liver unit and to an adult
hepatologist with extensive experience in PH. The pictures were
prepared in a consecutively numbered series loaded in a PowerPoint
(Microsoft, Redmond, WA) presentation with no patient infor-
mation and sent simultaneously to the observers for blind, inde-
pendent scoring. Ethical approval was granted by the local ethics
committee, provided the material was anonymised.
Selection Methodology
The patients were chosen from a population of children with
either chronic liver disease or extrahepatic portal vein obstruction
(EHPVO) and managed at the Paediatric Hepatology, Gastroenter-
ology and Transplantation Unit of the Hospital Papa Giovanni XXIII
in Bergamo.
The patients were selected based on confirmed diagnosis,
representation of different ages and aetiologies, and broad distri-
bution of severity of clinical signs of PH. Pictures of patients having
bled or been treated with band ligation or sclerotherapy were
excluded to avoid biases because of the recognition of signs of
treatment. The pictures were selected based on good quality, similar
projection, and clear view of the lower oesophagus during insuf-
flation. All of the photographs were reviewed independently and
blinded of underlying diagnosis.
Endoscopic Procedure
The procedures were performed by 2 expert endoscopists and
using a forward-viewing flexible fiberoptic conventional endoscope
(GIF-160, GIF-XP160; Olympus America, Melville, NY) under
deep sedation. The pictures taken for grading of oesophageal
varices were captured when the distal oesophagus was fully dis-
tended with air.
Varice Classification
We tested 2 classifications of variceal size:
1. Classification A (class A) considered 3 degrees of variceal size.
Grade 0: no oesophageal varices; grade 1: small and
nontortuous oesophageal varices; grade 2: tortuous oesophageal
varices but occupying less than one-third of the distal
oesophagus radius; grade 3: large and tortuous oesophageal
varices covering more than one-third of the distal oesophagus
radius (8,9).
2. Classification B (class B) included only 2 degrees of variceal
size. Grade 0: no varices; grade 1 or small and grade 2 or large
varices. No description of small and large varices was provided
to the observers to guide grading in class B.
In addition, red signs (class Red) were divided into 2 groups:
presence or absence of any of red wale markings, cherry-red spots,
or hemocystic spots.
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Endoscopic Classification, Oesophageal Varices
As a speculation, we then calculated the different rate of
treatment that would be applied if different classifications and
different criteria were used to indicate prophylaxis.
The observers received the different classifications named on
a PowerPoint presentation without providing visual examples for
the scoring scale, to measure and describe the agreement without
affecting the usual observers practice.
Statistical Tests
We used the Fleiss k test to measure the overall agreement in
the assessment of varices among the 10 observers. To evaluate the
agreement between 9 observers compared with one taken as refer-
ence we used the Cohen k test. Cohen k is a measure of the
agreement between 2 raters, in which agreement due to chance
is factored out. Fleiss k applies to the case in which the number of
raters is >2. The k is constructed to be 0 when the agreement
obtained can be entirely attributed to chance, and it attains a
maximal value of 1.0 only in the case of complete agreement. A
negative value of k indicates an observed agreement less than that
expected by chance. Values >0.80 are considered perfect, values
between 0.60 and 0.80 excellent, values between 0.40 and 0.60
good, and those between 0.30 and 0.40 are regarded as fair. Values
<0.30 are considered consistent with poor agreement (10).
RESULTS
Patient Characteristics
Median age of the subjects at the time of endoscopy was 9.4
years (range 218 years, boy/girl 40/60). The underlying diseases
causing PH were EHPVO (n 21), biliary atresia (n 37), con-
genital hepatic fibrosis (n 32), and chronic hepatitis (n 10). The
reference observer (observer 10) described the following distri-
bution of findings: class A, no varices 19%, small 24%, medium
size 42%, and large 15%; class B, no varices 18%, small 46%, and
large 36%; presence of red signs (class Red), no signs 80% and
presence of signs 20% (Fig. 1).
Figure 2 shows the pictures of 3 different degrees of oeso-
phageal size according to the reference observer.
Overall Agreement
Classification A (Class A): 3 Degrees
The overall agreement using class A was 0.34 (95% CI
0.330.36) (fair agreement, Fleiss k test). The agreement was good
90
o
N
80
70
60
Percentage
50 No varices
Small
40 Medium
Large
30
s
Ye
20
10
0
Class A Class B Red signs
FIGURE 1. Classification of varices by the reference observer.
177
 DAntiga et al JPGN  Volume 61, Number 2, August 2015

for the presence versus absence of varices (Fleiss k 0.48, 95% CI

0.450.50) and for the presence of large varices (Fleiss k 0.43, 95%
CI 0.400.46) (Table 1).

Classification B (Class B): 2 Degrees

The overall agreement for class B was 0.38 (95% CI 0.36
0.40) (fair agreement, Fleiss k test). The agreement was good for the
presence versus absence of varices (Fleiss k 0.45, 95% CI 0.420.48)
and for the presence of large varices (k 0.43, 95% CI 0.400.46)
(Table 1).

Classification Red (Class Red)

For this classification, the overall Fleiss k statistic of con-
cordance was good for the presence of red signs (k 0.48, 95% CI Grade 1: small
0.450.51).

Agreement With a Reference Observer

Classification A (Class A)
The overall agreement with the reference observer was 0.34
(range 0.230.45) (fair agreement, Cohen k test) (Fig. 3); the group
agreement with the observer was good for the presence of varices
(k 0.53, range 0.300.71) and fair for the presence of large varices
(k 0.34, range 0.230.48). There was low concordance in classify-
ing small and medium varices (k 0.27 and 0.25, respectively)
(Table 1).

Classification B (Class B)
Grade 2: medium
The overall agreement with the reference observer was 0.38
(range 0.260.52) (fair agreement, Cohen k test) (Fig. 4); the group
agreement with the observer was good for the presence of
varices (k 0.48, range 0.300.63) and good for the presence
of large varices (k 0.42, range 0.240.54) (Table 1).

Classification Red (Class Red)

The agreement with the reference observer was good (0.49,
range 0.400.59, Cohen k test).

Agreement on Grouped Features

Medium and Large Varices in Class A
Grouping no varices plus small varices and comparing
it with medium plus large varices, the mean agreement Grade 3: large
between the group and the reference observer using class A was
excellent with Cohen test (k 0.60, range 0.490.68) and good with FIGURE 2. Endoscopic appearance of small-, medium-, and large-
Fleiss test (k 0.57, 95% CI 0.540.60) (Fig. 5). sized oesophageal varices classified by the reference observer.
If medium and large sizes were adopted in this cohort of
children to indicate primary prophylaxis, class A would lead to
(k 0.58, range 0.440.72) and good with Fleiss test (k 0.53, 95% CI
prophylactic treatment in 60% (8%) patients, whereas class B
would indicate prophylaxis only in 36% (10%) (P 0.0001, 0.50360.5620) (Fig. 6).
Student t test).

Small Varices With Red Marks and Medium and
Large Varices in Class A
Considering the guidelines proposed in adults to indicate
prophylaxis, including small varices with red marks, as well as
medium and large varices, the mean agreement between the group
and the reference observer in class A was good with Cohen test
Small Varices With Red Marks and Large Varices in
Class B
Considering the guidelines proposed in adults to indicate
prophylaxis, including small varices with red marks, as well as large
varices, the mean agreement between the group and the reference
observer in class B was good with Cohen test (k 0.46, range

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 JPGN  Volume 61, Number 2, August 2015 Endoscopic Classification, Oesophageal Varices

TABLE 1. Fleiss and Cohen coefficient of agreement within the group for the studied classifications

Class A Class B Class A Class A

Class A Class B Class Red Presence of Presence of Grade Class B Grade
Overall Overall Overall varices varices 23 Large red 2 3 red

Fleiss (95% CI) 0.34 (0.330.36) 0.38 (0.360.40) 0.48 (0.450.51) 0.48 (0.450.50) 0.45 (0.420.48) 0.57 (0.540.60) 0.46 (0.440.49) 0.53 (0.500.56)
Cohen (range) 0.34 (0.230.45) 0.38 (0.260.52) 0.49 (0.400.59) 0.53 (0.300.71) 0.48 (0.300.63) 0.60 (0.490.68) 0.46 (0.400.61) 0.58 (0.440.72)

Fleiss k test refers to the agreement among all of the 10 observers. Cohen k test is an index of agreement of each of the 9 observers compared with the
reference observer (observer no. 10). Grade 2, medium size; grade 3, large size varices; red, red marks. CI confidence interval.

0.400.61) and good with Fleiss test (k 0.46, 95% CI 0.4359
0.4943) (Fig. 7).
If small size with red marks, and medium- and large-sized
varices were adopted in this cohort of children to indicate primary
prophylaxis, class A would lead to prophylactic treatment in 60%
(10%) patients, whereas class B would indicate prophylaxis only
in 46% (9%) patients (P 0.005, Student t test).
DISCUSSION
Multicentre prospective trials in children with PH and oeso-
phageal varices are dependent on the accuracy and reproducibility
of the endoscopic findings (7), yet scoring systems for the diagnosis
and grading of varices have not been validated or standardized in
children, and little is known about their reproducibility.
Gastrointestinal haemorrhage is an important complication
of chronic liver disease or portal vein obstruction in children, and
several studies have described effective treatment for oesophageal
varices in children with cirrhotic and noncirrhotic PH (5,11,12).
Nonetheless, there are few published reports providing prevalence
figures derived from routine screening endoscopies for unselected
groups of children with PH. Studies from paediatric hepatology
referral centres suggest that >50% of cirrhotic children have varices
(6). The age at the first bleeding episode is related to the
underlying aetiology.
In a recent study, 65 children with EHPVO were studied for a
median of 8.4 years. A total of 32 (49%) patients presented with
bleeding at a median age 3.8 years, and during the follow-up period
43 of them (66%) had at least 1 bleeding episode (13). A study on
the long-term outcome of varices in children with EHPVO showed
that, among 44 children studied from age 12 to a mean age 20 years,
the probabilities of bleeding by age 18 and 23 years were 60% and
85%, respectively, in patients who had grade II or III oesophageal
varices at age 12, and concluded that children with EHPVO have a
risk of bleeding >50% during adolescence (14).
Although a small number of studies in children have
suggested that noninvasive tests may identify subjects at risk of
bleeding with sufficient accuracy (5,15,16), endoscopy remains the
reference test for the diagnosis of varices (4). A survey reported that
the majority of paediatric gastroenterologists consider endoscopy as
the preferred screening modality for oesophageal varices and
evidence of PH in children with liver disease (17).
The major reason for lack of good quality evidence on
management of PH in children is because many single-centre
studies have had too few subjects thereby lacking in statistical
power. The only way to evaluate strategies to prevent bleeding is to
carry out multicentre studies among centres following children with
chronic liver disease and performing diagnostic and therapeutic
endoscopy. Grading varices is essential in the management of these
patients. It follows that validation of this diagnostic procedure is an
essential preliminary step to any multicentre study (18).
In our study, we selected a group of patients with a clinical
diagnosis of PH, both cirrhotic and noncirrhotic, consecutively sent
to endoscopy for evaluation of varices. Endoscopic findings fol-
lowed a well-balanced distribution making statistics reliable for this
cohort. This is important because a limitation of k is that it is
affected by the prevalence of the finding under observation (19).
We chose to test and compare 2 different classifications to see
which would lead to better agreement among observers. The
traditional classification into 3 sizes (class A) performed similarly
to the simplified one (class B), with an overall fair interobserver
agreement in both. This grade of agreement is similar to what
has been reported in studies of adult patients with PH (Table 2)
(2023).
A limitation of this study was represented by the fact that we
used still photographs instead of videos. Although we collected
pictures taken during insufflation, a 20- to 30-second movie of each
patient endoscopy would have added power to the observers
evaluation.

50 70
Agreement in classification A Agreement in classification B
Cohen = 0.34 (range 0.230.45) Cohen = 0.38 (range 0.260.52)
60
40
50
Percentage
Percentage

30
No varices
40
No varices
Small
30 Small
20 Medium
Large
Large
20
10
10

0 0
1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 10
Observers Observe

FIGURE 3. Classification of varices scored by each observer using 3 FIGURE 4. Classification of varices scored by each observer using 2
degrees of size (classification A). The reference observer is number 10. degrees of size (classification B). The reference observer is number 10.

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 DAntiga et al JPGN  Volume 61, Number 2, August 2015

80 80
Agreement in classification A grouping medium and large varices Agreement in classification B grouping large and red-marked varices.
Cohen = 0.60 (range 0.490.68) Cohen = 0.46
70 70

60 60

50 50

Percentage
Percentage

40 40
No varices + small No varices + small
Medium + large
30 30
Large + red marks

20 20

10 10

0 0
1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 7 8 9 10
Observers Observers

FIGURE 5. Classification of varices scored by each observer using FIGURE 7. Classification of varices scored by each observer using
classification A and grouping together medium and large versus classification B and grouping together varices of large size plus those
absent and small varices. The reference observer is number 10. with red marks. The reference observer is number 10.

The present guidelines from the Baveno V Consensus Work-
shop on diagnosis and therapy in PH propose a 3-size classification
and recommend that patients with small varices without red signs
who have not bled do not require prophylaxis, whereas those with
medium-to-large oesophageal varices and those with red marks,
irrespective of size, should benefit from primary prophylaxis (24). It
should be clarified that in children, there is no evidence to support
primary prophylaxis of oesophageal bleeding for varices of any size
or colour. We know that children do not necessarily have the same
risk of bleeding as adults, and therefore these guidelines cannot be
adopted in paediatric patients.
Nevertheless, to better understand the differences between
class A and class B in this study, we evaluated the agreement and the
percentage of patients in our cohort that would have been treated if
the same indications for prophylaxis in adults were adopted. Group-
ing medium and large varices against small and no varices in class A
resulted in an excellent agreement, superior to class B. In this
perspective, with 3 categories of varices (small, medium, and large),
it would not be relevant if 1 observer classifies varices as medium
and the other as large because the management will be the same for
both types. Conversely, using class B, if one observer calls the
varices small and the other large, the clinical implication will be
significant because divergent assessment will lead to prophylactic
treatment versus none. Remarkably, if the sizes and the marks
indicating primary prophylaxis in adults (medium and large varices,
varices with red marks irrespective of size) were adopted in this
cohort of children, class A would lead to prophylactic treatment in
60% of the patients, an extremely large proportion of cases com-
pared with class B that would indicate treatment only in 46%. This
suggests that the observers, when scoring with class B, tend to
distribute medium-sized varices unevenly and downgrade them to
the low-risk group. In addition, based on our own data, the 3-grade
system showed the worst agreement between small- and medium-
sized varices, so probably here the medium vessels were inappro-
priately assigned and with this score the patients would be exposed
to risks of prophylactic treatment inappropriately. For this reason,
when it comes to future studies on indication to treat varices in
children, the use of a 3-grade versus a 2-grade score will be
extremely relevant. From these results, it is clear that further studies
to correlate different scoring systems with subsequent risks of
bleeding are needed because it is only with such studies that the
better grading system can be identified.
In 1990, Bendtsen et al (21) carried out an interobserver
agreement study of varices in adults with cirrhosis. The varices were
graded on a scale of 0 to 3 according to size. Overall agreement
among the endoscopists on the presence (grades 1 to 3) or absence
(grade 0) of varices was 70% and was not related to the experience

TABLE 2. Interobserver agreement on oesophageal varices: studies

80
Agreement in classification A grouping medium, large, and red-marked varices. comparison
Cohen = 0.58
70
Study (reference) Agreement (k)
60
Presence of varices
50 Cales et al (20) 0.40 (0.360.44)
Percentage

Bendtsen et al (21) 0.38  0.16

40
No varices + small Cales et al (22) 0.59
Cales et al (23) 0.52 (0.490.56)
30 Medium + large +
red marks Our study, class A 0.53 (0.300.71)
20 Our study, class B 0.48 (0.300.63)
Size of varices
10 Cales et al (20) 0.51 (0.490.54)
Bendtsen et al (21) 0.52  0.17
0
1 2 3 4 5 6 7 8 9 10 Our study, class A, overall 0.34 (0.230.45)
Observers Our study, class B, overall 0.38 (0.260.52)
Our study, class A, grade 2 3 0.60 (0.490.68)
FIGURE 6. Classification of varices scored by each observer using Our study, class A, grade 2 3 red 0.58 (0.440.72)
classification A and grouping together varices of medium and large Our study, class B, large and red 0.46 (0.400.61)
size plus those with red marks. The reference observer is number 10.

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 JPGN  Volume 61, Number 2, August 2015
of the endoscopist. The average k value was 0.38 (standard
deviation 0.16), showing an overall fair agreement. Discrimi-
nation between varices with no risk of bleeding (graded 0 to 1)
and varices at risk (graded 2 to 3) gave a k value of 0.52. Similarly,
Cales et al (20,22,23) performed several studies in adults showing a
good agreement for the presence or the grade of oesophageal varices
and for red signs. These findings are extremely similar to what we
have demonstrated in the present study focused on children
(Table 2). Nevertheless, in our opinion, these levels of agreement
seem suboptimal for such a relevant issue. The variation in grading
of varices shown in our study and previous studies, and therefore the
potential variation in provision of therapy, is sufficiently concern-
ing to require attention to better training of endoscopists to grade
varices more uniformly.
In conclusion, in this multicentre study, we found that pae-
diatric endoscopists working in tertiary care hospitals in Europe are in
agreement on the diagnosis and grading of oesophageal varices in
children. Nevertheless, variation in scoring and therefore in hypothe-
tical provision of therapy was wide. The results of this study support
the feasibility and reliability of multicentre prospective trials in
children with PH, although a better training of paediatric endoscopists
in scoring oesophageal varices is advocated.
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