Exploring the agreement between diagnostic criteria for IBS in primary care in Greece
BMC Research Notes
Project Note Exploring the agreement between diagnostic criteria for IBS in primary care in Greece
Foteini Anastasiou 2
Ioannis A Mouzas 1
Joanna Moschandreas 0
Elias Kouroumalis 1
Christos Lionis 2
0 Biostatistics Laboratory, Department of Social Medicine, Faculty of Medicine, University of Crete , Heraklion, Crete , Greece
1 Department of Gastroenterology, University Hospital of Heraklion , Heraklion, Crete , Greece
2 Clinic of Social and Family Medicine, Department of Social Medicine, Faculty of Medicine, University of Crete , Heraklion, Crete , Greece
Background: Irritable Bowel Syndrome (IBS) is frequently diagnosed in primary care. Its diagnosis is based on diagnostic criteria but their use is limited in primary care. We aimed to assess the diagnostic agreement between the older (Manning's and Rome II) and the new (Rome III) criteria for the diagnosis of IBS in primary care in Greece. Methods: Medical records of 5 Health Centers in rural Crete, Greece, were reviewed for a fouryear period and patients with the diagnosis of IBS were invited to a structured interview. Kappa agreement of the Rome III criteria with the criteria of Manning and Rome II was estimated. One hundred and twenty three patients were eligible for interview and 67 (54.5%) participated. Fortysix (69%) fulfilled the Manning, 32(48%) the Rome II, and 16(24%) the Rome III criteria. Twentyseven (40%) patients were identified as IBS according to the questionnaire for the identification of functional gastrointestinal diseases (FGIDs). The agreement of Rome III with Manning criteria was poor (kappa = 0.25). The agreement between the FGIDs questionnaire and the Manning, Rome II and Rome III criteria was: kappa = 0.30, 0.31 and 0.24 respectively. Moderate agreement was found between the Rome II and III criteria (kappa = 0.51). Conclusion: Questionnaires and criteria deriving from expert's consensus meetings or tertiary hospitals are not easy to apply in rural primary care where symptoms are often underestimated by patients and complicated questions can be confusing.
Irritable Bowel Syndrome (IBS) is frequently diagnosed in
primary care. [
] During the last decades efforts to provide
reliable diagnostic criteria for IBS have been undertaken,
starting with the criteria of Manning [
] and the
consensuses of Rome I, II and III. [
] Classification criteria such
as Rome II developed through experts consensus may be
less applicable to primary care IBS patients  and their
implementation in primary and secondary health care
settings does not seem to be widely adopted. [
In Greece the subject of functional gastrointestinal
disorders in primary health care seems to be neglected.[
recent study in rural Crete revealed that primary care
physicians failed to diagnose these disorders.[
crosssectional study led to the development of a database of
patients with IBS. The advent of the new consensus (Rome
III) on the diagnosis of IBS was an important incentive to
explore to what extent the application of the new
standards alters the diagnosis previously made within the
primary care setting in Crete. This paper seeks to explore
issues of diagnostic suitability and applicability of
different classification criteria when they are used for IBS
patients in primary care.
Setting and study population
The medical records of four Primary Health Care (PHC)
centers and one primary surgery were reviewed from
March 1996 till February 2000 with a methodology
] All the patients with the diagnosis
of IBS or spastic colitis or functional disorders of the large
bowel were pooled together as IBS patients (ICPC 2: D93/
ICD10: K58). The estimated occurrence rate of the IBS
patients in this cross-sectional study was 1.2 per 1000
] This low IBS rate was attributed to the free
access that Greek patients have to public health services
without prior referral from their primary care centre. It
was also uncertain to what extend patients with IBS were
experiencing minor symptoms and thus they did not seek
medical care from their primary care physicians. [
Patients with IBS in this Cretan database were mostly
women older than 70 and this fact can explain the high
occurrence rate of IBS in people older than 65 years.
However, both findings from this report need to be verified in
future studies in this region.
All the identified IBS patients were considered eligible for
a structured interview.
Each of the eligible patients was personally invited to a
semi-structured interview. All interviews were performed
by the same researcher during scheduled home visits and
were based on a detailed personal and family history
questionnaire. Co-morbidity and medication were
documented both through direct questions during the
interview and by patient's personal insurance book. The
Manning criteria for IBS and the Rome II criteria for IBS
and dyspepsia were applied. [
The questionnaire for the identification of dyspepsia in
the general population (IDGP), which was translated and
validated into Greek [
] was applied in order to
document co-morbidity with dyspepsia and GERD. It consists
of 11 main questions answered by yes or no, on upper
gastrointestinal symptoms together with frequencies and
consultation behavior, and one open question. The
questionnaire for the identification of functional
gastrointestinal disorders (FGIDs) [
] was also used. This
questionnaire based on the Rome I criteria through nine
different sets of questions provides a detailed picture of
patients gastrointestinal problems. Main questions on
symptoms duration from this questionnaire combined
with Rome's II three main diagnostic criteria extended our
comparison towards Rome III criteria retrospectively. All
the diagnostic criteria and the questions used for the
Rome III are shown in Table 1.
Comparisons of the characteristics of participants and
non-participants were made using the chi-squared test for
categorical variables and the non-parametric
Mann-Whitney test for possible age differences, as age appeared
negatively skewed in each group. In the FGIDs questionnaire
age is a criterion for the differential diagnosis of organic
disease against IBS thus no comparison with age was
performed for this questionnaire. The chance-corrected
agreement between the Manning and the Rome II criteria
compared with the new Rome III criteria was estimated
using Cohen's kappa [
]. Confidence intervals were
calculated using the asymptotic variance, based on the
normal approximation to the distribution of the kappa
]. Strength of agreement was interpreted using
the following categories: < 0.20 poor, 0.20–0.40 fair,
0.41–0.60 moderate, 0.61–0.80 good, over 0.80 very
] Possible age and sex differences between the
proportions classified with IBS using the three criteria
(Manning's, Rome II, and Rome III) were assessed using
the Mann-Whitney test and Fisher's exact test respectively.
Confidence intervals for single proportions, and for
differences between proportions, were calculated using the
normal approximation to the binomial distribution. SPSS
version 15 was used for all statistical analyses (SPSS for
Windows, release 15.0.0, and 6/9/2006. Chicago: SPSS
Inc). The significance level was set to 5%.
This study was approved by the Ethical Committee of the
University Hospital of Heraklion, Crete, Greece (RN:
7173/2000). All participating patients were informed
about the purposes of the study and gave their consent.
The original database included 146 patients identified
with the diagnosis of IBS. [
] Ten double entries were
located. For thirteen entries, no date of birth was
available. These patients were excluded due to the high
possibility of synonymies. Finally, 123 patients were contacted for
interview. Sixty-seven patients participated in the
interview (54.5%). A flowchart including reasons for
non-participation is shown in Figure 1. The mean interval period
between the original doctor's diagnosis and the interview
was 6.4 (SD: 1.24) years. The characteristics of patients
with IBS according to participation status are presented in
Table 2. Age distribution was not found to differ between
the two groups (Mann-Whitney z = -1.543, p = 0.123).
There was weak evidence of an association between sex
and participation status (X2 = 4.24 on 1 df, p = 0.039),
with more male non-participants than expected (25
observed, 20 expected) and fewer female non-participants
(31 observed, 36 expected).
Old vs new diagnostic criteria
Of the 67 IBS patients that finally participated in the
interview, 46 (69%, 95% CI: 58%–80%) fulfilled two or more
of the Manning criteria by the time of interview.
Thirtytwo subjects (48%, 95% CI: 36%–60%) fulfilled the
Rome II criteria, all of them also fulfilled the criteria of
Manning. The modified Rome III questions/criteria were
satisfied by 16 subjects (24%, 95% CI: 14%–34%), all of
whom also fulfilled both Rome II and Manning criteria.
Twenty-seven patients (40%, 95% CI: 29%–52%)
satisfied the conditions for IBS according to the FGIDs
Poor agreement was found between the Rome III and the
Manning criteria, kappa = 0.25 (95% CI: 0.12 to 0.38).
Only moderate agreement was found between the Rome
II and Rome III criteria, kappa 0.51(95% CI: 0.33 to 0.69).
There was also poor agreement between the FGIDs
questionnaire and the Manning, Rome II and the Rome III
criteria with kappa = 0.30 (95% CI: 0.12 to 0.49), kappa = 0.
31 (95% CI: 0.08 to 0.53) and kappa = 0.24 (95% CI: 0.01
to 0.46) respectively. Gender and age were not statistically
significant risk factors for the positive diagnosis of IBS
with any of the diagnostic criteria.
Five (7.5%, 95% CI: 1.2%–13.8%) of the participants
stated that they did not suffer from any gastrointestinal
symptom in the last 12 months prior to the interview.
The investigation for co morbidity with other
gastrointestinal disorders revealed 31 patients (46%, 95% CI: 34%–
58%) experiencing GERD like symptoms according to the
IDGP questionnaire. Within this group of patients 24
(77.4%) fulfilled the criteria of Manning, whereas 15
(48.4%) and 8 (25.8%) fulfilled the Rome II and III
criteria respectively. Nine of the 67 patients (13%, 95% CI: 5%
to 22%) patients had undergone cholecystectomy or
experienced gall bladder problems in the past. Seven (10.4%,
95% CI: 2.5% to18%) patients had dyspepsia according
to the IDGP questionnaire and one patient had FD
according to Rome II. Four of the patients (6%, 95% CI:
0.3% to12%) had been diagnosed with cancer (1 gastric,
1 ovarian, 2 cervical).
Sixteen patients were suffering from one or more
gastrointestinal symptom (24%, 95% CI: 14% to 34%) without
fulfilling any of the IBS criteria. Symptoms more
frequently than 6 times per year were reported by 59 (88%)
of the participants whereas 3 (0.4%) had symptoms less
The main findings of the study
In our study population more patients fulfilled Manning's
criteria, fewer the Rome II and even fewer the Rome III
criteria which proved the most restrictive. In previous studies
the criteria of Manning and the Rome III criteria were
found more sensitive in diagnosing IBS patients in
primary care compared to Rome II. [
] The complexity
of questions about the duration of symptoms might have
played an important role for the difference between the
Rome II and III criteria. It is also supported that criteria
that are based on the frequency of symptoms have lower
prevalence values compared to criteria based on the
presence of symptoms. [
] Our findings indicate that IBS
diagnosis in rural areas of Crete has not been based on
complex criteria. In the same vein, the FGIDs
questionnaire revealed fewer patients as having IBS than the
Manning and Rome II criteria and showed low agreement
compared with all the criteria. This questionnaire was
expected to be more restrictive in the primary care
population as there is a strong argument that primary care
patients have different disease characteristics than
High co-morbidity with GERD like symptoms was noted.
The observed rate in our study (46%) was among the
highest reported according to a review of the international
] It is difficult to explain this prominent
overlap and although both conditions are highly
prevalent, the overlapping symptoms are lately attributed to a
FFliogwurceha1rt of IBS patients
Flow chart of IBS patients.
possible common disease process. [
] Co morbidity with
dyspepsia was relatively low (10.4%) compared with
other studies. [
The study findings in the light of other studies
Criteria developed by specialists have been criticized for
low performance in primary care.[
] Skepticism as
to the degree of relevance of Rome diagnostic criteria for
IBS with everyday clinical primary practice is developing
and authors have suggested that the next consensus
meeting on IBS should be interdisciplinary. [
] Our results
are in agreement with international literature on the low
application of diagnostic criteria for IBS and especially the
Rome II. The Rome III criteria are considered as less
restrictive and thus closer to primary care reality,[
but in our study this role was not verified. In the Greek
primary setting the number of visits to the doctor due to
IBS was found low  compared to international data. In
another study from Crete, again, IBS patients reported that
they did not visit the PHC centre for their IBS problems
] All data form a puzzle showing that in IBS
patients in rural areas of Crete, both actual and as
perceived by individuals, symptoms are rather
underestimated. Further research is needed to confirm it.
Limitations of the study
Our study used the database of IBS patients identified in
medical records in a retrospective research. Information as
to what criteria were applied by primary care doctors was
not available. In most cases the diagnosis alone was the
only available data. Also poor demographic data entries
resulted in high numbers of excluded or non-participating
patients limiting in this way the strength of the results. For
the majority of the non participating patients there were
no available data about the presence of gastrointestinal
symptoms. Thus a potential selection bias could be
addressed. It should also be noted that although Cohen's
kappa statistic is an extremely widely used measure of
agreement at the present time in the biomedical literature,
certain "paradoxes" in its interpretation have been noted
in relation to unbalanced marginal totals, and also its
dependence on the prevalence of the condition [
Another limitation was the use of modified questions
matching the Rome III instead of the actual Rome III
criteria for a retrospective comparison. A similar approach
was attempted in another study the results of which
followed the pre existing research on Rome III. [
study provides a hint on the application of the Rome III in
IBS patients in rural Crete at a time where no other
information is available.
The 6.4 years interval between the first diagnosis and the
structured interview is another limitation as it could allow
changes and overlaps with other gastrointestinal diseases,
a finding common in IBS patients. [
]This interval did
not allow a direct comparison between the criteria and
doctor's diagnosis, but the retrospective comparison
between criteria at the time of interview was possible.
Implementation to practice and suggestions for future research
The low agreement between older and new criteria and
the tendency for greater fulfillment of the criteria of
Manning; reveal the necessity for a different approach to the
diagnosis of IBS in primary care in rural areas of Greece.
This approach has been also highlighted in a consensus
development for the diagnosis of IBS in primary care. [
Clinical manifestations of IBS and co morbidity with
other gastrointestinal diseases; both in primary care
patient and the general population in rural Greece; should
also be investigated in order to obtain a clear picture of the
In Greek primary care, international diagnostic criteria
display low agreement for the diagnosis of IBS. Amongst
these, the newest criteria display worse results than
expected. Questionnaires and criteria deriving from
tertiary hospitals or expert's consensus meetings seem to be
applied with difficulty in rural primary care where
symptoms are underestimated by patients and complicated
questions can be confusing.
IBS: Irritable Bowel Syndrome; IDGP: Identification of
Dyspepsia in the General Population questionnaire;
FGIDs: Identification of Functional Gastrointestinal
Diseases questionnaire; GERD: Gastro Esophageal Reflux
Disease; PHC: Primary Health Centre
The research programme received a grand from
CL, HC, IM, and FA conceived the idea. CL supervised the
collection of data. FA collected and analysed the data,
performed the interviews. JM performed all statistical
analysis. FA, JM and CL prepared the first draft. All authors read
and approved the final version of the manuscript.
The authors express their gratitude for the support of the study to the
directors and staff at the participating PHC Centres on Crete. Specific
thanks are extended to Dr N Antonakis, GP at the Anogia Health Centre;
Dr M Bathianaki, GP at the Archanes Primary Health Care Unit; Dr A
Batikas, GP at the Perama Health Centre, Dr M Chatziarsenis, Medical Director
at the Neapolis Health Centre-General Hospital; and Mrs A Romanidou,
midwife at the Spili Health Centre, for their contribution to the data
collection. Special thanks to Dr Ada Markaki for her valuable corrections on
the linguistics of the manuscript.
1. Thompson WG , Heaton KW , Smyth GT , Smyth C : Irritable bowel syndrome in general practice: prevalence, characteristics, and referral . Gut 2000 , 46 : 78 - 82 .
2. Manning AP , Thompson WG , Heaton KW , Morris AF : Towards positive diagnosis of the irritable bowel . Br Med J 1978 , 2 ( 6138 ): 653 - 654 .
3. Talley NJ , Stanghellini V , Heading RC , Koch KL , Malagelada JR , Tytgat GNJ : Rome II: A Multinational Consensus Document on Functional Gastrointestinal Disorders, Functional gastroduodenal disorders . Gut 1999 , 45 ( Suppl 2 ): ii37 - ii42 .
4. Tack J , Talley NJ , Camilleri M , Holtmann G , Hu PJ , Malagelada J-R , Stanghellini V : Functional Gastroduodenal Disorders . Gastroenterology 2006 , 130 : 1466 - 1479 .
5. Vandvik PO , Aabakken L , Farup PG : Diagnosing irritable bowel syndrome: poor agreement between general practitioners and the Rome II criteria . Scand J Gastroenterol 2004 , 39 : 448 - 453 .
6. Lea R , Hopkins V , Hastleton J , Houghton LA , Whorwell PJ : Diagnostic criteria for irritable bowel syndrome: utility and applicability in clinical practice . Digestion 2004 , 70 : 207 - 209 .
7. Spiegel MR : Do physicians follow evidence-based guidelines in the diagnostic work-up of IBS? Nat Clin Pract Gastroenterol Hepatol 2007 , 4 : 296 - 297 .
8. Lionis C , Olsen-Faresjo A , Anastasiou F , Wallander MA , Johansson S , Faresjo T : Measuring the frequency of functional gastrointestinal disorders in rural Crete: a need for improving primary care physicians' diagnostic skills . Rural Remote Health 2005 , 5 : 409 .
9. Papatheodoridis GV , Karamanolis DG : Prevalence and impact of upper and lower gastrointestinal symptoms in the Greek urban general population . Scand J Gastroenterol 2005 , 40 : 412 - 421 .
10. Kennedy T , Jones R : Development of a postal health status questionnaire to identify people with dyspepsia in the general population . Scand J Prim Health Care 1995 , 13 : 243 - 249 .
11. Anastasiou F , Antonakis N , Chaireti G , Theodorakis PN , Lionis C : Identifying dyspepsia in the Greek population: translation and validation of a questionnaire . BMC Public Health 2006 , 6 : 56 .
12. Mouzas IA , Fragiadakis N , Moschandreas J , Karachristos A , Skordilis P , Kouroumalis E , Manousos ON : Validation and results of a questionnaire for functional bowel disease in out-patients . BMC Public Health 2002 , 2 : 8 .
13. Cohen J : A coefficient of agreement for nominal scales . Educ Psychol Meas 1960 , 20 : 37 - 46 .
14. Altman DG : Practical Statistics for Medical Research Chapman & Hall 1991 : 404 - 407 .
15. Longstreth GF : Definition and classification of irritable bowel syndrome: current consensus and controversies . Gastroenterol Clin North Am 2005 , 34 : 173 - 187 .
16. Sperber AD , Shvartzman P , Friger M , Fich A : A comparative reappraisal of the Rome II and Rome III diagnostic criteria: are we getting closer to the 'true' prevalence of irritable bowel syndrome? Eur J Gastroenterol Hepatol 2007 , 19 : 441 - 447 .
17. Gwee KA : Irritable bowel syndrome and the Rome III criteria: for better or for worse? Eur J Gastroenterol Hepatol 2007 , 19 : 437 - 439 .
18. Rubin G , De Wit N , Meineche-Schmidt V , Seifert B , Hall N , Hugin P : The diagnosis of IBS in primary care: consensus development using nominal group technique . Family Practice Fam Pract 2006 , 23 : 687 - 692 .
19. Agreus L : Rome? Manning? Who cares? Am j Gastroenterol 2000 , 95 : 2816 - 2824 .
20. Agréus L , Svärdsudd K , Nyrén O , Tibblin G : Irritable bowel syndrome and dyspepsia in the general population: overlap and lack of stability over time . Gastroenterology 1995 , 109 : 671 - 680 .
21. Nastaskin I , Mehdikhani E , Conklin J , Park S , Pimentel M : Studying the overlap between IBS and GERD: a systematic review of the literature . Dig Dis Sci 2006 , 51 : 2113 - 2120 .
22. Talley NJ : Overlapping abdominal symptoms: why do GERD and IBS often coexist? Drugs Today ( Barc ) 2006 , 42 ( Suppl B ): 3 - 8 .
23. Gladman LM , Gorard DA : General practitioner and hospital specialist attitudes to functional gastrointestinal disorders . Aliment Pharmacol Ther 2003 , 17 : 651 - 654 .
24. Charapata C , Mertz H : Physician knowledge of Rome symptom criteria for irritable bowel syndrome is poor among non-gastroenterologists . Neurogastroenterol Motil 2006 , 18 : 211 - 216 .
25. Enck P , Martens U : [ The Next Consensus for the Irritable Bowel Syndrome has to be Interdisciplinary.][Article in German]. Z Gastroenterol 2008 , 46 : 211 - 215 .
26. Vasilopoulos T , Efthymiou C , Zagora E : A further exploration of patients with IBS in rural Crete . Rural Remote Health 2006 , 6 : 626 .
27. Byrt T , Bishop J , Carlin JB : Bias, Prevalence and Kappa . J Clin Epidemiol 1993 , 46 ( 5 ): 423 - 429 .
28. El-Serag HB , Pilgrim P , Schoenfeld P : Systemic review: Natural history of irritable bowel syndrome . Aliment Pharmacol Ther 2004 , 19 : 861 - 870 .