CLINICAL REVIEW ARTICLE
Systematic Review of the Clinical Disease Severity Indices for Inflammatory Bowel Disease Laith Alrubaiy, MD, MRCP,* Ibtihal Rikaby, MPharm,† Mohamed Sageer, MD,‡ Hayley Anne Hutchings, PhD,* and John Gordon Williams, FRCP, CBE*
Background: Clinical disease severity indices are increasingly being used in choosing treatment and monitoring the response of patients with inflammatory bowel disease (IBD). The aim of this study was to systematically review the clinical disease severity indices in IBD and to appraise their measurement properties and methodological quality. Methods: We searched the MEDLINE, Embase, and PsycINFO databases for original articles describing the development and/or evaluation of one or more of the measurement properties of clinical disease severity indices used in IBD. We assessed these properties (e.g., internal consistency, reliability, validity, responsiveness) using a standardized checklist. Results: We examined the full text of 142 articles that we deemed potentially eligible and identified 22 clinical disease severity indices in IBD. No clinical disease index has met all the required measurement properties. All of the validation studies were not descriptive enough to allow assessment of their methodology.
Conclusions: Although commonly used in multiple clinical trials, none of the clinical disease severity indices in IBD had all the required measurement properties. Further validation studies are required. (Inflamm Bowel Dis 2015;21:2460–2466) Key Words: clinical trials, outcome measures, Crohn’s disease, ulcerative colitis, inflammatory bowel disease
B
ecause of substantial morbidity and mortality related to inflammatory bowel disease (IBD), careful assessment of disease severity is necessary both to assess the efficacy of treatment and to predict disease course. With the development of newer therapies in IBD,1–3 there is growing need to predict disease outcome and risk of relapse during clinical remission. Clinical assessment of disease severity is increasingly being used in choosing treatment and monitoring the response.4–6 Disease severity indices were used as a way to assess the disease severity and were based on clinical, laboratory, histopathological, or endoscopic findings. These indices were used in varying combinations in scales or scoring systems.7,8 Although used in several clinical settings, endoscopic examinations to Received for publication February 12, 2015; Accepted March 13, 2015. From the *Patient & Population Health and Informatics Research, College of Medicine, Swansea University, Swansea, United Kingdom; †Cardiff and Vale University Health Board, Heath Park, Cardiff, United Kingdom; and ‡Lahey Hospital & Medical Center, Burlington, Massachusetts. Supported by the Welsh Clinical Academic Training (WCAT) scheme and its collaboration between Swansea University, Wales Deanery, and the Welsh Government. The authors have no conflicts of interest to disclose. Reprints: Laith Alrubaiy, MD, MRCP, College of Medicine, Swansea University, Room 220, Grove Building, Swansea SA2 8PP, United Kingdom (e-mail: [email protected]). Copyright © 2015 Crohn’s & Colitis Foundation of America, Inc. DOI 10.1097/MIB.0000000000000438 Published online 11 May 2015.
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assess inflammatory activity are invasive, time-consuming, and expensive and therefore are unsuitable for routine use in clinical practice. Indices using imaging techniques9,10 are not readily available and are useful in assessing patients with Crohn’s disease (CD) rather than ulcerative colitis (UC). Therefore, clinical severity indices are still commonly used routinely in clinical practice. Several clinical severity indices have been developed to assess the disease severity and the efficacy of new therapies in IBD. However, there is no agreement about the best clinical index to use in practice, or the definition of remission.7,8,11 To decide which of the clinical indices are most useful in assessing clinical change in IBD, a full understanding of their clinimetric properties is needed. Therefore, the aim of this study was to conduct a systematic review of the available clinical indices in IBD using a robust method of evaluation to assess their psychometric properties.
METHODS Search Strategy This systematic review was undertaken in line with search strategies checklist of the Cochrane review group12 and followed the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) statement.13 We searched the following electronic databases through OvidSP up to October 1, 2014: MEDLINE, Embase, and Inflamm Bowel Dis Volume 21, Number 10, October 2015
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TABLE 1. Quality Criteria for Rating the Results of Measurement Properties14 Properties Reliability Internal consistency
Reproducibility (test–retest reliability)
Measurement error
Validity Content validity
Factor analysis
Construct validity (hypothesis testing)
Responsiveness
Ceiling and floor effects
Interpretability
Ratings
Quality Criteria
+ ? 2 + ? 2 + ? 2
Cronbach’s alpha(s) between 0.70 and 0.90 No information available Cronbach’s alpha(s) ,0.70 or .0.90 or not done ICC or weighted kappa $0.70 OR Pearson’s r $0.80 No information available ICC or weighted kappa ,0.70 OR Pearson’s r ,0.80 Measurement error and SDC are measured. SDC is less than MIC No information available The study did not report a convincing evidence that the measurement error was assessed and/or it was more than MIC
+ ? 2 + ? 2 + ? 2 + ? 2 + ? 2
Appropriate assessment of content validity was performed No information available Content validity was not assessed properly Important factors/domains should explain at least 50% of the variance No information available Important factors/domains explain ,50% of the variance Correlation coefficient for the validity should be in the middle between 0.4–0.8 No information available Correlation coefficient for the validity is not between 0.4 and 0.8 Responsiveness was assessed using an appropriate method No information available Responsiveness was not assessed using an appropriate method #15% of the respondents achieved the highest or lowest possible scores No information available .15% of the respondents achieved the highest or lowest possible scores, despite adequate design and methods Mean and SD scores were presented of at least 4 relevant subgroups of patients, and MIC was defined No information available Mean and SD scores were not presented of at least 4 relevant subgroups of patients, or MIC was not defined
+ ? 2
+, positive rating; ?, no information available or indeterminate rating; 2, negative rating; ICC, intraclass correlation coefficient; MIC, minimally important change; SDC, smallest detectable change.
PsycINFO. Targeted hand searches were carried out. We did the systematic review in 3 parts:
1. We searched the database for studies that included IBD as a major topic. The search terms we used were inflammatory bowel disease, Crohn’s disease, ulcerative colitis, terminal ileitis, regional ileitis, granulomatous enteritis, proctitis, proctocolitis, and colitis. 2. We searched the articles that included clinical indices to assess the disease severity of patients with IBD. The search terms we used were severity of illness index, disease activity, severity index, disease severity, disease assessment, illness index severity, clinical index, health related outcome
measure, disability, health status, health status measures, outcome assessment, treatment, disease severity score, questionnaires, disease severity scale, evaluation, disease evaluation, rating scale, and scoring system. 3. We identified the articles that discussed the validation and psychometric properties of these measures. The search terms we used were psychometrics, reproducibility, reliability, validation studies, validation, face validity, content validity, construct validity, concurrent validity, convergent validity, and discriminant validity. We also identified additional references through targeted searching of journal and related websites. The pool of references www.ibdjournal.org |
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TABLE 2. Cohen’s Criteria for the Level of Credibility of the Outcome Measures18 Category Well-established assessment
Approaching well-established assessment
Promising assessment
Criteria The measure must have been presented (validated) in at least 2 peer-reviewed articles by different investigators or investigatory teams Sufficient detail about the measure to allow critical evaluation and replication (e.g., measure and manual provided or available on request) Detailed information (e.g., statistics presented) indicating good validity and reliability in at least 1 peer-reviewed article The measure must have been presented in at least 2 peer-reviewed articles, which might be by the same investigator or investigatory team Sufficient detail about the measure to allow critical evaluation and replication (e.g., measure and manual provided or available on request) Validity and reliability information either presented in vague terms (e.g., no statistics presented) or only moderate values presented The measure must have been presented in at least 1 peer-reviewed article Sufficient detail about the measure to allow critical evaluation and replication (e.g., measure and manual provided or available on request) Validity and reliability information either presented in vague terms (e.g., no statistics presented) or moderate values presented
and their abstracts were uploaded to EndNote software. Duplicate references were removed using the functionality tools of EndNote and by manual review of the references. We screened the abstracts of the retrieved articles to identify eligible articles.
Selection Criteria We included all original articles in English describing the development and/or evaluation of one or more of the measurement properties (e.g., internal consistency, reliability, validity, responsiveness) of clinical disease severity indices in adult patients with IBD. Two reviewers (L.A. and I.R.) independently screened the titles, abstracts, and references of these articles to obtain any additional articles of relevance. Full texts of eligible articles were obtained. If any disagreement existed regarding the inclusion or exclusion of articles, a third independent reviewer was consulted.
Data Extraction Data from eligible articles were extracted independently using a preprepared data extraction pro forma. The following data were extracted:
1. The clinical indices used to assess severity in IBD. 2. Measurement properties: We assessed the measurement properties of each measure using the Terwee’s checklist14 (Table 1). The measurement properties of each questionnaire were divided into 4 domains15: reliability (including internal consistency, reliability, and measurement error),1 validity (including content validity, structural validity, and hypothesis testing [construct validity]),2 responsiveness, and3 interpretability, which is the ability to interpret the quantitative scores of the outcome measure.14
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3. Methodological quality assessment: We reported on the methodological quality of the included studies using the COSMIN (COnsensus-based Standards for the selection of health Measurement INstruments) checklist.16,17 Each measurement property is assessed against certain quality standards and rated on a 4-point scale (poor, fair, good, or excellent). An overall score for the methodological quality of a certain property is determined by taking the lowest rating. We used COSMIN checklist to assess the methodology of the internal consistency, reliability, measurement error, responsiveness, content validity, construct validity, and factor analysis (structural validity). 4. Levels of the disease measures indices establishment or use in literature: We used Cohen’s criteria18 (Table 2) to determine the overall establishment of each specific clinical disease severity index taking into account the number of peer-reviewed articles that assessed its measurement properties, the information available, and the detailed statistics of the psychometric properties of the measure.
RESULTS Results of the Database Search and Included Studies The database search resulted in the identification of 1210 articles (Fig. 1). References were uploaded into EndNote, and duplicates were removed, leaving 959 articles. After screening the titles and abstracts, 422 articles were excluded because they did not include validation of clinical disease severity indices. The full texts of the remaining 537 articles were obtained and
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FIGURE 1. Flowchart of the systematic search results.
reviewed. We excluded 395 from the 537 articles that did not match the eligibility criteria (290 articles did not include the validation or evaluation of the psychometric properties of the clinical disease severity indices measures, and 105 articles were specifically related to nonclinical disease severity indices). A final total of 142 articles were deemed eligible. After linking multiple reports of the same indices, we identified that these articles covered 22 clinical disease severity indices in IBD (Table 3).
Assessing the Psychometric Properties of the Disease Severity Indices in IBD When evaluating the quality of measurement properties for each of the 22 disease indices, none met all the criteria. A summary of the measurement properties of the commonly used clinical indices is described in Table 4. Although most of the clinical indices had some form of validation, none of these studies covered all the required aspects of validity and
reliability.14 We did not find any study that assessed the ceiling and flooring effect, measurement error, and factor analysis of the clinical disease severity indices in IBD. With the exception of IBD-control questionnaire, internal consistency was either not assessed or not adequate for any of the clinical disease severity indices. Most validation studies examined the construct validity of the clinical indices using other clinical, endoscopic, or biochemical measures of disease severity. Responsiveness and test–retest reliability were not assessed for all clinical indices using the appropriate statistical techniques. Half of the clinical disease indices items were not selected using a valid psychometric approach. In UC, the commonly used clinical indices were the Simple Clinical Colitis Activity Index, Lichtiger Index, and the Mayo Clinic Score. They correlated well with clinical, endoscopic, and biochemical markers of UC activity. They also demonstrated good test–retest reliability and responsiveness.20,27,41–45 www.ibdjournal.org |
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TABLE 3. Summary of the Clinical Disease Severity Indices in IBD For UC Truelove and Witts Severity Index15 Powell-Tuck Index19 Simple Clinical Colitis Severity Index20 Lichtiger Index21 Clinical Activity Index22 Improvement Based on Individual Symptoms Score23 Ulcerative Colitis Clinical Severity Score24 Seo Score25,26 Mayo Clinic Activity Score27 Endoscopic—Clinical Correlation Index28 For CD CDAI29 HBI30 van Hees Index31 Cape Town Index32 Daily Practice Composite Score (DP-6)33 Perianal CD Fistula Drainage Assessment34 Perianal Disease Activity Index35 Perianal Crohn’s Disease Activity Index36 For both CD and UC Manitoba Inflammatory Bowel Disease Index37 IBD-control questionnaire38 German Inflammatory Bowel Disease Activity Index39 Physician Global Assessment40
In CD, the commonly used clinical indices were the Crohn’s Disease Activity Index (CDAI) and the Harvey– Bradshaw Index (HBI). The formal validity and reliability testing of the CDAI29 was not reported in the original article in 1976.29 However, subsequent studies have shown good construct validity using clinical and biochemical assessment of CD.29,31 This good correlation was seen in the HBI.30 All of the studies were not descriptive enough to allow using the COSMIN criteria to assess their methodology. For example, no study described how the missing values were handled or included factor analysis of the questions. Therefore, all indices had their methodology rated as poor to fair. When using Cohen’s criteria to assess the level of establishment, no disease severity index was considered as a well established one. Simple Clinical Colitis Activity Index, Mayo Clinic Score, Clinical Activity Index, Lichtiger Index, CDAI, HBI, Seo Score, Perianal Disease Activity Index, and van Hees Index were approaching the well-establishment status. The rest of the indices were regarded as promising clinical severity indices because they did not achieve all Cohen’s criteria.
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DISCUSSION In recent decades, several clinical indices have been proposed to assess the disease severity in IBD,7,8 but most of them have not been properly validated and have not used robust methodology.4 Using the different scoring systems makes it difficult to compare different clinical trials especially when the endpoints are different. Names of these indices and their abbreviations vary between different publications, which further aggravates the situation. As a result of the multiplicity of indices, no single index has been selected as the “Gold standard.” Some of the disease severity indices that were used in clinical trials and led to approval of many new therapies in IBD34,46 did not go through the appropriate validation process of their validity, reliability, and responsiveness. In this study, we systematically reviewed the frequently used clinical indices for the assessment of severity of CD and UC. In applying the modified Terwee’s criteria,14 we found that all of the measurement properties of the disease severity indices were often neither properly assessed nor clearly reported. Important information on item generation and selection was often very limited in most of these indices. Although subsequent studies have examined the validity and reliability of commonly used indices, they focused on the construct validity, by correlating the indices against other clinical measures of disease severity, which themselves lack proper validation. However, the construct validity is only one form of validity, and other aspects such as responsiveness, internal consistency, and test–retest reliability should be assessed. For example, responsiveness is very important in clinical trials because it allows assessing the change in clinical condition after a therapy or intervention. Furthermore, no study included the assessment of measurement error, factor analysis, and the ceiling or flooring effects in assessing the disease indices. We used a robust quality criteria14 to systematically evaluate the psychometric properties of the identified health-related quality of life measures. We also used COSMIN checklist16 to assess the methodological quality of the properties of the healthrelated quality of life measures in IBD. These criteria are increasingly used in systematic reviews of outcome measures47–52 and have been shown to be valid and reliable.53 The COSMIN and Terwee’s checklists14,16,17 have only recently been introduced and therefore may not be appropriate for the assessment of measures that were developed before its introduction. Although the COSMIN checklist and the quality criteria for the measurement properties were designed to be as objective as possible,16,53 individual reviewer’s judgment can be different. Therefore, 2 reviewers evaluated the included studies, and a third reviewer was consulted in case of disagreement. Previous reviews of clinical disease severity indices in IBD7,8 did not follow a systematic approach or use a standardized checklist in their evaluation. There is no review in the literature that has evaluated the methodological quality of the measurement properties of all clinical indices in IBD.
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TABLE 4. Measurement Properties of the Clinical Disease Severity Indices in IBD Clinical Disease Severity Indices UC TL&W PT CAI LI SCCAI Mayo Clinic Score Seo Index ECCI CD CDAI HBI CTI VH Both MIBDI IBD-control questionnaire
Test–retest Reliability
Content Validity (Item Selection)
Construct Validity
Responsiveness
? + + + + + 2 +
? ? ? + + ? + ?
? + + + + + + +
? 2 + + + + + +
2 ? ? ?
+ + + 2
+ + + +
? ? ? ?
+ +
2 +
+ +
? +
+, positive rating; ?, no information available or indeterminate rating; 2, negative rating. CAI, Clinical Activity Index; CTI, Cape Town Index; ECCI, Endoscopic—Clinical Correlation Index; LI, Lichtiger Index; MIBDI, Manitoba Inflammatory Bowel Disease Index; PT, Powell-Tuck Index; SCCAI, Simple Clinical Colitis Activity Index; TL&W, Truelove and Witts Index; VH, van Hees Index.
To our knowledge, this is the first systematic review of clinical disease severity indices in IBD that has appraised the measurement properties and their methodological quality using a robust and standardized approach. Despite poor validation, a few indices are better than others. Most of the currently available clinical indices are supported by evidence of at least 1 type of reliability or validity, and further validation studies might support their use. The commonly used and validated indices are Simple Clinical Colitis Activity Index, Mayo Clinic Score, and Lichtiger Index in UC and the CDAI and HBI in CD. Several new clinical disease severity indices in IBD are emerging such as the IBD-control questionnaire, which require further validation and psychometric testing. We hope that this review will better guide the use of clinical disease severity indices in various clinical and research settings.
ACKNOWLEDGMENTS Author contributions: L. Alrubaiy was responsible for developing initial drafts of the article, designing the study, obtaining funding, data collection and analysis, and final approval of the study. I. Rikaby contributed to collection and assembly of data and final approval of the article. M. Sageer contributed to data collection and all drafts of the article. H. A. Hutchings and J. G. Williams contributed to designing the study, critical revision of all drafts of the article, and data analysis.
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Systematic Review of the Clinical Disease Severity Indices for Inflammatory Bowel Disease Laith Alrubaiy, MD, MRCP,* Ibtihal Rikaby, MPharm,† Mohamed Sageer, MD,‡ Hayley Anne Hutchings, PhD,* and John Gordon Williams, FRCP, CBE*
Background: Clinical disease severity indices are increasingly being used in choosing treatment and monitoring the response of patients with inflammatory bowel disease (IBD). The aim of this study was to systematically review the clinical disease severity indices in IBD and to appraise their measurement properties and methodological quality. Methods: We searched the MEDLINE, Embase, and PsycINFO databases for original articles describing the development and/or evaluation of one or more of the measurement properties of clinical disease severity indices used in IBD. We assessed these properties (e.g., internal consistency, reliability, validity, responsiveness) using a standardized checklist. Results: We examined the full text of 142 articles that we deemed potentially eligible and identified 22 clinical disease severity indices in IBD. No clinical disease index has met all the required measurement properties. All of the validation studies were not descriptive enough to allow assessment of their methodology.
Conclusions: Although commonly used in multiple clinical trials, none of the clinical disease severity indices in IBD had all the required measurement properties. Further validation studies are required. (Inflamm Bowel Dis 2015;21:2460–2466) Key Words: clinical trials, outcome measures, Crohn’s disease, ulcerative colitis, inflammatory bowel disease
B
ecause of substantial morbidity and mortality related to inflammatory bowel disease (IBD), careful assessment of disease severity is necessary both to assess the efficacy of treatment and to predict disease course. With the development of newer therapies in IBD,1–3 there is growing need to predict disease outcome and risk of relapse during clinical remission. Clinical assessment of disease severity is increasingly being used in choosing treatment and monitoring the response.4–6 Disease severity indices were used as a way to assess the disease severity and were based on clinical, laboratory, histopathological, or endoscopic findings. These indices were used in varying combinations in scales or scoring systems.7,8 Although used in several clinical settings, endoscopic examinations to Received for publication February 12, 2015; Accepted March 13, 2015. From the *Patient & Population Health and Informatics Research, College of Medicine, Swansea University, Swansea, United Kingdom; †Cardiff and Vale University Health Board, Heath Park, Cardiff, United Kingdom; and ‡Lahey Hospital & Medical Center, Burlington, Massachusetts. Supported by the Welsh Clinical Academic Training (WCAT) scheme and its collaboration between Swansea University, Wales Deanery, and the Welsh Government. The authors have no conflicts of interest to disclose. Reprints: Laith Alrubaiy, MD, MRCP, College of Medicine, Swansea University, Room 220, Grove Building, Swansea SA2 8PP, United Kingdom (e-mail: [email protected]). Copyright © 2015 Crohn’s & Colitis Foundation of America, Inc. DOI 10.1097/MIB.0000000000000438 Published online 11 May 2015.
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assess inflammatory activity are invasive, time-consuming, and expensive and therefore are unsuitable for routine use in clinical practice. Indices using imaging techniques9,10 are not readily available and are useful in assessing patients with Crohn’s disease (CD) rather than ulcerative colitis (UC). Therefore, clinical severity indices are still commonly used routinely in clinical practice. Several clinical severity indices have been developed to assess the disease severity and the efficacy of new therapies in IBD. However, there is no agreement about the best clinical index to use in practice, or the definition of remission.7,8,11 To decide which of the clinical indices are most useful in assessing clinical change in IBD, a full understanding of their clinimetric properties is needed. Therefore, the aim of this study was to conduct a systematic review of the available clinical indices in IBD using a robust method of evaluation to assess their psychometric properties.
METHODS Search Strategy This systematic review was undertaken in line with search strategies checklist of the Cochrane review group12 and followed the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) statement.13 We searched the following electronic databases through OvidSP up to October 1, 2014: MEDLINE, Embase, and Inflamm Bowel Dis Volume 21, Number 10, October 2015
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TABLE 1. Quality Criteria for Rating the Results of Measurement Properties14 Properties Reliability Internal consistency
Reproducibility (test–retest reliability)
Measurement error
Validity Content validity
Factor analysis
Construct validity (hypothesis testing)
Responsiveness
Ceiling and floor effects
Interpretability
Ratings
Quality Criteria
+ ? 2 + ? 2 + ? 2
Cronbach’s alpha(s) between 0.70 and 0.90 No information available Cronbach’s alpha(s) ,0.70 or .0.90 or not done ICC or weighted kappa $0.70 OR Pearson’s r $0.80 No information available ICC or weighted kappa ,0.70 OR Pearson’s r ,0.80 Measurement error and SDC are measured. SDC is less than MIC No information available The study did not report a convincing evidence that the measurement error was assessed and/or it was more than MIC
+ ? 2 + ? 2 + ? 2 + ? 2 + ? 2
Appropriate assessment of content validity was performed No information available Content validity was not assessed properly Important factors/domains should explain at least 50% of the variance No information available Important factors/domains explain ,50% of the variance Correlation coefficient for the validity should be in the middle between 0.4–0.8 No information available Correlation coefficient for the validity is not between 0.4 and 0.8 Responsiveness was assessed using an appropriate method No information available Responsiveness was not assessed using an appropriate method #15% of the respondents achieved the highest or lowest possible scores No information available .15% of the respondents achieved the highest or lowest possible scores, despite adequate design and methods Mean and SD scores were presented of at least 4 relevant subgroups of patients, and MIC was defined No information available Mean and SD scores were not presented of at least 4 relevant subgroups of patients, or MIC was not defined
+ ? 2
+, positive rating; ?, no information available or indeterminate rating; 2, negative rating; ICC, intraclass correlation coefficient; MIC, minimally important change; SDC, smallest detectable change.
PsycINFO. Targeted hand searches were carried out. We did the systematic review in 3 parts:
1. We searched the database for studies that included IBD as a major topic. The search terms we used were inflammatory bowel disease, Crohn’s disease, ulcerative colitis, terminal ileitis, regional ileitis, granulomatous enteritis, proctitis, proctocolitis, and colitis. 2. We searched the articles that included clinical indices to assess the disease severity of patients with IBD. The search terms we used were severity of illness index, disease activity, severity index, disease severity, disease assessment, illness index severity, clinical index, health related outcome
measure, disability, health status, health status measures, outcome assessment, treatment, disease severity score, questionnaires, disease severity scale, evaluation, disease evaluation, rating scale, and scoring system. 3. We identified the articles that discussed the validation and psychometric properties of these measures. The search terms we used were psychometrics, reproducibility, reliability, validation studies, validation, face validity, content validity, construct validity, concurrent validity, convergent validity, and discriminant validity. We also identified additional references through targeted searching of journal and related websites. The pool of references www.ibdjournal.org |
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TABLE 2. Cohen’s Criteria for the Level of Credibility of the Outcome Measures18 Category Well-established assessment
Approaching well-established assessment
Promising assessment
Criteria The measure must have been presented (validated) in at least 2 peer-reviewed articles by different investigators or investigatory teams Sufficient detail about the measure to allow critical evaluation and replication (e.g., measure and manual provided or available on request) Detailed information (e.g., statistics presented) indicating good validity and reliability in at least 1 peer-reviewed article The measure must have been presented in at least 2 peer-reviewed articles, which might be by the same investigator or investigatory team Sufficient detail about the measure to allow critical evaluation and replication (e.g., measure and manual provided or available on request) Validity and reliability information either presented in vague terms (e.g., no statistics presented) or only moderate values presented The measure must have been presented in at least 1 peer-reviewed article Sufficient detail about the measure to allow critical evaluation and replication (e.g., measure and manual provided or available on request) Validity and reliability information either presented in vague terms (e.g., no statistics presented) or moderate values presented
and their abstracts were uploaded to EndNote software. Duplicate references were removed using the functionality tools of EndNote and by manual review of the references. We screened the abstracts of the retrieved articles to identify eligible articles.
Selection Criteria We included all original articles in English describing the development and/or evaluation of one or more of the measurement properties (e.g., internal consistency, reliability, validity, responsiveness) of clinical disease severity indices in adult patients with IBD. Two reviewers (L.A. and I.R.) independently screened the titles, abstracts, and references of these articles to obtain any additional articles of relevance. Full texts of eligible articles were obtained. If any disagreement existed regarding the inclusion or exclusion of articles, a third independent reviewer was consulted.
Data Extraction Data from eligible articles were extracted independently using a preprepared data extraction pro forma. The following data were extracted:
1. The clinical indices used to assess severity in IBD. 2. Measurement properties: We assessed the measurement properties of each measure using the Terwee’s checklist14 (Table 1). The measurement properties of each questionnaire were divided into 4 domains15: reliability (including internal consistency, reliability, and measurement error),1 validity (including content validity, structural validity, and hypothesis testing [construct validity]),2 responsiveness, and3 interpretability, which is the ability to interpret the quantitative scores of the outcome measure.14
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3. Methodological quality assessment: We reported on the methodological quality of the included studies using the COSMIN (COnsensus-based Standards for the selection of health Measurement INstruments) checklist.16,17 Each measurement property is assessed against certain quality standards and rated on a 4-point scale (poor, fair, good, or excellent). An overall score for the methodological quality of a certain property is determined by taking the lowest rating. We used COSMIN checklist to assess the methodology of the internal consistency, reliability, measurement error, responsiveness, content validity, construct validity, and factor analysis (structural validity). 4. Levels of the disease measures indices establishment or use in literature: We used Cohen’s criteria18 (Table 2) to determine the overall establishment of each specific clinical disease severity index taking into account the number of peer-reviewed articles that assessed its measurement properties, the information available, and the detailed statistics of the psychometric properties of the measure.
RESULTS Results of the Database Search and Included Studies The database search resulted in the identification of 1210 articles (Fig. 1). References were uploaded into EndNote, and duplicates were removed, leaving 959 articles. After screening the titles and abstracts, 422 articles were excluded because they did not include validation of clinical disease severity indices. The full texts of the remaining 537 articles were obtained and
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FIGURE 1. Flowchart of the systematic search results.
reviewed. We excluded 395 from the 537 articles that did not match the eligibility criteria (290 articles did not include the validation or evaluation of the psychometric properties of the clinical disease severity indices measures, and 105 articles were specifically related to nonclinical disease severity indices). A final total of 142 articles were deemed eligible. After linking multiple reports of the same indices, we identified that these articles covered 22 clinical disease severity indices in IBD (Table 3).
Assessing the Psychometric Properties of the Disease Severity Indices in IBD When evaluating the quality of measurement properties for each of the 22 disease indices, none met all the criteria. A summary of the measurement properties of the commonly used clinical indices is described in Table 4. Although most of the clinical indices had some form of validation, none of these studies covered all the required aspects of validity and
reliability.14 We did not find any study that assessed the ceiling and flooring effect, measurement error, and factor analysis of the clinical disease severity indices in IBD. With the exception of IBD-control questionnaire, internal consistency was either not assessed or not adequate for any of the clinical disease severity indices. Most validation studies examined the construct validity of the clinical indices using other clinical, endoscopic, or biochemical measures of disease severity. Responsiveness and test–retest reliability were not assessed for all clinical indices using the appropriate statistical techniques. Half of the clinical disease indices items were not selected using a valid psychometric approach. In UC, the commonly used clinical indices were the Simple Clinical Colitis Activity Index, Lichtiger Index, and the Mayo Clinic Score. They correlated well with clinical, endoscopic, and biochemical markers of UC activity. They also demonstrated good test–retest reliability and responsiveness.20,27,41–45 www.ibdjournal.org |
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TABLE 3. Summary of the Clinical Disease Severity Indices in IBD For UC Truelove and Witts Severity Index15 Powell-Tuck Index19 Simple Clinical Colitis Severity Index20 Lichtiger Index21 Clinical Activity Index22 Improvement Based on Individual Symptoms Score23 Ulcerative Colitis Clinical Severity Score24 Seo Score25,26 Mayo Clinic Activity Score27 Endoscopic—Clinical Correlation Index28 For CD CDAI29 HBI30 van Hees Index31 Cape Town Index32 Daily Practice Composite Score (DP-6)33 Perianal CD Fistula Drainage Assessment34 Perianal Disease Activity Index35 Perianal Crohn’s Disease Activity Index36 For both CD and UC Manitoba Inflammatory Bowel Disease Index37 IBD-control questionnaire38 German Inflammatory Bowel Disease Activity Index39 Physician Global Assessment40
In CD, the commonly used clinical indices were the Crohn’s Disease Activity Index (CDAI) and the Harvey– Bradshaw Index (HBI). The formal validity and reliability testing of the CDAI29 was not reported in the original article in 1976.29 However, subsequent studies have shown good construct validity using clinical and biochemical assessment of CD.29,31 This good correlation was seen in the HBI.30 All of the studies were not descriptive enough to allow using the COSMIN criteria to assess their methodology. For example, no study described how the missing values were handled or included factor analysis of the questions. Therefore, all indices had their methodology rated as poor to fair. When using Cohen’s criteria to assess the level of establishment, no disease severity index was considered as a well established one. Simple Clinical Colitis Activity Index, Mayo Clinic Score, Clinical Activity Index, Lichtiger Index, CDAI, HBI, Seo Score, Perianal Disease Activity Index, and van Hees Index were approaching the well-establishment status. The rest of the indices were regarded as promising clinical severity indices because they did not achieve all Cohen’s criteria.
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DISCUSSION In recent decades, several clinical indices have been proposed to assess the disease severity in IBD,7,8 but most of them have not been properly validated and have not used robust methodology.4 Using the different scoring systems makes it difficult to compare different clinical trials especially when the endpoints are different. Names of these indices and their abbreviations vary between different publications, which further aggravates the situation. As a result of the multiplicity of indices, no single index has been selected as the “Gold standard.” Some of the disease severity indices that were used in clinical trials and led to approval of many new therapies in IBD34,46 did not go through the appropriate validation process of their validity, reliability, and responsiveness. In this study, we systematically reviewed the frequently used clinical indices for the assessment of severity of CD and UC. In applying the modified Terwee’s criteria,14 we found that all of the measurement properties of the disease severity indices were often neither properly assessed nor clearly reported. Important information on item generation and selection was often very limited in most of these indices. Although subsequent studies have examined the validity and reliability of commonly used indices, they focused on the construct validity, by correlating the indices against other clinical measures of disease severity, which themselves lack proper validation. However, the construct validity is only one form of validity, and other aspects such as responsiveness, internal consistency, and test–retest reliability should be assessed. For example, responsiveness is very important in clinical trials because it allows assessing the change in clinical condition after a therapy or intervention. Furthermore, no study included the assessment of measurement error, factor analysis, and the ceiling or flooring effects in assessing the disease indices. We used a robust quality criteria14 to systematically evaluate the psychometric properties of the identified health-related quality of life measures. We also used COSMIN checklist16 to assess the methodological quality of the properties of the healthrelated quality of life measures in IBD. These criteria are increasingly used in systematic reviews of outcome measures47–52 and have been shown to be valid and reliable.53 The COSMIN and Terwee’s checklists14,16,17 have only recently been introduced and therefore may not be appropriate for the assessment of measures that were developed before its introduction. Although the COSMIN checklist and the quality criteria for the measurement properties were designed to be as objective as possible,16,53 individual reviewer’s judgment can be different. Therefore, 2 reviewers evaluated the included studies, and a third reviewer was consulted in case of disagreement. Previous reviews of clinical disease severity indices in IBD7,8 did not follow a systematic approach or use a standardized checklist in their evaluation. There is no review in the literature that has evaluated the methodological quality of the measurement properties of all clinical indices in IBD.
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TABLE 4. Measurement Properties of the Clinical Disease Severity Indices in IBD Clinical Disease Severity Indices UC TL&W PT CAI LI SCCAI Mayo Clinic Score Seo Index ECCI CD CDAI HBI CTI VH Both MIBDI IBD-control questionnaire
Test–retest Reliability
Content Validity (Item Selection)
Construct Validity
Responsiveness
? + + + + + 2 +
? ? ? + + ? + ?
? + + + + + + +
? 2 + + + + + +
2 ? ? ?
+ + + 2
+ + + +
? ? ? ?
+ +
2 +
+ +
? +
+, positive rating; ?, no information available or indeterminate rating; 2, negative rating. CAI, Clinical Activity Index; CTI, Cape Town Index; ECCI, Endoscopic—Clinical Correlation Index; LI, Lichtiger Index; MIBDI, Manitoba Inflammatory Bowel Disease Index; PT, Powell-Tuck Index; SCCAI, Simple Clinical Colitis Activity Index; TL&W, Truelove and Witts Index; VH, van Hees Index.
To our knowledge, this is the first systematic review of clinical disease severity indices in IBD that has appraised the measurement properties and their methodological quality using a robust and standardized approach. Despite poor validation, a few indices are better than others. Most of the currently available clinical indices are supported by evidence of at least 1 type of reliability or validity, and further validation studies might support their use. The commonly used and validated indices are Simple Clinical Colitis Activity Index, Mayo Clinic Score, and Lichtiger Index in UC and the CDAI and HBI in CD. Several new clinical disease severity indices in IBD are emerging such as the IBD-control questionnaire, which require further validation and psychometric testing. We hope that this review will better guide the use of clinical disease severity indices in various clinical and research settings.
ACKNOWLEDGMENTS Author contributions: L. Alrubaiy was responsible for developing initial drafts of the article, designing the study, obtaining funding, data collection and analysis, and final approval of the study. I. Rikaby contributed to collection and assembly of data and final approval of the article. M. Sageer contributed to data collection and all drafts of the article. H. A. Hutchings and J. G. Williams contributed to designing the study, critical revision of all drafts of the article, and data analysis.
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