Endoscopic scoring indices for evaluation of disease activity in ulcerative colitis

Nadia Mohammed Vashist; Mark Samaan; Mahmoud H Mosli; Claire E Parker; John K MacDonald; Sigrid A Nelson; GY Zou; Brian G Feagan; Reena Khanna; Vipul Jairath

doi:10.1002/14651858.CD011450.pub2

Table 1. Partially validated endoscopic scoring indices

	Index	Reference	Validation study ID
1	Azzolini Classification	Azzolini 2005	Jun 2008
2	Baron Score	Baron 1964	Burger 2011; Hirai 2010; Jun 2008; Osada 2010; Thomas 2009; Walsh 2009
3	Blackstone Endoscopic Interpretation	Blackstone 1984	Osada 2010
4	CGSUC	Zou 2005	Jun 2008
5	Endoscopic Activity Index (EAI)	Naganuma 2010	de Lange 2004; Naganuma 2010
6	Jeroen Score	Jeroen 2002	Jun 2008
7	Magnifying Colonoscopy Grade	Nishio 2006	Nishio 2006
8	Matts Score	Matts 1961	Naganuma 2010; Osada 2010
9	Mayo Clinic Endoscopic Subscore	Schroeder 1987	Daperno 2011; Dhanda 2012; Osada 2010; Rubin 2012; Walsh 2009
10	Modified Mayo Clinic Endoscopic Subscore	Lobatón 2015	Levesque 2014
11	Modified Baron Score	Feagan 2005	Jun 2008; Levesque 2014; Walsh 2009
12	Osada Score (Modified 6‐Point Activity Index)	Osada 2010	Osada 2010
13	Rachmilewitz Endocopic Score	Rachmilewitz 1989	Hirai 2010; Naganuma 2010; Schoepfer 2009
14	St. Mark's Index (Powell‐Tuck Index)	Powell‐Tuck 1982	Higgins 2005a
15	Ulcerative Colitis Colonoscopic Index of Severity (UCCIS)	Samuel 2013	Samuel 2013
16	Ulcerative Coltiis Disease Activity Index (endoscopic) (Sutherland Index)	Sutherland 1987	Higgins 2005a
17	Ulcerative Colitis Endoscopic Index of Severity (UCEIS)	Travis 2012	Levesque 2014; Travis 2013
18	Truelove and Witts Sigmoidoscopic Score	Truelove 1955	Jun 2008
19	Watson Grade	Kiesslich 2012	Kiesslich 2012

Table 1. Partially validated endoscopic scoring indices

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Table 2. Non‐validated endoscopic scoring indices

	Index	Reference
1	Beattie Score	Beattie 1996
2	Binder Score	Binder 1970
3	Carbonnel Score	Carbonnel 1994
4	Danielsson‐Löfberg Score	Danielsson 1987; Löfberg 1994
5	Dick Score	Dick 1964
6	Friedmann Score	Friedmann 1986
7	Froslie Endoscopic Score	Froslie 2007
8	Lemann Score	Lemann 1995
9	Levine Score	Levine 2002
10	Lindgren Score	Lindgren 2002
11	Maier Score	Maier 1988
12	McPhee Proctoscopic Grading Scale	McPhee 1987
13	Rutter Score	Rutter 2004
14	Saverymuttu Score	Saverymuttu 1986
15	Sigmoidoscopic Index	Hanauer 2004
16	Sigmoidoscopic Inflammation Grade Scale/Lemann Score	Lemann 1995
17	Truelove and Richards Sigmoidoscopic Appearance	Truelove 1956
18	van der Heide Index	van der Heide 1987

Table 2. Non‐validated endoscopic scoring indices

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Table 3. Reliability

Study ID	Index	Inter‐rater ƙ (between raters)	Inter‐rater ICC (between raters)	Intra‐rater ƙ (within rater)	Intra‐rater ICC (within rater)	Internal Consistency
Daperno 2011	Mayo Clinic Endoscopic Subscore	pre‐training: 0.445 post‐training: 0.713
Daperno 2014	Mayo Clinic Endoscopic Subscore	experts: 0.53 non‐experts: 0.71
de Lange 2004	EAI	experts: 0.97 (95% CI 0.92‐1.00) non‐experts: 0.79 (95% CI 0.71‐0.49)
Kiesslich 2012	Watson Grade	0.87
Osada 2010	Modified 6‐point Activity Index	experts: 0.65 trainees: 0.54		experts: 0.79 trainee: 0.64
	Matts Score	experts: 0.76 trainees: 0.44		experts: 0.78 trainees: 0.41
	The Mayo Endoscopic Subscore	experts: 0.74 trainees: 0.46		experts: 0.75 trainees: 0.48
	Baron Score	experts: 0.61 trainees: 0.47		experts: 0.62 trainees: 0.46
	Blackstone Score	experts: 0.57 trainees: 0.46		experts: 0.73 trainees: 0.51
Samuel 2013	UCCIS		Vascular pattern rectum: 0.75 sigmoid: 0.81 descending colon: 0.74 transverse colon: 0.86 ascending/cecum: 0.85 Granularity rectum: 0.70 sigmoid: 0.78 descending colon: 0.73 transverse colon: 0.88 ascending/cecum: 0.82 Ulceration rectum: 0.80 sigmoid: 0.75 descending colon: 0.72 transverse colon: 0.73 ascending/cecum: 0.73 Bleeding/Friability rectum: 0.68 sigmoid: 0.58 descending colon: 0.56 transverse colon: 0.73 ascending/cecum: 0.77 SAES rectum: 0.79 sigmoid: 0.78 descending colon: 0.71 transverse colon: 0.84 ascending/cecum: 0.85
Travis 2013	UCEIS	0.50		0.72		0.863*
* Cronbach alpha analysis SAES: segmental assessment of endoscopic severity

Table 3. Reliability

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Table 4. Criterion Validity

Study ID	Index	Comparison	Correlation
Nishio 2006	Magnifying Colonscopy Grade	Mucosal IL‐8 activity	ρ = NS (P < 0.001)
Samuel 2013	UCCIS	C‐reactive protein	r = 0.56 (P < 0.001)
		albumin	r = ‐0.55 (P < 0.001)
		hemoglobin	r = ‐0.39 (P < 0.01)
		platelet count	r = 0.19 (P > 0.05)
Schoepfer 2009	Rachmilewitz Endoscopic Score	Fecal calprotectin	r = 0.834 (P < 0.001)
		C‐reactive protein	r = 0.503 (P < 0.001)
		Blood leukocytes	r = 0.461 (P < 0.001)

Table 4. Criterion Validity

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Table 5. Construct Validity

Study ID	Index	Comparison	Correlation
Burger 2011	Baron Score	SCCAI	ƙ = 0.27
Burger 2011	Baron Score	Truelove and Richards Index	ƙ = 0.58
Dhanda 2012	Mayo Clinic Endoscopic Subscore	Riley Score	Week 4 r = 0.55
Higgins 2005a	St. Mark's Index	UCDAI	r = 0.881 (95% CI 0.814‐0.925); ρ = 0.867
		SCCAI	r = 0.908 (95% CI 0.855‐0.924); ρ = 0.866
		Seo Index	r = 0.803 (95% CI 0.699‐0.873); ρ = 0.705
Hirai 2010	Baron Score	Rachmilewitz Score	Week 0 r = 0.39 (95% CI 0.18‐0.57, P = 0.0004) Week 4 r = 0.56 (95% CI 0.36‐0.71, P < 0.0001) Week 8 r = 0.76 (95% CI 0.60‐0.85, P < 0.0001)
		UCDAI	Week 0 r = 0.49 (95% CI 0.29‐0.64, P < 0.0001) Week 4 r = 0.72 (95% CI 0.57‐0.82, P < 0.0001) Week 8 r = 0.85 (95% CI 0.74‐0.91, P < 0.0001)
		Seo Index	Week 0 r = 0.29 (95% CI 0.06‐0.49, P = 0.01) Week 2 r = 0.29 (95% CI 0.04‐0.51, P = 0.02) Week 4 r = 0.53 (95% CI 0.29‐0.70, P < 0.0001)
		Lichtiger Index	Week 0 r = 0.47 (95% CI 0.26‐0.62, P < 0.0001) Week 4 r = 0.56 (95% CI 0.35‐0.71, P < 0.0001) Week 8 r = 0.78 (95% CI 0.64‐0.78, P < 0.0001)
	Rachmilewitz Endoscopic Score	Rachmilewitz Score	Week 0 r = 0.34 (95% CI 0.11‐0.52, P = 0.0003) Week 2 r = 0.66 (95% CI 0.48‐0.78, P < 0.0001) Week 4 r = 0.89 (95% CI 0.73‐0.71, P < 0.0001)
		UCDAI	Week 0 r = 0.44 (95% CI 0.23‐0.60, P < 0.0001) Week 4 r = 0.79 (95% CI 0.67‐0.87, P < 0.0001) Week 8 r = 0.89 (95% CI 0.82‐0.94, P < 0.0001)
		Lichtiger Index	Week 0 r = 0.35 (95% CI 0.13‐0.54, P =0.002) Week 4 r = 0.28 (95% CI 0.02‐0.49, P = 0.003) Week 8 r = 0.65 (95% CI 0.44 to 0.78, P < 0.0001)
		Seo Index	Week 0 r = 0.33 (95% CI 0.10‐0.51, P = 0.005) Week 4 r = 0.67 (95% CI 0.50‐0.79, P < 0.0001) Week 8 r = 0.80 (95% CI 0.67‐0.88, P < 0.0001)
Jun 2008	CGSUC	Truelove and Witts Score	ρ = 0.750 (P < 0.001)
		Baron Score	ρ = 0.740 (P < 0.001)
		Modified Baron Score	ρ = 0.742 (P < 0.001)
		Jeroen Score	ρ = 0.799 (P < 0.001)
		Azzolini Score	ρ = 0.685 (P < 0.001)
	Truelove and Witts Score	CGSUC	ρ = 0.750 (P < 0.001)
		Baron Score	ρ = 0.814 (P < 0.001)
		Modified Baron Score	ρ = 0.760 (P < 0.001)
		Jeroen Score	ρ = 0.782 (P < 0.001)
		Azzolini Score	ρ = 0.756 (P < 0.001)
	Baron Score	CGSUC	ρ = 0.740 (P < 0.001)
		Truelove and Witts Score	ρ = 0.814 (P < 0.001)
		Modified Baron Score	ρ = 0.750 (P < 0.001)
		Jeroen Score	ρ = 0.828 (P < 0.001)
		Azzolini Score	ρ = 0.732 (P < 0.001)
	Modified Baron Score	CGSUC	ρ = 0.742 (P < 0.001)
		Baron Score	ρ = 0.760 (P < 0.001)
		Truelove and Witts Score	ρ = 0.750 (P < 0.001)
		Jeroen Score	ρ = 0.761 (P < 0.001)
		Azzolini Score	ρ = 0.693 (P < 0.001)
	Jeroen Score	CGSUC	ρ = 0.799 (P < 0.001)
		Baron Score	ρ = 0.782 (P < 0.001)
		Truelove and Witts Score	ρ = 0.828 (P < 0.001)
		Modified Baron Score	ρ = 0.761 (P < 0.001)
		Azzolini Score	ρ = 0.788 (P < 0.001)
	Azzolini Score	CGSUC	ρ = 0.685 (P < 0.001)
		Truelove and Witts Score	ρ = 0.756 (P < 0.001)
		Baron Score	ρ = 0.732 (P < 0.001)
		Modified Baron Score	ρ = 0.693 (P < 0.001)
		Jeroen Score	ρ = 0.788 (P < 0.001)
Naganuma 2010	EAI	Lichtiger Index	r = 0.77 (P < 0.001)
		Matts Score	r = 0.91 (P < 0.001)
		Rachmilewitz Endoscopic Score	r = 0.87, (P < 0.001)
Nishio 2006	Magnifying Colonoscopy Grade	Riley Score	ρ = NS (P < 0.001)
Rubin 2012	Mayo Clinic Endoscopic Subscore	SCCAI	r = 0.525 (P < 0.0001)
Rubin 2012	Mayo Clinic Endoscopic Subscore	Rubin Histologic Score	r = 0.597 (P < 0.0001)
Samuel 2013	UCCIS	SCCAI	r = 0.62 (P < 0.0001)
		Rachmilewitz Score	r = 0.5 (P < 0.001)
		Patient‐Defined Remission Score	r = 0.43 (P < 0.01)
Schoepfer 2009	Rachmilewitz Score (endoscopic)	Rachmilwitz Score (clinical)	r = 0.672 (P < 0.01)
Thomas 2009	Baron Score	Truelove and Richards Score	ƙ = 0.58
	Baron Score	SCCAI	ƙ = 0.27
Travis 2013	UCEIS	Visual Analogue Scale	median 0.93 across investigators (minimum 0.78, maximum 0.99) statistically significant P > 0.05
Walsh 2009	Baron Score	Modified Baron Score	ƙ = 0.89
Walsh 2009	Baron Score	Mayo Endoscopic Subscore	ƙ = 0.83
ρ = Spearman's rank correlation coefficient Abbreviations: CGSUC, Chinese Grading Score for Ulcerative Colitis; EAI, Endoscopic Activity Index; IL, Interleukin; NS, Not Stated; SCCAI, Simple Clinical Colitis Activity Index

Table 5. Construct Validity

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Table 6. Responsiveness

Study ID	Index	Treatment	Effect size (95% CI)	Guyatt's responsiveness statistic (95% CI)	Area under the ROC curve (95% CI)	Mean change (P value)
Levesque 2014	Mayo Clinic Endoscopic Subscore	Asacol	0.49 (0.28, 0.71)	0.32 (0.11, 0.53)	0.66 (0.55, 0.78)
	Modified Baron Score		0.49 (0.28, 0.71)	0.33 (0.13, 0.54)	0.65 (0.54, 0.77)
	UCEIS		0.58 (0.36, 0.81)	0.47 (0.25, 0.69)	0.68 (0.58, 0.79)
Ikeya 2016	Mayo Clinic Endoscopic Subscore	Tacrolimus				2.9 (+/‐ 0.9) to 2.0 (+/‐ 1.0) (P < 0.001)
Ikeya 2016	UCEIS	Tacrolimus				6.2 (+/‐ 0.9) to 3.4 (+/‐ 2.1) (P < 0.001)

Table 6. Responsiveness

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Table 7. The Methodological Quality of Endoscopic Index Measurement Properties as Described in the Original Development Articles (COSMIN Checklist)

	A	B	C	D	E	F	G	H	I	J
Study ID	IC	RB	ME	COV	FA	HT	CCV	CRV	RP	IT	GN
Burger 2011	‐	‐	‐	‐	‐	good	‐	‐	‐	‐	‐
Daperno 2011	‐	good	‐	‐	‐	‐	‐	‐	‐	‐	‐
Daperno 2014	‐	‐	‐	‐	‐	‐	‐	‐	‐	‐	‐
de Lange 2004	‐	good	‐	‐	‐	‐	‐	‐	‐	‐	‐
Dhanda 2012	‐	‐	‐	‐	‐	excellent	‐	‐	‐	‐	‐
Higgins 2005a	‐	‐	‐	‐	‐	good	‐	‐	‐	‐	‐
Hirai 2010	‐	‐	‐	‐	‐	good	‐	‐	‐	‐	‐
Ikeya 2016	‐	‐	‐	‐	‐	‐	‐	‐	fair	‐	‐
Jun 2008	‐	‐	‐	‐	‐	good	‐	‐	‐	‐	‐
Kiesslich 2012	‐	good	‐	‐	‐	‐	‐	‐	‐	‐	‐
Levesque 2014	‐	‐	‐	‐	‐	‐	‐	‐	excellent	‐	‐
Naganuma 2010	‐	‐	‐	‐	‐	excellent	‐	‐	‐	‐	‐
Nishio 2006	‐	‐	‐	‐	‐	good	‐	good	‐	‐	‐
Osada 2010	‐	excellent	‐	‐	‐	‐	‐	‐	‐	‐	‐
Rubin 2012	‐	good	‐	‐	‐	good	‐	‐	‐	‐	‐
Samuel 2013	‐	excellent	‐	‐	‐	excellent	‐	excellent	‐	‐	‐
Schoepfer 2009	‐	‐	‐	‐	‐	excellent	‐	excellent	‐	‐	‐
Thomas 2009	‐	‐	‐	‐	‐	good	‐	‐	‐	‐	‐
Travis 2013	‐	good	‐	‐	‐	good	‐	‐	‐	‐	‐
Walsh 2009	‐	‐	‐	‐	‐	excellent	‐	‐	‐	‐	‐
IC ‐ internal consistency; RB ‐ reliability; ME ‐ measurement error; COV ‐ content validity; FA ‐ factor analysis; HT ‐ hypothesis testing; CCV ‐ cross cultural validity; CRV ‐ criterion validity; RP ‐ responsiveness; IT ‐ interpretability; GN ‐ generalizability

Table 7. The Methodological Quality of Endoscopic Index Measurement Properties as Described in the Original Development Articles (COSMIN Checklist)

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Table 8. Summary of operating properties of histologic scoring indices for Crohn's disease

Scoring index	Validity			Reliability				Responsiveness	Feasibility
	Content validity	Criterion validity	Construct validity	Intra‐rater	Inter‐rater	Test‐retest	Internal consistency
Azzolini Classification	?	?	+	?	?	?	?	?	?
Baron Score	?	?	+	+	+	?	?	?	?
Blackstone Endoscopic Interpretation	?	?	?	+	+	?	?	?	?
CGSUC	?	?	+	?	?	?	?	?	?
Endoscopic Activity Index (EAI)	?	?	+	?	+	?	?	?	?
Jeroen Score	?	?	+	?	?	?	?	?	?
Magnifying Colonscopy Grade	?	+	+	?	?	?	?	?	?
Matts Score	?	?	+	+	+	?	?	?	?
Mayo Clinic Endoscopic Subscore	?	?	+	+	+	?	?	+	?
Modified Mayo Clinic Endoscopic Subscore	?	?	?	?	?	?	?	+	?
Modified Baron Score	?	?	+	?	+	?	?	+	?
Osada Score (Modified 6‐Point Activity Index)	?	?	?	+	+	?	?	?	?
Rachmilewitz Endocopic Score	?	+	+	?	?	?	?	?	?
St. Mark's Index (Powell‐Tuck Index)	?	?	+	?	?	?	?	?	?
Ulcerative Colitis Colonoscopic Index of Severity (UCCIS)	?	?	?	?	?	?	?	?	?
Ulcerative Coltiis Disease Activity Index (endoscopic) (Sutherland Index)	?	?	?	?	?	?	?	?	?
Ulcerative Colitis Endoscopic Index of Severity (UCEIS)	?	?	?	?	?	?	?	?	?
Truelove and Witts Sigmoidoscopic Score	?	?	?	?	?	?	?	?	?
Watson Grade	?	?	?	?	+	?	?	?	?
+ positive rating ? no information or indeterminate rating ‐ Negative rating

Table 8. Summary of operating properties of histologic scoring indices for Crohn's disease

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