Role of intestinal ultrasound in ulcerative colitis: A systematic review

Table 8 Summary of studies evaluating correlation of colonoscopy and intestinal ultrasound in ulcerative colitis

Ref.	Study type	Number of patients	Treatment	IUS predictors	Colonoscopy score	Follow-up duration	Time points of IUS	Correlation with colonoscopy
Borthne et al[48]	Prospective	UC 4, CD 17 (pediatric)	NA	BWT, length, CDS, lymph nodes	-	Cross-sectional	Baseline	Sensitivity and diagnostic accuracy of IUS as compared to endoscopy: 93.3%
Bremner et al[49]	Prospective	12 UC (25 CD, 1 in determinate colitis, 6 normal	NA	BWT	Subjective assessment	Cross-sectional	Baseline	Colonic BWT > 2.9: Sensitivity for moderate/severe disease: 48%, specificity: 93%, PPV: 83%; ileal BWT > 2.5 mm: Sensitivity for moderate/severe disease: 75%, specificity: 92%, PPV: 88%
Chavannes et al[72]	Cross-sectional, single centre	33 children with suspected IBD (11 UC)	NA	Ileo-colonoscopy	UCEIS	Cross-sectional	Baseline	Colonic BWT > 1.9 mm: AUC: 0.743, sensitivity: 64%, specificity: 76% to detect inflamed bowel; agreement with colonoscopy: Prediction of IBD: 69.7%, kappa = 0.52; distribution of disease: 45.5%, kappa = 0.48
Haber et al[47]	Prospective	21 UC pediatrics (26 CD, controls)	NA	BWT, BWS, wall echo pattern	No, mild, severe	Cross-sectional	Baseline	AUC: 0.743, sensitivity: 64%, specificity: 76% to detect inflamed bowel
Parente et al[50]	Prospective	83 moderate to severe UC	High dose systemic steroids	BWT, CDS	Baron score	15 mo	Baseline, 3, 9, and 15 mo	Agreement with colonoscopy: Prediction of IBD: 69.7%, kappa = 0.52; distribution of disease: 45.5%, kappa = 0.48
Parente et al[51]	Prospective	83 moderate to severe UC	Same as above	BWT, CDS	Baron score	15 mo	Baseline, 3, 9, and 15 mo	Similar result as the study above
Yamada et al[62]	Prospective	26 UC	NA	SWE, SWD	UCEIS	Cross-sectional	-	SWE and UCEIS correlation: r = -0.404, P = 0.041. No significant correlation between SWD & UCEIS
Carter et al[53]	Retrospective	11 UC (167 CD)	NA	BWT, BWS, CDS, wall echogenicity, i-fat	NA	Cross-sectional	Baseline	Sensitivity 90%, specificity: 23% as compared to colonoscopy/MRE (combined CD and UC)
Antonelli et al[52]	Retrospective	51 moderate to severe UC	NA	BWT > 4 mm	Mayo score	Cross-sectional	-	BWT strongly correlated with CRP and endoscopic score
Allocca et al[16]	Prospective	53 UC	NA	BWT > 3 + CDS; BWT > 4.43 + no CDS	Mayo endoscopic score	Cross-sectional	Baseline	Sensitivity: 68%, specificity: 100%, accuracy: 83%, PPV: 100%, NPV: 73%
Kinoshita et al[54]	Prospective, multi centre (n = 5)	156 UC	NA	BWT, BWS, wall echogenicity	Matt’s endoscopic classification	Cross-sectional	Baseline	Significant concordance between maximum grades (kappa = 0.47) and grades among all colonic segments (kappa = 0.55)
Luo et al[14]	Retrospective	50 UC, 50 CD, and 50 controls	NA	CDS	Active vs remission	Cross-sectional	Baseline	Higher Limberg’s score in active disease (odds ratio: 26.325, P < 0.05)
Sathananthan et al[58]	Prospective, single centre	39 UC (35 CD)	5-ASA, immunomodulator, biologics, steriods	BWT, CDS	MES	Cross-sectional	Same day or within 30 d	Same day colonoscopy (sensitivity 100%, specificity 100%, PPV 100%, NPV 100%, kappa = 1); colonoscopy within 30 d (sensitivity 92%, specificity 86%, PPV 92%, NPV 86%, kappa = 0.77 (MES ≥ 1). Extent: Sensitivity 92%, specificity 80%, PPV 88%, NPV 86%, kappa = 0.7
Sagami et al[57]	Single centre, prospective, cross-sectional	53 UC	5-ASA, immunomodulators, budesonide, anti-TNF	BWT, BWS, CDS	MES	Cross-sectional	Baseline	BWT > 4 mm trans-perineal USG (sensitivity: 100%, specificity: 45.8%, AUC: 0.904) to predict MES, better than trans-abdominal ultrasound (sensitivity: 96.3%, specificity: 12.5%, AUC: 0.667). Correlation of MES with rectal BWT (trans-perineal US): BWT and MES: r = 0.7204, P < 0.0001; CDS and MES: r = 0.6619, P < 0.0001
Kamel et al[56]	Prospective	14 UC (26 CD)	NA	BWT, CDS, BWS, i-fat, lymph nodes, stricture, abscess	NA	Cross-sectional	Baseline	100% agreement between colonoscopy and IUS
Allocca et al[17]	Prospective	43 UC	Details not available	BWT, CDS	Mayo endoscopic score	Cross-sectional	Baseline	MUC > 6.2 discriminated active UC (sensitivity 85%, specificity 94%, AUC 0.902); MUC > 8.2 100% specific; FCP no incremental value
Zhang et al[59]	Retrospective	103 UC	NA	BWT, CDS	Mayo endoscopic score	Cross-sectional	Baseline	Prediction of endoscopic activity: BWT: Not significant; CDS: OR = 2.492, P < 0.001
Bots et al[23]	Prospective	60 UC	Conventional therapy, biologic, tofacitinib, topical tacrolimus	BWT, vascularity, haustrations, fat wrapping	Mayo endoscopic score, UCEIS	Cross-sectional	Baseline	UC-IUS score has strong correlation with endoscopic disease activity (ρ = 0.83 for Mayo score, ρ = 0.76 for UCEIS score); BWT > 2.1 for Mayo 0 vs Mayo 1-3: Sensitivity: 82.6%, specificity: 93%, AUC: 0.91. BWT > 3.2 for Mayo 0-1 vs Mayo 2-3: Sensitivity: 89.1%, specificity: 92.3%, AUC: 0.946. BWT > 3.9 mm for Mayo 3 vs others: Sensitivity: 80.6%, specificity: 84.1, AUC: 0.909
Allocca et al[18]	Prospective	98 UC	NA	BWT, CDS	MES	Cross-sectional	Baseline	Significant correlation between MES and MUC (r = 0.653)
Bots et al[23]	Retrospective, single center	65 UC (280 CD)	Biologics, conventional therapy	BWT, CDS, BWS, i-fat, haustrations, lymph nodes, motility	MES	Cross-sectional	Baseline	Agreement with endoscopy: 86.3%. Correlation: 0.70. Kappa agreement: 0.61 (both UC and CD)
Miyoshi et al[61]	Retrospective	24 UC (31 CD, 10 IBS)	NA	BWT, BWS, CDS, modified Limberg’s score, SMI	MES	Cross-sectional	≤ 15 d between IUS and colonoscopy	BWT < 3.75 mm and SMI < 49.7: Sensitivity: 70%, specificity: 97.7%, PPV: 95.5%, NPV: 82.7%, accuracy: 86.5%
de Voogd et al[2]	Prospective	30 UC	Tofacitinib	BWT	MES and UCEIS	8 wk	Baseline and 8 wk	BWT correlated with MES and UCEIS. Cutoff values for BWT: (1) 2.8 mm for endoscopic remission (AUC: 0.87, 95%CI: 0.74-1.00, P = 0.006) (sensitivity 73%, specificity 100%); (2) 3.9 mm for improvement (AUC: 0.92, 95%CI: 0.82-1.00, P < 0.0001) (sensitivity 81%, specificity 100%); and (3) Decrease of 32% for response (AUC: 0.87, 95%CI: 0.74-1.00, P = 0.002) (sensitivity 71%, specificity 90%). Correlation: ΔBWT and ΔMES: 0.50, P = 0.009; ΔBWT and ΔUCEIS: 0.68, P < 0.0001 (sigmoid); ΔBWT and ΔMES: 0.67, P = 0.001; ΔBWT and ΔUCEIS: 0.50, P = 0.02 (descending colon)
van Wassenaer et al[64]	Prospective cross-sectional	35 UC (pediatric)	NA	UC-IUS score, Civitelli index	Mayo endoscopic score	Cross-sectional	Baseline	UC-IUS score better than Civitelli index for both sensitivity (88%-100% vs 65-80%) and specificity (84%-87% vs 89-93%) (MES ≥ 2). Higher AUC in ascending colon (0.82 vs 0.76) and transverse colon (0.88 vs 0.77). No difference in descending colon (both 0.84)
Goodsall et al[4]	Prospective	29 UC	NA	BWT, CDS, BWS, MUC	UCEIS	Cross-sectional	Baseline	MUC had significant correlation with UCEIS (r = 0.32; 95%CI: 0.14-0.49; P < 0.001)
Lim et al[63]	Prospective cross-sectional	29 UC (22CD)	NA	BWT, BWS, i-fat, CDS	UCEIS	Cross-sectional	Baseline	Sensitivity: 50%, specificity: 100%, PPV: 100%, NPV: 84%; 100% sensitivity/specificity in transverse colon; correlation with endoscopic activity index: 0.648 (P < 0.01)
Maeda et al[20]	Retrospective	58 UC	5-ASA, topical therapy, anti-TNF, vedolizumab	BWT, CDS, BWS, enlarged lymph nodes, MUC	MES	3 mo	Baseline, 3, 6, 12 mo	MUC and MES: 0.61 (entire colon). Most severely affected segment: BWT and MES: 0.88; CDS and MES: 0.98; MUC and MES: 0.88. Accuracy of MUC > 6.2 to differentiate MES ≥ 1 and 0 (sensitivity: 24%, specificity: 100%, PPV: 100%, NPV: 0.47, AUC: 0.67)
Rispo et al[22]	Prospective	86 UC	5-ASA, steroids, IMS, biologics	Milan ultrasound criteria	Mayo endoscopic score	Cross-sectional	-	HHIUS MUC > 6.2: Sensitivity: 80%, specificity: 88%, PPV: 83%, NPV: 86%, accuracy: 84%; highest in sigmoid colon; lowest in rectum

TNF: Tumor necrosis factor; BWT: Bowel wall thickness; CDS: Color Doppler signal; IUS: Intestinal ultrasound; IUS: Intestinal ultrasound; SWE: Shear wave elastography; HHIUS: Hand-held intestinal ultrasound; 5-ASA: 5-amino salicylic acid; UC: Ulcerative colitis; PPV: Positive predictive value; NPV: Negative predictive value; IMS: Immunosuppressant; MUC: Milan ultrasound score; MES: Mayo endoscopic score; BWS: Bowel wall stratification; UCEIS: Ulcerative colitis endoscopic activity index; i-fat: Inflammatory fat; CD: Crohn’s disease; CI: Confidence interval; AUC: Area under the curve; SMI: Submucosal index.