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Use of Transabdominal Ultrasound in Ulcerative Colitis

MostafaEzzatMostafa,Moustafa H. Elshamy, Tarik Ibrahim zaher, El sayedSaadAbdElbaser

Tropical medicine department, Zagazig university, Egypt Abstract

Background; ulcerative colitis is one type of IBD and its prevalence is increasing worldwide and in Egypt and the disease itself carries a lot of sufferings and burden on the patients due to its chronic course and periods of relapse,ulcerative colitis needs regular follow up and monitoring, the use of ultrasound is being increased in diagnosis and follow upof IBD patients as a simple, reliable and non-invasive method.

Patients and methods this study included a group of 30 ulcerative colitis patients in different disease activity and tested by the trans abdominal ultrasound to measure the wall thickness of sigmoid colon as marker of disease inflammation and activity.

Results;the study showed that US is a sensitive easy tool to diagnose changes in the bowel wall thickness in ulcerative colitis and these changes correlate with the clinical severity of disease . Conclusion; ultrasound in the hands of the trained personnel is a valuable tool to assess ulcerative colitis by detection of changes in the colonic wall thickness that my correlate with clinical activity of the disease.

Introduction

Inflammatory bowel disease (IBD) is a chronic relapsing idiopathic inflammation of gastrointestinal tract (Xavier and Podolsky, 2007(1). The two main forms of IBD; Crohn’s disease (CD) and Ulcerative colitis have many similarities but there are several clinical and pathological differences . Ulcerative colitis (UC) is a chronic immune-mediated inflammatory condition that causes continuous mucosal inflammation of the colon in variable extent and is characterized by relapsing and remitting course and diagnosis of ulcerative colitis is based basically on endoscopic and histopathological examination (Magro F et al., 2017)(2).

Ultrasonography is non-invasive method mainly used for evaluation of different abdominal organs, but not accurate in assessing the bowel. However, improvement in technology and increasing experience with sonography led to increase the role of ultrasound in bowel diseases.

Also, new techniques such as contrast-enhanced ultrasound increased this role (Dietrich, 2009)(3).

The advantages of ultrasonography include the rapid evaluation of bowel wall thickness and also,

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visualization of the vascularization of the bowel using color Doppler. The third major advantage, in comparison to other cross-sectional imaging modalities, includes the direct visualization of motility(Kucharzik et al., 2017)(4).

Ultrasonography of IBD patients requires convex array probes of 3-5 MHz and higher frequency linear array probes from 5-15 MHz that allow adequate assessment of the five-layer wall pattern of the gastrointestinal tract, In patients with clinical features suggestive of ulcerative colitis, trans- abdominal ultrasonography can be used as an initial method for detection of the affected bowel segment (Strobel et al., 2011)(5).

Ultrasound has multiple possible uses in IBD: initial evaluation of clinically suspected patients of IBD, monitoring therapeutic response, suspicion of relapse, and detection of complication and extra intestinal manifestations(Parente F et al., 2005)(6).

Patients and methods A- Patients:

This cross sectional studywas conducted in Tropical medicine departmentatZagazig University Hospitals in the period between July 2019 and December 2019 and included a total of 30 individuals of ulcerative colitis (UC) patients (14 male and 16 female).The patients with ulcerative colitis were further divided according to disease activity into 4 groups; 7 patients were in severe disease activity, 4 patients were in moderate disease activity, 7 patients were in mild disease activity and 12 patients were in clinical remission.

The diagnosis of ulcerative colitis was based on combination of clinical picture, endoscopic findings and histological examination of biopsy. Clinical severity of active UC (either in newly diagnosed patient or in relapse) was diagnosed based on Truelove and Witt’s’ classification (Truelove and Witt’s., 1955)(7)asit is simple and involves clinical and lab parameters with better assessment of patient condition.

Remission of UC in clinical practice was defined as a stool frequency ≤ 3/day with neither bleeding nor urgency, while relapse was defined as a flare of symptoms in a patient with established UC who was in clinical remission associated with rectal bleeding which was an essential component of relapse according to the 2nd European evidence-based consensus on the diagnosis and management of ulcerative colitis (Dignass et al., 2012)(8).

Table (1): Truelove and Witt’s classification clinical index.

Fulminant Severe

Moderate Mild

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>10

Continuous

>90

>37.8 Transfusion required

> 30

> 30

<3

>6 Frequent

>90

>37.8

<10.5

>30

> 30

<3 4-6

Moderately frequent

≤90

≤37.8 10.5-11.5

≤30

≤30

≤3

< 4 No/

Intermittent

<90

<37.5

>11.5

<30 Normal Normal - Diarrhea

- Blood - Pulse

- Temperature - Hb(g/dl) - ESR(mm/h) - CRP(mg/L) - Albumin (g/dl)

Patient less than 18 years old and patients with Crohn’s disease, Ischemic colitis, Nonspecific colitis, Microscopic colitis and Portal hypertension were excluded from the study.

B-Methods:

All patients were subjected to careful medical history taking and complete physical examination together with lab investigations (CBC, ESR and CRP) to evaluate the patient condition and disease activity.

The patients then examined with Transabdominal ultrasound; all the examinations were performed by a single operator using sonoscapeS11 ultrasound machine with a low frequency (2- 6MHz) curved-array transducer to general examination of all quadrants of abdomen for potential pathologic abnormalities like pathological distension, motility and para-intestinal structures such as abscesses. This was followed by examination using a high resolution linear-array transducer (4–12 MHz) for detailed examination of the bowel wall structure using a consistent technique and protocol: examination of the proximal to distal colon followed by complete examination of the small bowel. All the examinations were performed without any preceding preparation and without contrast material. The assessment focused on measurement of sigmoid colon wall thickness as a sign of disease activity.

Results:

Table (2): Socio-demographic characteristics of the studied group:

Variable The case group(30)

mean ± SD (Range) median

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Age (years):

34.1±12.1 (18-59) 30.5

Variable NO(30) %

Sex Male Female

14 16

46.7%

53.3%

This table shows that the age of the studied group was (34.1±12.1) ranged from (18to 59) years and (53.3%) of them were females.

Table (3): Clinical data of the study group:

Variable The case group(30)

mean ± SD (Range) median Disease duration

(months): 55.5±65.8

(1-240) 24 Variable

NO(30) %

Disease activity Clinical remission Mild disease activity Moderate disease activity Severe disease activity

12 7 4 7

40.0%

23.3%

13.3%

23.3%

This table shows that the disease durationof the studied group was (55.5±65.8) ranged from (1to 240), (40.0%) of them had clinical remission, (23.3%) were Mild or severe disease activity and (13.3%) had moderate disease activity.

Table (4): Laboratory investigations of the studied group:

Variable The studied group(30)

mean ± SD (Range) median ESR

30.5±18.3 (10-85) 24

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CRP 18.6±19.3 (1.1-98.0) 14.5

Hb(g/dl) 11.9±1.5

(7.8-14.8) 12.0 platelets(10*3/dl) 196.3±46.3

(120-300) 190 WBCs(10*3/dl)

6.4±1.5 (4.5-11) 6

This table shows that the laboratory investigations of the studied group.

Table (5): Correlation between disease severity and disease duration with patients' characteristics among the studied group:

Variables

Disease severity Disease duration

r p SIG r p SIG

Age 0.01 >0.05 NS 0.2 >0.05 NS

Disease duration 0.09 >0.05 NS --- --- ---

ESR 0.02 >0.05 NS 0.3 >0.05 NS

CRP 0.7 0.001** HS -0.1 >0.05 NS

Hb -0.2 >0.05 NS -0.1 >0.05 NS

platelets 0.06 >0.05 NS -0.3 >0.05 NS

WBCs 0.3 >0.05 NS -0.02 >0.05 NS

Sigmoid colon wall thickness

0.8 0.001** HS -0.3 >0.05 NS

*Statistically significant difference (P ≤ 0.05), **statistically highly significant difference (P ≤ 0.001), S= significant, HS= highly significant.

Regarding correlation between disease severity and other patients' characteristics, this table

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shows there was statistically significant positive correlation between disease severity with CRP and sigmoid colon wall thickness (increase disease severity was associated with higher CRP and sigmoid colon wall thickness) and no statistically significant correlation between disease severity and any of other variables among the studied group.

Regarding correlation between disease duration and other patients' characteristics, this table shows there was no statistically significant correlation between disease duration and any of other variables among the studied group.

Table (6): Comparison between patients with different disease activity regarding sigmoid colon wall thickness:

Disease activity

Number of patients (30)

Sigmoid colon wall thickness(mm) mean ± SD (Range)

F test

p-value LSD

Clinical remission 12 2.43±0.54 (1.7-3.9)

17.8

0.001**

0.6 (1) 0.01* (2) 0.001**(3) 0.05 (4) 0.001**(5) 0.009* (6)

Mild activity 7 2.7±0.31

(2.3-3.1) Moderate activity 4

3.85±0.48 (3.4-4.4) Severe activity 7 5.5±1.7

(2.1-7.0)

*Statistically significant difference (P ≤ 0.05)

**Statistically highly significant difference (P ≤ 0.001) (1) Clinical remission versus mild activity group (2) Clinical remission versus moderate activity group (3) Clinical remission versus severe activity group (4) Mild activity versus moderate activity group (5) Mild activity versus severe activity group (6) Moderate activity versus severe activity group

In this table, there was statistically significant difference between patients with different disease activity regarding sigmoid colon wall thickness with increasing thickness with higher disease severity.

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Figure (2):sigmoid colon wall thickness measurement demonstrating wall thickening.

Figure (3); ROC curve for the role of sigmoid colon thickness in detection of disease activity

Table (7); accuracy ofsigmoid colon thickness in detection of disease activity:

Variable Cut off AUC p 95% CI

Sigmoid colon thickness

2.8 0.85 <0.001** 0.72-0.99

Variable Sensitivity Specificity PVP PVN Accuracy Sigmoid

colon thickness

83% 77% 80% 75% 80%

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This table shows thatsigmoid colon thicknessis a good predictor marker for detection of ulcerative colitis severity and activity with (80.0%) accuracy.

Discussion

In the present study 30 patients were diagnosed with UC, based on clinical, endoscopic and histopathological examinations, were recruited at different disease activity and examined using intestinal US (IUS) by measuring the sigmoid colon wall thickness as a sign of inflammation and disease activity. Results were documented and correlated with the demographic, clinical and laboratory data of the patients under study. The mean value of sigmoid colon wall thickness among all patients was (3.4±1.5mm), while the mean value in severe disease (5.5±1.7mm), moderately active disease (3.85±0.48mm), mild active disease (2.7±0.31mm) and clinical remission (2.43±0.54mm). Thus current study showed statistically significant difference among different disease activities regarding sigmoid colon wall thickness (p=0.001) with increasing wall thickness with higher disease activity with high sensitivity (83%). Similar results were obtained from Maconi G et al.; 1999(9), Ruess et al.; 2000(10) and Bremner et al.; 2006(11), they stated that the degree of bowel wall thickness, as evaluated by US correlatedwith clinical, biochemical and endoscopic activity of UC, both before and after treatment.

In consistent with our results, another study byCarter D. and Eliakim R. 2017(12),showed that the sensitivity of US for detection of bowel wall thickness was 90%, and demonstrated that bowel US is useful and feasible imaging tool for the detection of the inflammation and complications of IBD, and suggested that bedside bowel US can be a part of non-invasive examination modalities in IBD patients. The TRUST&UC study, was the largest multi-center study investigating the use of bowel US in patients with UC, clearly demonstrated the high sensitivity of bowel US to detect disease activity and therapeutic response and clearly support bowel US as a non-invasive monitoring tool for UC (Maaser C et al.; 2019)(13). On the other hand, other studies (Shirahama M et al., 2003(14),Bavil AS et al.; 2012(15)found no significant difference in bowel wall thickness between active and inactive phases of UC while there was significant difference regarding intramural blood flow. They explained the non-correlation between bowel wall thickness and disease activity may be due to small number of patients. While they included 50 patients, in our study only 30 patients were included, but we have significant correlation between the bowel wall thickness and the disease activity, so, it cannot be explained based on the number of patients, but other factors may be related to operator experience in doing US or patient factors (fasting versus after meal), may underlie such difference in the results.

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Regarding inflammatory markers, our study showed that CRP mean value is (18.6±19.3) with statistically significant difference (p=0.001) among patient groups; severe activity (43.5±28.5), moderate activity (21.7±4.5), mild activity ( 10.3±6.5) and clinical remission (7.85±4.4) is present, this was consistent with (Osada et al 2008)(16)who reported that CRP is often high in moderate and severe UC, and is more sensitive than ESR because of shorter half-life.Rubin DT et al., 2019(17) reported the same results stating that although ESR and CRP are nonspecific markers and may be elevated with other systemic inflammation, they correlate with the endoscopic disease activity. Magro F et al., 2017(2)also,documented that with exception of proctitis, CRP broadly correlate with clinical severity and elevated CRP is generally associated with elevated ESR and hypoalbuminemia in acute severe activity.

The mean value of hemoglobin (Hb) level was (11.9±1.5gm/dl), and anemia was documented in all patients groups; clinical remission (12.1±1.8), mild activity (12.6±1.02), moderate activity (10.5±0.6) and severe activity (11.5±1.2). the discrepancy in Hb levels between moderate and severe active diseases may be explained by that most of patients with severe diseases presented acutely and this was consistent with (Osterman and Lichtenstein., 2016)(18)who reported that anemia is a common finding in ulcerative colitis and different types of anemia are present, although anemia may indicate severe disease activity as used to differentiate between disease activity as in Truelove and Witt’s classification (Truelove and Witt’s., 1955)(7)our study showed nostatistically significant difference among patients with different disease activity regarding Hb level (p=0.1).

Our present study showed no abnormalities in the other CBC parameters perhaps due to small number of patients ; WBC mean value was (6.4±1.5) and mean platelets value was (196.3±46.3) ,although leukocytosis and thrombocytosis usually occur during disease activity as reported by (Osterman and Lichtenstein., 2016)(18)and (Magro F et al., 2017)(2).

Conclusion

Ulcerative colitis is becoming of an important interest due to increase in its prevalencein Egypt(Esmat et al., 2014)(19).

In our study US has proved sensitive and reliable to detect changes in the colonic wall thickness and differentiate between different degrees of activity among UC patients and thus might be used in diagnosis and follow up UC patient.

This study has certain limitations. The patients were not subjected to any treatment, therefore

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response to therapy was not evaluated. In addition other ultrasound modalities including color Doppler, sonoelastograghy and contrast enhanced sonography were no applied

References

1-Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature.

2007; 448(7152):427-34.

2-Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de Acosta M et al.Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1:

definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders. Journal of Crohn's and Colitis. 2017; 11(6):649-70.

3-Dietrich CF. Significance of abdominal ultrasound in inflammatory bowel disease. Digestive Diseases. 2009; 27(4):482-93.

4-Kucharzik T, Kannengiesser K, Petersen F. The use of ultrasound in inflammatory bowel disease.

Annals of Gastroenterology: Quarterly Publication of the Hellenic Society of Gastroenterology.

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5-Strobel D, Goertz RS, Bernatik T. Diagnostics in inflammatory bowel disease: ultrasound. World journal of gastroenterology: WJG. 2011; 17(27):3192.

6-Parente F, Greco S, Molteni M, Anderloni A, Porro GB. Imaging inflammatory bowel disease using bowel ultrasound. European journal of gastroenterology &hepatology. 2005; 17(3):283-91

7-Truelove SC, Witts LJ. Cortisone in ulcerative colitis. British medical journal. 1955; 2(4947):1041 8-Dignass A, Lindsay JO, Sturm A, Windsor A, Colombel JF, Allez M et al. Second European

evidence-based consensus on the diagnosis and management of ulcerative colitis part 2: current management. Journal of Crohn's and Colitis. 2012; 6(10):991-1030.

9-Maconi G.Ultrasonography in the evaluation of extension, activity, and follow-up of ulcerative colitis. Scandinavian journal of gastroenterology. 1999; 34(11):1103-7.

10.Ruess L, Blask AR, Bulas DI, Mohan P, Bader A, Latimer JS et al.Inflammatory bowel disease in children and young adults: correlation of sonographic and clinical parameters during treatment.

American Journal of Roentgenology. 2000; 175(1):79-84

11.Bremner AR, Griffiths M, Argent JD, Fairhurst JJ, Beattie RM. Sonographic evaluation of inflammatory bowel disease: a prospective, blinded, comparative study. Pediatric radiology.

2006; 36(9):947-53.

12.Carter D, Eliakim R.Feasibility of bedside bowel ultrasound performed by a gastroenterologist for detection and follow-up of inflammatory bowel disease. Isr Med Assoc J. 2017; 19(3):139-42.

13-Maaser C, Petersen F, Helwig U, Fischer I, Roessler A, Rath S et al. Intestinal ultrasound for monitoring therapeutic response in patients with ulcerative colitis: results from the TRUST&UC

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study. Gut. 2019 Dec 20.

14.Shirahama M, Ishibashi H, Onohara S, Miyamoto Y. Application of color Doppler ultrasonography to ulcerative colitis. Journal of Medical Ultrasonics. 2003; 30(1):39-44.

15.Bavil AS, Somi MH, Nemati M, Nadergoli BS, Ghabili K, Mirnour R et al.Ultrasonographic evaluation of bowel wall thickness and intramural blood flow in ulcerative colitis. ISRN gastroenterology. 2012; 2012.

16-Osada T, Ohkusa T, Okayasu I, Yoshida T, Hirai S, Beppu K et al.Correlations among total colonoscopic findings, clinical symptoms, and laboratory markers in ulcerative colitis. Journal of gastroenterology and hepatology. 2008; 23:S262-7.

17-.Rubin DT, Ananthakrishnan AN, Siegel CA, Sauer BG, Long MD. ACG clinical guideline:

ulcerative colitis in adults. American Journal of Gastroenterology. 2019; 114(3):384-413.

18-Osterman MT and Lichtenstein GR., (2016): Ulcerative colitis, in: Sleisenger and Fordtran's Gastrointestinal and Liver, 10th edition, by Feldman M, Friedman LS and Brandt LJ, Elsevier Saunders, Philadelphia, P: 2024

19-Esmat S, El Nady M, Elfekki M, Elsherif Y, Naga M.Epidemiological and clinical characteristics of inflammatory bowel diseases in Cairo, Egypt. World journal of gastroenterology: WJG. 2014;

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