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14 Title: Endoanal ultrasound for perianal Crohn’s disease: is there correlation
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16 Paper code: Chirurgia-4810
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18 Submission Date: 2018-02-01 03:38:02
19 Article Type: Original Article
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23 Files:
24 1): Reply letter to comments on the manuscript
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27 Description: Reply to editors.
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30 2): Manuscript

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32 Version: 3
33 Description: Manuscript revised with correction to table 3.
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37 3): Figures 1
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39 Description: FIGURE 1
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9 Dear Editor,
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11 I corrected the table 3 including all the missing data, that was a formatting error occurred when
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14 I hope that the final proof is satisfying.
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17 Regards
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20 Dr. Umberto Morelli
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9 Title: Endoanal ultrasound for perianal Crohn’s disease: is there correlation with fecal
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12 incontinence?
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21 Authors and academic degrees:
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23 Umberto Morelli, MD, MSc1, Luís Alberto Magna, MD, PhD2, Claudio Saddy Rodrigues
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25 Coy, MD, PhD1, Raquel Franco Leal, MD, PhD1, Maria de Lourdes Setsuko Ayrizono, MD,
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28 PhD1*.
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32 Coloproctology Unit, Surgery Department, School of Medical Sciences,
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34 University of Campinas (UNICAMP), Sao Paulo, Brazil.
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39 Genetic Department, School of Medical Sciences,
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41 University of Campinas (UNICAMP), Sao Paulo, Brazil.
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51 *Corresponding author
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53 Maria de Lourdes Setsuko Ayrizono
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57 Zip code 13025-010, Campinas, Sao Paulo, Brazil. Tel: +55-19-32517966
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60 luayrizono@terra.com.br
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67 Keywords: Crohn’s disease, endoanal ultrasound, inflammatory bowel disease, anal fistula ,
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69 fecal incontinence.
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9 Abstract
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14 BACKGROUND The incidence of perianal Crohn disease (PCD) is variable between 20% and
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16 25 % of patients with Crohn disease (CD). The assessment of PCD consists in clinical examination
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18 followed eventually by examination under anesthesia. Our aim was to verify if a clinical evaluation
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21 using the Jorge-Wexner score to assess fecal incontinence in patients with PCD is correlated to real
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23 anatomical defects, assessed with the use of endoanal ultrasound (EAUS) and Starck score for
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25 sphincteric lesions. METHODS: Cohort study that included patients more than 18 years old, both
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28 genders, an established diagnosis of PCD, was performed. All patients were submitted to a standard
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30 outpatient clinical evaluation and to a questionnaire to calculate the Jorge-Wexner score for fecal

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32 incontinence and to a 2D and 3D EAUS. The Starck score was calculated for each exam.
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34 RESULTS: Twenty-four patients were included, 16 females and 8 males, mean age 40.54 years
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37 old. Seven (29.16%) have small bowel CD, 7 (29.16%) large bowel CD, 2 (8.33%) both small and
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39 large bowel CD, and in 8 patients (33.33%) PCD was the only clinical manifestation of CD. Both
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41 scores had a normal distribution, with a mean Wexner score of 3.83 (SD 4.52) and a mean Starck
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44 score of 9.75 (SD 2.54). There is no statistical correlation between the two scores with a confidence
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46 interval of 95%. CONCLUSION: The Jorge-Wexner score use in clinical practice in PCD patients
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48 is not advised for therapeutic management and planning, whereas EAUS was a useful tool to
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9 Introduction
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14 Perianal Crohn’s disease (CD) can be associated with the classical ileocolic localization , but
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16 could be the only manifestation in some individuals (1).
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18 The incidence of perianal Crohn’s disease (PCD) is variable between 20% and 25% (2) and
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21 is more frequent when the rectum is involved (35-45% of CD patients) (3), with some cohort
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23 studies reporting incidence as high as 78% (4). PCD is associated with high morbidity and has a
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25 great impact on the quality of life of these patients, especially for the pain and the risk of sphincteric
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28 lesions that can lead to fecal incontinence. Treating PCD, achieving the closure of fistulas and the
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30 complete healing of the abscesses needs both medical and surgical therapy, including

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32 immunosuppressive and immunobiological therapies (5). Surgical therapy includes incision and
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34 drainage of abscesses, fistulotomy of superficial fistulas, and in some cases, placement of non-
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37 cutting setons in patients with active rectal disease or high fistulas. The standard assessment of PCD
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39 is clinical examination followed by EUA (Examination Under Anesthesia) (6) but American
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41 Gastroenterological Association (AGA) introduced endoanal ultrasound (EAUS) and magnetic
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44 resonance imaging (MRI) as useful diagnostic tools to assess fistulas and plan the treatment(7).
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46 They can verify the effectiveness of treatments during follow-up, but this standard of care is
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48 practiced only in highly specialized centers. MRI is able to precisely assess and classify fistula-in-
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51 ano in 76% to 100% (8, 9) of the cases, and with its use, the surgeon can obtain useful information
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53 that can change the surgical strategy in 15% to 21% of the cases (10). European Crohn’s and Colitis
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57 diagnostic precision of 56% - 100% and its findings can modify the surgical strategy in 10% to 15%
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60 of the cases (12) with great benefits for the patients (13). The combinations of MRI and EAUS,
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62 joint with EUA, gives us the 100% of diagnostic precision in PCD (14). MRI is expensive, needs
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67 available. Otherwise, EAUS is less expensive, can be performed by various categories of adequately
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69 trained physicians (gastroenterologists, colorectal surgeons), and can be easily available (15). There
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81 are few studies about EAUS in PCD patients and comparing clinical and ultrasound scores in this
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84 context(16, 17). Many guidelines do not include performing MRI or EAUS before surgically
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86 treating PCD, with the risk of adding injury to a already injured sphincteric complex (18), causing
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88 or worsen fecal incontinence. In this paper, we performed 3D and 2D EAUS to evaluate the
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90 sphincteric anatomy of PCD patients using a quantitative score and compared it to a widely used
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93 score for fecal incontinence, thus comparing function (continence) to anatomy (sphincters
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95 integrity).The aim was to observe if there is any correlation between these two quantitative scores,

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9 already used in literature together as clinical evaluation, comparing sphincters integrity and
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11 functionality (19, 20).
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16 Materials and methods
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20 This is an observational prospective study compliant with the Declaration of Helsinki and
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22 the STROBE statement for Observational Studies (21). The University of Campinas Ethical
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Committee approved the study (no 0792.0.146.000-09). This project was carried out at the State
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27 University of Campinas, Coloproctology Unit - in the Outpatients Clinic for Inflammatory Bowel
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29 Disease - Gastrocentro. The inclusion criteria of the study were: patients with more than 18 years
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31 old, an already established diagnosis of PCD, both genders. Exclusion criteria were: patients
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34 without a clearly established diagnosis of PCD and anyone who manifest the will of not to
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38 (history taking, treatment and score recording (Crohn’s Disease Activity Index - CDAI and Perianal

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41 Disease Activity Index - PDAI and physical examination), with an assessment of the sphincteric
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43 functionality with external examination of the perineum, palpation and a digital rectal examination
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45 (DRE). During DRE the patient was asked to squeeze or to push, in order to clinically assess the
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47 sphincteric tone and functionality. This was performed by only one experienced colorectal surgeon
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In all patients the Jorge-Wexner score for fecal incontinence was calculated (22). (Table S1)
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59 submitted to a 2D and 3D EAUS, performed by one of the four authors (UM, MLSA, RFL, CSRC).
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61 The EAUS was realized with a Bruël and Kjær ultrasound scanner (Denmark - Model: Ultraview
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800 System®) equipped with a 6-16 MHz rotating transducer with a 360° cross-sectional image of
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66 the anal sphincters; 3D scans were done and archived for being reviewed and assessed after the
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68 patients’ consult. The anal probe was inserted with the patient in Sim’s position, positioned at the
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70 level of the puborectalis muscle, and oriented so that the rectovaginal septum (women) or prostate
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83 (men) was uppermost on the screen (23). The gain settings and scanning parameters were the same
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85 for all subjects, and comparable to those used in literature (gain 51%, contrast 3, gamma correction
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87 3) (24). All scans were reviewed with BK 3DView© version 7.0.0.412 from B-K Medical© , a
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90 score for quantitative classification of the anal sphincter defects was calculated following the
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92 classification developed by Starck et al. (25) for research purposes. (Table S2)
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9 low scan at the level of the subcutaneous external anal sphincter. Each set of images was exported
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11 and saved in Windows bitmap format (*.bmp). The images were analyzed using a software (Image
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14 Measurement Professional v. 3.0, Bersoft, Toronto, Canada) capable of calculating first-and second-
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16 order statistics for each image, such as the number of pixels and the mean gray-scale tone, for
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18 evaluating the sphincteric lesions (17, 24). The potential bias of previous sphincteric lesion in
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21 primiparous or multiparous female patients was considered not to have any influence on the
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23 objective of the study given that the same results were observed in the male patients , as described
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25 in the results section. We performed a statistical analysis (one-sample Kolmogorov-Smirnov test
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28 and the two tailed Spearman test and Pearson test (SPSS for Windows®, Version 15 (2006)) in order
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32 score alone (Wexner score) as a representation of anatomical integrity in this particular kind of
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34 patients is correct or not. The 95% confidence interval (CI) was computed using the variance
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41 Results
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44 30 patients were included into the study group, but 6 were excluded, 3 for not being able to
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48 after the EAUS for not having a definite diagnosis of PCD after further investigation. The total of
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53 males, mean age was 40.54 years old (median 41.5 years old range 24-64, standard deviation (SD)
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55 9.75). All 24 (100%) patients have established diagnosis of PCD; 7 (29.16%) had also a diagnosis
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60 involving the small bowel and the colon-rectum, and 8 (33.33%) had a unique diagnosis of PCD.
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62 All patients were submitted to a questionnaire in order to calculate the Jorge-Wexner score (22). All
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67 the Starck score was calculated for each patient. (Table S3)
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69 The two scores have a normal distribution, with a mean Wexner score of 3.8333 (SD
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81 4.52689) and a mean Starck score of 9.7500 (SD 2.54097). (Table S4)
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88 No correlation between the Jorge-Wexner score and this particular data subset was found. A
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9 Discussion
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11 Currently, the majority of the patients with perianal CD receive in their diagnostic and
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16 recording (18) (Crohn’s Disease Activity Index - CDAI and Perianal Disease Activity Index - PDAI
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18 in case of PCD), in some cases followed by a programmed EUA in case of doubts or need for
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21 eventual surgical management of undrained sepsis and fistulas.
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23 The clinical evaluation of the sphincteric function is routinely performed in all the patients
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25 that present with an anorectal disease (27). The standard classification divides fecal incontinence in
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28 two groups: minor (gases and liquid stools) and major (solid stools). The first evaluation is realized
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32 of muscular structures, presence of lesions, and with appropriate commands of contraction and
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37 Using scores is useful to refine this primary assessment that is limited being subjective and
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44 are available in literature (28), and most centers uses the Jorge-Wexner score (also known as the
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48 twenty (serious fecal incontinence with continuous use of diapers). All patients were submitted to
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60 used to assess the grade and severity of fecal incontinence, it is validated and used in many studies
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62 published in current literature and guidelines (29) and the Starck score, developed for obstetric
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64 lesions and used to assess the severity of sphincteric lesions with EAUS. In our study, we saw that
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67 the 33,33% of the patients observed have PCD as the unique presentation of CD. Its natural history
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69 affects the sphincters in various ways, altering their anatomical integrity, functions and role in fecal
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81 continence. The use of Starck score was dictated by its simple application in sphincteric lesions and
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84 the lack of similar scores in literature to give a quantitative scoring of sphincteric lesions in EAUS.
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86 It can be argued that it is used in obstetrical lesions only, and PCD has a different mechanism of
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9 comparing it to another quantitative score derived from 2D-3D EAUS to assess the eventual
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14 variables (both quantitative), lead us to rethink the way we still currently assess the patients with
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16 PCD in most of medical practices. Also, patients generally are assessed by different physicians
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18 (multidisciplinary teams, change of medical insurance company, etc), and this almost oblige the
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21 physicians to use scores, reducing the bias that is normally present in everyone clinical examination,
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23 as stated by Dobben et al. (30). These authors found a good correlation between anal inspection and
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25 DRE compared to anorectal physiology tests and EAUS in evaluating fecal incontinence, however
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28 was inaccurate for determining external anal sphincter defects more than 90 degrees, that are not so
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32 of the perineum and the sphincters in case of PCD is still the EUAS (9) , but this procedure is time
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37 EAUS is an excellent method to assess the pelvic floor as a whole and the sphincteric
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39 complex (32), and is sufficient to help both the clinicians and the surgeons to achieve better results.
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41 Sakse et al. (33) did not found any correlation between the Starck and the Jorge-Wexner score in the
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44 population they examined, although this study considers sphincteric lesions caused in vaginal
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46 delivery and not PCD. Previous studies have demonstrated a degree of correlation between defects
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48 detected on EAUS and fecal incontinence following obstetric sphincter tears. Norderval et al. (34)
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53 at a median of 21 (range, 9-35) months after delivery in a data set that is considerable (n=61),
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57 following primary repair after delivery with the Jorge-Wexner score after 4 years in 41 patients.
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60 Those results, although they were found in a different category of patients, strongly suggest that
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62 sphincteric lesions lead to incontinence along the time (35) altering first the mechanical part of the
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67 We were unable to find any correlation between the Jorge-Wexner score and the
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69 subcategories of the Starck score so the main hypothesis of our study (no correlation between Jorge-
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81 Wexner score and Starck score) was demonstrated. This is maybe related to the small number of
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84 patients evaluated, but our study is the first that evaluate the efficacy of a score used to asses fecal
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86 incontinence comparing it to a score that express quantitatively the real anatomical conditions of the
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88 sphincteric complex in this subpopulation (PCD). Another objection could rise about our sample,
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93 partum, mostly to the external sphincter; but we did not found any correlation, also clinically, in the
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9 male group of the sample. However, Lunniss et al. showed that fecal incontinence is linked more to
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14 Our study showed that we cannot rely on Jorge-Wexner score as a functional score for
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16 evaluating incontinence in this particular subpopulation, PCD patients. 2D and 3D EAUS is a
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18 reliable and maybe essential tool in the evaluation of this particular disease (PCD) (36-41), to
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21 prevent surgical maneuvers that could worsen the already critical anatomical condition in those
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23 patients, underestimated through the routine follow-up examination. We chose EAUS instead of
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25 MRI as imaging system because of its reliability, cost effectiveness and efficacy in detecting
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28 sphincteric lesions in multiple categories of patients (1, 42, 43), and it is currently used and
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30 recommended for the assessment of PCD (44, 45). In routine assessment of PCD patients, not all

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32 the practices have the possibility to obtain an MRI (especially the gold-standard performed with an
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34 endoanal coil), and most of small to medium hospitals do not have a MRI machine or a qualified
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37 radiologist especially in developing countries despite all efforts to provide a high-standards level of
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39 management of this disease (39, 46). Ultrasound imaging could be easily performed by
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41 gastroenterologists and colorectal surgeons (non specialized in radiology) with a relatively fast
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44 learning curve , can be realized at the point of care in multiple settings (36), is cost-effective and
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48 Conclusion
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60 with limited technological resources and developing countries.
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67 References
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81 1. Sandborn WJ, Fazio VW, Feagan BG, Hanauer SB. AGA technical review on perianal
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83 Crohn's disease. Gastroenterology. 2003;125(5):1508-30.
84 2. Tang LY, Rawsthorne P, Bernstein CN. Are perineal and luminal fistulas associated in
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86 Crohn's disease? A population-based study. Clin Gastroenterol Hepatol. 2006;4(9):1130-4.
87 3. Schwartz DA, Loftus EV, Jr., Tremaine WJ, Panaccione R, Harmsen WS, Zinsmeister AR,
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89 et al. The natural history of fistulizing Crohn's disease in Olmsted County, Minnesota.
90 Gastroenterology. 2002;122(4):875-80.
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92 4. Harper PH, Fazio VW, Lavery IC, Jagelman DG, Weakley FL, Farmer RG, et al. The long-
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94 term outcome in Crohn's disease. Dis Colon Rectum. 1987;30(3):174-9.
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9 5. Van Assche G, Dignass A, Reinisch W, van der Woude CJ, Sturm A, De Vos M, et al. The
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11 second European evidence-based Consensus on the diagnosis and management of Crohn's disease:
12 Special situations. J Crohns Colitis. 2010;4(1):63-101.
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14 6. Taxonera C, Schwartz DA, Garcia-Olmo D. Emerging treatments for complex perianal
15 fistula in Crohn's disease. World J Gastroenterol. 2009;15(34):4263-72.
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17 7. American Gastroenterological Association medical position statement: perianal Crohn's
18 disease. Gastroenterology. 2003;125(5):1503-7.
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20 8. Hussain SM, Outwater EK, Joekes EC, Ulrich F, Delemarre HB, Bemelman WA, et al.
21 Clinical and MR imaging features of cryptoglandular and Crohn's fistulas and abscesses. Abdom
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23 Imaging. 2000;25(1):67-74.
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25 9. Schwartz DA, Wiersema MJ, Dudiak KM, Fletcher JG, Clain JE, Tremaine WJ, et al. A
26 comparison of endoscopic ultrasound, magnetic resonance imaging, and exam under anesthesia for
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28 evaluation of Crohn's perianal fistulas. Gastroenterology. 2001;121(5):1064-72.
29 10. Beets-Tan RG, Beets GL, van der Hoop AG, Kessels AG, Vliegen RF, Baeten CG, et al.
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31 Preoperative MR imaging of anal fistulas: Does it really help the surgeon? Radiology.
32 2001;218(1):75-84.
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34 11. Caprilli R, Gassull MA, Escher JC, Moser G, Munkholm P, Forbes A, et al. European
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37 Gut. 2006;55 Suppl 1:i36-58.
38 12. Bor R, Farkas K, Bálint A, Szűcs M, Ábrahám S, Milassin Á, et al. Prospective Comparison

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48 14. Schwartz DA, Pemberton JH, Sandborn WJ. Diagnosis and treatment of perianal fistulas in
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54 16. Zawadzki A, Starck M, Bohe M, Thorlacius H. A unique 3D endoanal ultrasound feature of
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55 perianal Crohn's fistula: the 'Crohn ultrasound fistula sign'. Colorectal Dis. 2012;14(9):e608-11.
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57 17. Losco A, Vigano C, Conte D, Cesana BM, Basilisco G. Assessing the activity of perianal
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66 19. Vitton V, Damon H, Roman S, Nancey S, Flourie B, Mion F. Transcutaneous posterior tibial
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69 option? Inflamm Bowel Dis. 2009;15(3):402-5.
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81 20. Vitton V, Gigout J, Grimaud JC, Bouvier M, Desjeux A, Orsoni P. Sacral nerve stimulation
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84 disruption. Dis Colon Rectum. 2008;51(6):924-7.
85 21. Galera Llorca J, Lahoz Grillo R, Roig Loscertales F. [The reporting of observational studies:
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87 analysis using the STROBE statement]. Rev Esp Salud Publica. 2011;85(6):583-91.
88 22. Jorge JM, Wexner SD. Etiology and management of fecal incontinence. Dis Colon Rectum.
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90 1993;36(1):77-97.
91 23. Bartram CI, Frudinger A. Handbook of anal endosonography. Petersfield: Wrightson
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9 24. Caprioli F, Losco A, Vigano C, Conte D, Biondetti P, Forzenigo LV, et al. Computer-
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11 assisted evaluation of perianal fistula activity by means of anal ultrasound in patients with Crohn's
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14 25. Starck M, Bohe M, Valentin L. Results of endosonographic imaging of the anal sphincter 2-
15 7 days after primary repair of third- or fourth-degree obstetric sphincter tears. Ultrasound Obstet
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17 Gynecol. 2003;22(6):609-15.
18 26. Rothman KJ, Greenland S, Lash TL. Modern epidemiology. 3rd ed. ed. Philadelphia, Pa. ;
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20 London: Lippincott Williams & Wilkins; 2008.
21 27. Bharucha AE. Management of fecal incontinence. Gastroenterol Hepatol (N Y).
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23 2008;4(11):807-17.
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25 28. Pescatori M, Anastasio G, Bottini C, Mentasti A. New grading and scoring for anal
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28 29. Baxter NN, Rothenberger DA, Lowry AC. Measuring fecal incontinence. Dis Colon
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35 31. Santoro GA, Wieczorek AP, Dietz HP, Mellgren A, Sultan AH, Shobeiri SA, et al. State of

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37 the art: an integrated approach to pelvic floor ultrasonography. Ultrasound Obstet Gynecol.
38 2011;37(4):381-96.

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40 32. Sakse A, Secher NJ, Ottesen M, Starck M. Defects on endoanal ultrasound and anal
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48 sonographic classification of defects. Ultrasound Obstet Gynecol. 2008;31(1):78-84.
49 34. Starck M, Bohe M, Valentin L. The extent of endosonographic anal sphincter defects after
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54 35. Lunniss PJ, Kamm MA, Phillips RK. Factors affecting continence after surgery for anal
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87 disease. Dig Dis. 2009;27(4):565-70.
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90 of Magnetic Resonance Imaging, Transrectal and Transperineal Sonography, and Surgical Findings
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9 45. Torres Udos S, Rodrigues JO, Junqueira MS, Uezato S, Netinho JG. The Montreal
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11 classification for Crohn's disease: clinical application to a Brazilian single-center cohort of 90
12 consecutive patients. Arq Gastroenterol. 2010;47(3):279-84.
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14 46. Morris OJ, Draganic B, Smith S. Does a learning curve exist in endorectal two-dimensional
15 ultrasound accuracy? Tech Coloproctol. 2011;15(3):301-11.
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18 NOTES
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23 Author’s Contributions: All authors contributed to draft this paper and revise the data. LAM
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25 elaborated the statistics.
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30 Funding

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32 This research did not receive any specific grant from funding agencies in the public, commercial, or
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39 Conflict of interest
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41 The authors declare that they have no competing interests.
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44 Tables
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48 Type of Never* Rarely* Sometime* Usually* Always*
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Gas 0 1 2 3 4
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62 Wears pas 0 1 2 3 4
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65 Altered lyfestyle 0 1 2 3 4
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70 Table 1- Jorge-Wexner Incontinence score (Jorge & Wexner, 1993). *Never= zero; Rarely=
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83 less than once per month; Sometime= more than once per month; Usually = one or more episodes
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85 per week but less than daily; Always = more than one episode per day.
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16 SCORE
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18 Defect characteristic 0 1 2 3
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21 External sphincter
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23 Lenght of defect None Half or less > 50% Whole
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25 Depht of defect None Partial Total -
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28 Size of defect None ≤90° 91-180° >180°
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30 Internal Sphincter

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32 Lenght of defect None Half or less > que 50% Whole
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35 Depht of defect None Partial Total -

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37 Size of defect None ≤90° 91-180° >180°
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42 Table 2- Starck Score (adapted from Starck et col.). No defect= score 0; Maximal defect= 16
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15 ID WEXNER EAS EAS EAS IAS IAS IAS STARCK
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17 SCORE LOD DOD SOD LOD DOD SOD SCORE
18 TOT.
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20 1 0 1 2 2 1 2 2 10
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22 2 6 1 2 2 2 2 1 9
23 3 1 2 2 3 2 2 1 13
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25 4 0 1 2 1 1 2 2 9
26 5 1 2 2 2 2 1 1 11
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28 6 12 1 2 1 2 2 2 10
29 7 2 2 2 2 0 0 0 6
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31 8 3 1 2 2 1 2 1 9
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33 9 0 1 2 1 1 2 2 9
34 10 4 1 1 2 1 2 1 8
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36 11 0 3 2 2 2 2 3 14
37 12 4 1 2 2 1 1 1 8
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39 13 4 1 2 2 2 2 3 12
40 14 0 2 2 3 2 2 2 13
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42 15 8 2 2 3 2 2 3 14
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44 16 0 1 2 2 1 2 1 9
45 17 2 1 1 2 1 2 1 8
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47 18 14 1 2 2 1 2 1 12
48 19 4 1 1 1 1 1 1 6
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53 22 0 2 2 2 1 2 2 11
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61 Table 3: WEXNER score and STARCK score. EAS= External Anal Sphincter; IAS= Internal
62 Anal Sphincter; LOD= Length Of Defect; DOD= Depht Of Defect; SOD= Size Of Defect.
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13 Wexner score Starck score
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19 N 24 24
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Normal Parametersa.b Mean 3.8333 9.7500
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24 Std. Deviation 4.52689 2.54097
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27 Most Extreme Absolute 0.235 0.158
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30 Differences Positive 0.235 0.158

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33 Negative -0.199 - 0.108
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35 Kolmogorov-Smirnov Z 1.153 0.773

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39 Asymp. Sig. (2-tailed) 0.140 0.589
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44 Table 4: Distribution of Wexner score and Starck score. (a) One-Sample Kolmogorov-
45 Smirnov Test distribution is normal. (b) Calculated from data.
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12 Wexner score Starck score
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16 Spearman's rho Wexner score Correlation Coefficient 1.000 - 0.187
17 Sig. (2-tailed) . 0.383
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19 N 24 24
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22 Starck score Correlation Coefficient - 0.187 1.000
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24 Sig. (2-tailed) 0.383 .
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27 N 24 24
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32 Table 5: Pearson coefficient calculated for Wexner score vs Starck score.
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49 Figure 1: Scatter box plot representing the correlation between Wexner score and Starck score.
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