J Neurogastroenterol Motil 2023; 29(3): 370-377  https://doi.org/10.5056/jnm21233
Ethnic Differences in Anorectal Manometry Findings in Patients With Fecal Incontinence: Results From a Multiethnic Cohort According to the London Classification
Daniel L Cohen,1* Amir Mari,2 Anton Bermont,1 Dana Zelnik Yovel,1 Vered Richter,1 and Haim Shirin1
1The Gonczarowski Family Institute of Gastroenterology and Liver Diseases, Shamir (Assaf Harofeh) Medical Center, Zerifin, Israel; and 2Department of Gastroenterology, Nazareth Hospital EMMS, Nazareth, Israel
Correspondence to: *Daniel L Cohen, MD
The Gonczarowski Family Institute of Gastroenterology and Liver Diseases, Shamir (Assaf Harofeh) Medical Center, Zerifin 70300, Israel
Tel: +972-8-977-9720, Fax: +972-8-977-9727, E-mail: docdannycohen@yahoo.com
Received: November 30, 2021; Revised: July 19, 2022; Accepted: February 20, 2023; Published online: July 30, 2023
© The Korean Society of Neurogastroenterology and Motility. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background/Aims
Clinical rates of fecal incontinence (FI) are known to vary based on race and ethnicity. It is unclear if anorectal manometry (ARM) findings in patients with FI differ based on ethnicity.
Methods
High-resolution ARM studies performed between 2014-2021 due to FI at 2 hospitals with multiethnic populations were retrospectively reviewed.
Results
Four hundred and seventy-nine subjects were included––87 (18.2%) Arab Israelis, 76 (15.9%) immigrants from the former Soviet Union, and 316 (66.0%) Jewish Israelis. Median age was 67 years old (76.0% women: 90.4% were parous). The Arab Israeli group had higher rates of smoking, diabetes, and obesity. Over 95% of ARM’s were abnormal per the London classification including 23% with “combined anal hypotension and hypocontractility,” 36% with “anal normotension with anal hypocontractility,” 67% with “dyssynergia,” and 65% with either “rectal hyposensation” or “borderline rectal hyposensation.” On univariate analyses, significant differences between the ethnic groups were noted in the rates of “anal hypotension with normal contractility,” “combined anal hypotension with anal hypocontractility,” and “dyssynergia.” In multivariate logistic regression analyses controlling for age, gender, parity, smoking, diabetes, and obesity, the Arab Israeli group remained several times more likely to have “combined anal hypotension and hypocontractibility” compared to the other groups.
Conclusions
Ethnicity impacts ARM findings in patients with FI. The reason for this is unclear and future studies on ethnically diverse populations evaluating the clinical relevance of these findings are warranted.
Keywords: Ethnicity; Fecal incontinence; Manometry
Introduction

Fecal incontinence (FI) is defined as the uncontrolled passage of solid or liquid stool and affects approximately 14.4% of adults.1 Studies have shown that there are racial and ethnic differences in the clinical rates of FI. For example, several studies from the United States have shown that white adults are more likely to have FI than blacks.2,3 Additionally, another study suggested that Hispanics are more likely to have FI, and Asians are less likely, than either whites or blacks.1 It remains unclear why ethnicity affects rates of FI.

FI can result from numerous etiologies.4,5 Patients being evaluated for FI often undergo anorectal manometry (ARM) testing which has been shown to have good diagnostic accuracy.6,7 Measurements for ARM in healthy volunteers are known to vary based on several factors including age, gender, and parity.8

Additionally, studies suggest that there may be ethnic differences in normal-value measurements of healthy subjects between Western and Asian populations.9 For example, in a study of healthy Korean volunteers, women had lower anal resting and squeeze pressures than were reported in a Western population.10

As there are known ethnic differences in clinical FI rates and possible ethnic differences in healthy-value ARM measurements, this suggests that there may be ethnic differences in ARM measurements in patients with FI. As no studies have previously evaluated this, we sought to evaluate this by comparing the ARM parameters between 3 distinct ethnic groups from our diverse population with FI—Arab Israelis (AI), immigrants from the former Soviet Union (SU), and Jewish Israelis (JI).

Materials and Methods

Study Design

A retrospective study was performed using data from 2 tertiary medical centers (Shamir Medical Center and Nazareth Hospital EMMS), each of which serves a diverse, multi-ethnic population. The study was approved by the Ethics Committee (ASF-0159-21).

High-resolution anorectal manometry (HR-ARM) reports were reviewed for all patients referred for evaluation of FI between January 2014 and May 2021. Patients were referred by gastroenterologists, colorectal surgeons, gynecologists, or primary care physicians. Demographic data including age, gender, ethnicity, and parity were recorded. Additionally, data on smoking status, diabetes, and body mass index (BMI) was obtained by telephone interview with the subjects. Obesity was defined as a BMI > 30.

All subjects were included in the study if FI was the main indication on their referral for ARM. This was the definition of FI used in the study as no further data on the quality and severity of their FI was available. No specific prior medical or surgical history was used as exclusion criteria. Subjects under the age of 18 were excluded. If a subject underwent multiple studies during the study period, only the first (index) study was included. Studies in which the ARM data was not interpretable were excluded.

High-resolution Anorectal Manometry Protocol and Interpretation via the London Classification

At each center, HR-ARM was performed using the same system (ManoScanAR, Medtronic, Minneapolis, MN, USA). HR-ARM studies were performed according to the standard protocol,8 and the results were recorded. A study of healthy subjects from the Mayo Clinic using the same HR-ARM system was chosen to use for its normal values.11 The HR-ARM values from our study subjects were compared to these normal values according to gender. Any value outside of the 10-90% normal range was considered abnormal. The normal values used in this study can be found in Supplementary Table. Using these values and the London classification definition, dyssynergia was defined as a failure of coordinated anal relaxation during push (< 20% relaxation of the anal sphincter).8

These findings were then interpreted according to the London classification,8 with the following exceptions. As the balloon expulsion test was not regularly performed at our institutions, it was not included. For measurements of anal tone, a 20-second measurement was used for the mean maximum pressure as was used by Oblizajek et al,11 as opposed to a 60-second measurement recommended by the London classification. Also for anal squeeze pressures, three 20-second measurements were recorded and the greatest value was used,11 as opposed to the 5-second measurements recommended by the London classification.8 Finally, the length of the high pressure zone, which may impact FI, was included in this study even though it is not part of the London classification. Any study in which no abnormalities were identified in any of the 4 areas of the London classification was considered a “normal exam.”

Ethnic Groups of Subjects

The HR-ARM variables were compared between subjects from 3 different ethnic groups. Data on residents’ ethnicity, religion, and country of birth are collected by the government and available via the medical centers’ electronic records.

The first group consisted of AI. The second group consisted of immigrants from the former SU, many of whom speak Russian and immigrated to Israel in the 1990’s after the fall of the Soviet Union. Finally, the third group consisted of all other JI. This was likely the most ethnically diverse group as it included subjects of both Ashkenazi (European) and Sephardic (Middle Eastern) heritage, including both immigrants and native-born Israelis. Studies evaluating these specific ethnic groups are found throughout the medical literature, including studies such as this comparing all 3 of these groups to each other.12-14

Statistical Methods

Categorical variables were summarized as frequency and percentage. Age, parity, and BMI were evaluated for normal distribution using histogram and since they were skewed, they were reported as median and interquartile range (IQR). T squared test and Fisher’s exact test were applied to compare categorical variables between the ethnic groups. Kruskal-Wallis test and Mann–Whitney U test were used to compare age and parity between the groups. Multiple logistic regression was used to study the association between ethnicity and the study outcomes while controlling for age, gender, smoking, diabetes, and obesity. In a further analysis, only women were included in the multivariable regression, and age and parity were considered as confounders.

All statistical tests were two-sided and P < 0.05 was considered as statistically significant. SPSS software was used for all statistical analysis (IBM SPSS Statistics for Windows, version 26; 2019; IBM Corp., Armnok, NY, USA).

Results

Overall Study Population

A total of 1022 HR-ARM studies were performed during the study period, of which 479 (46.9%) were performed for the evaluation of FI and included in the study (Figure). No studies were excluded due to uninterpretable data. Demographic data of the study population can be found in Table 1. The median age was 67 years old (IQR, 59-74) with 76% being women. Of the women, 90.4% were parous with a median number of children of 3 (IQR, 2-4).

Table 1 . Demographic Data of the Study Population

Demographic variablesAll patients
N = 479
Arab Israeli
n = 87 (18.2%)
Former Soviet Union
n = 76 (15.9%)
Jewish Israeli
n = 316 (66.0%)
P-value
Age (yr)67 (59-74)64 (53-70)68 (60.5-74.75)68 (60-75)0.014
Age < 50 (yr)60 (12.5)16 (18.4)7 (9.2)37 (11.7)0.153
Female gender364 (76.0)71 (81.6)59 (77.6)234 (74.1)0.326
Parity amongst females (n = 364)329 (90.4)68 (95.8)43 (72.9)218 (93.2)< 0.001
Number of children per woman3 (2-4)4 (3-6)2 (0-3)3 (2-4)< 0.001
Current smoker (n = 475)76 (16.0)30 (35.7)4 (5.3)42 (13.3)< 0.001
Diabetes (n = 476)174 (36.6)47 (55.3)30 (39.5)97 (30.8)< 0.001
Body mass index (n = 454)26.7 (23.3-30.1)28.0 (24.3-34.0)27.9 (24.8-30.9)26.0 (23.1-29.4)< 0.001
Obesity (n = 454)120 (26.4)36 (43.9)22 (31.9)62 (20.5)< 0.001

Data are presented as median (interquartile range [IQR]) or n (%).

P < 0.05 was considered statistically significant.


Figure 1. Flow chart of the study population. HR-ARM, high-resolution anorectal manometry.

Demographic Differences Between the Ethnic Groups

Of the study population, 87 (18.2%) were AI subjects, 76 (15.9%) were in the SU group, and 316 (66.0%) were JI subjects. These percentages are similar to each groups’ representation within the overall Israeli population.15,16 No significant differences were noted between the groups in terms of gender, but other demographic differences were noted. The median age of the AI group was significantly younger than the other 2 groups, although there was no difference in the percentage of subjects under the age of 50. There were also differences in terms of parity. Less women in the former SU group were parous than the other groups, while the AI group had significantly more children per woman than the other groups. Finally, smoking, diabetes, and obesity were all more prevalent in the AI group.

High-resolution Anorectal Manometry Findings

Over 95% of the study population had abnormalities per the London classification. Details of the HR-ARM findings can be found in Table 2. Disorders of anal tone and contractility were common with nearly one-quarter of subjects having “combined anal hypotension and hypocontractility” and over a third of the population having “anal normotension with anal hypocontractility.” The most common abnormality was “dyssynergia” which was identified in two-thirds of cases. Additionally, nearly two-thirds had either “rectal hyposensation” or “borderline rectal hyposensation,” while “rectal hypersensation” was extremely rare.

Table 2 . Anorectal Manometry Results According to the London Classification

London classification diagnosesAll patients
N = 479
Arab Israeli
n = 87 (18.2%)
Former Soviet Union
n = 76 (15.9%)
Jewish Israeli
n = 316 (66.0%)
P-value
Disorders of rectoanal inhibitory reflex
Rectoanal areflexia54 (11.3)6 (6.9)7 (9.2)41 (13.0)0.247
Disorders of anal tone and contractility
Max resting pressure62.6 ± 28.152.2 ± 24.765.1 ± 29.464.9 ± 28.0
Max squeeze pressure127.2 ± 65.082.2 ± 43.7146.6 ± 65.3134.8 ± 64.6
Combined anal hypotension and hypocontractility113 (23.6)38 (43.7)15 (19.7)60 (19.0)< 0.001
Anal hypotension with normal contractility36 (7.5)0 (0.0)9 (11.8)27 (8.5)0.007
Anal normotension with hypocontractility174 (36.3)37 (42.5)20 (26.3)117 (37.0)0.090
Disorders of rectoanal coordination (n = 357)
Dyssynergia238 (66.7)45 (54.9)37 (66.7)156 (69.6)0.036
Poor propulsion12 (3.4)5 (6.1)2 (3.9)5 (2.2)0.353
Poor propulsion and dyssynergia22 (6.2)4 (4.9)2 (3.9)16 (7.1)0.628
Disorders of rectal sensation
Rectal hyposensation197 (41.1)39 (44.8)36 (47.4)122 (38.6)0.276
Borderline rectal hyposensation118 (24.6)17 (19.5)20 (26.3)81 (25.6)0.485
Either rectal hyposensation or borderline hyposensation315 (65.8)56 (64.4)56 (73.7)203 (64.4)0.288
Rectal hypersensation2 (0.4)0 (0.0)0 (0.0)2 (0.6)-
Overall London classification
Normal exam per London classification22 (4.6)1 (1.1)1 (1.3)20 (6.3)0.048
High pressure zone
High pressure zone length2.54 ± 0.822.41 ± 0.762.49 ± 0.962.59 ± 0.80
Short high pressure zone208 (43.4)45 (51.7)35 (46.1)128 (40.5)0.157

Data are presented as n (%) or mean ± SD.

P < 0.05 was considered statistically significant.



Ethnic Differences in High-resolution Anorectal Manometry Findings

Several differences were noted in HR-ARM findings between the 3 ethnic groups. Significant differences were noted in the rates of “anal hypotension with normal contractility,” “combined anal hypotension with anal hypocontractility,” and “dyssynergia.” Due to this, there was also a significant difference in the percentage of those with a normal examination. However, no significant differences were noted in terms of the other diagnoses.

Logistic Regression Analyses

Multivariable logistic regression analyses were performed adjusting for age and gender (Table 3). These analyses showed that significant differences still persisted between the ethnic groups. Compared to the other 2 groups, the AI group was several times more likely to have “combined anal hypotension and hypocontractibility.” Also, the AI group was less likely to have “dyssynergia” compared to the JI group.

Table 3 . Multivariate Logistic Regression Analysis Adjusting for Age and Gender

OutcomeArab Israel compared to Jewish IsraeliFormer Soviet Union compared to Jewish IsraeliFormer Soviet Union compared to Arab Israeli
Combined anal hypotension and hypocontractility3.759 (2.213-6.385)1.033 (0.546-1.954)0.275 (0.133-0.567)
P < 0.001P = 0.920P < 0.001
Anal hypotension with normal contractility-1.393 (0.617-3.143)-
P = 0.996P = 0.425P = 0.996
Dyssynergia0.575 (0.339-0.976)1.168 (0.589-2.319)1.817 (0.891-3.147)
P = 0.040P = 0.658P = 0.103

Data are presented as adjusted odds ratio (95% confidence interval).

P < 0.05 was considered statistically significant.



A more robust model was then constructed adjusting for age, gender, smoking, diabetes, and obesity (Table 4). Even controlling for these variables, the AI group remained several times more likely to have “combined anal hypotension and hypocontractibility” than the other groups, although “dyssynergia” became non-significant.

Table 4 . Multivariate Logistic Regression Analysis Adjusting for Age, Gender, Smoking, Diabetes, and Obesity

OutcomeArab Israel compared to Jewish IsraeliFormer Soviet Union compared to Jewish IsraeliFormer Soviet Union compared to Arab Israeli
Combined anal hypotension and hypocontractility5.114 (2.753-9.498)1.137 (0.582-2.223)0.222 (0.100-0.496)
P < 0.001P = 0.707P < 0.001
Anal hypotension with normal contractility-1.453 (0.580-3.640)-
P = 0.997P = 0.425P = 0.997
Dyssynergia0.689 (0.373-1.271)1.547 (0.701-3.415)2.247 (0.924-5.464)
P = 0.233P = 0.280P = 0.074

Data are presented as adjusted odds ratio (95% confidence interval).

P < 0.05 was considered statistically significant.



Finally, additional multivariate analyses were performed on the subgroup of women adjusting for the impact of age and parity (Table 5). These analyses showed that the AI group remained several times more likely to have “combined anal hypotension and hypocontractibility” compared to the other groups despite controlling for parity.

Table 5 . Multivariate Logistic Regression Analysis of Women Adjusting for Age and Parity

OutcomeArab Israel compared to Jewish IsraeliFormer Soviet Union compared to Jewish IsraeliFormer Soviet Union compared to Arab Israeli
Combined anal hypotension and hypocontractility2.740 (1.467-5.116)1.077 (0.508-2.283)0.393 (0.156-0.989)
P = 0.002P = 0.846P = 0.047
Anal hypotension with normal contractility-1.136 (0.453-2.848)-
P = 0.997P = 0.786P = 0.997
Dyssynergia0.563 (0.298-1.066)1.187 (0.535-2.633)2.105 (0.803-5.525)
P = 0.078P = 0.674P = 0.130

Data are presented as adjusted odds ratio (95% confidence interval).

P < 0.05 was considered statistically significant.


Discussion

This is the first study to evaluate and show differences in HR-ARM findings in patients with FI based on ethnicity. As such, this study adds to the literature on ethnic differences in patients with FI.

Studies showing racial or ethnic differences in FI rates mainly come from the diverse population of the United States. The largest such study included over 71 000 participants involved in the National Gastrointestinal Survey.1 This study, including both men and women, found significant differences in FI rates based on ethnicity and race. White individuals were more likely to have ever experienced FI compared to black or Asian individuals. Additionally, Hispanic participants were even more likely to report FI than white participants. The authors hypothesized that differing rates of pelvic organ prolapse and pelvic organ dysfunction may account for these differences in prevalence. Another study also showed increased rates of FI amongst both white women and men as compared to blacks.17

A study from Alabama also showed that black women were less likely to report FI than white women, but showed no difference amongst men.2 Many studies on FI are conducted just amongst women, and this finding that black women have lower rates of FI than white women has been repeatedly shown.3,18-20 One study also showed that American Indian/Native Alaskan women had lower rates of FI than white women.19 Data on Hispanic women has been more variable with the largest study showing a higher rate of FI compared to white women,1 but other studies showing either no difference19 or a lower prevalence compared to white women,21,22 with potential reporting bias being proposed as the reason for this discrepancy.1,22

While these studies evaluated clinical rates of FI between races and ethnicities, there is a lack of studies evaluating ethnic differences in HR-ARM. HR-ARM is an important diagnostic technique as it can objectively assess anorectal sensorimotor function, obtaining measurements that describe voluntary and involuntary control of the anal canal, rectoanal coordination, and rectal sensation.8 Studies of healthy volunteers, in which normal values for HR-ARM are obtained, tend to come from mostly homogenous populations, therefore limiting the ability to compare between races and ethnicities. For example, studies from Western populations tend to come from heavily Caucasian populations,11,23 while studies from Asian exclusively contain Asian subjects.10 The authors of a study evaluating normal values in a Korean population noted differences in their values as compared to a study of Western volunteers, and they hypothesized that differences in physical stature and physique between ethnic groups may contribute to these differences in HR-ARM measurements.10 However, this suggestion was debated by others, with multiple other factors, including differences in HR-ARM technique, being suggested as the actual cause.24 Regardless, the lack of studies from diverse, multiethnic populations in which these groups can be compared head-to-head remains one of the limitations of our knowledge of HR-ARM values at this time.

One study evaluated differences in ARM findings between men and women with FI.25 This study showed that there were differences in the pathophysiology of FI between the sexes. Women were more likely to have structural abnormalities, while men were more likely to have impaired rectal sensation and functional disturbances of evacuation. This difference in pathophysiology can be explained by the differences in anatomy and effect of childbirth between the sexes.

However, in our study, we also found differences in pathophysiology between ethnicities. AI subjects were more likely to suffer from “combined anal hypotension and hypocontractibility” than SU and JI subjects, even after accounting for age, sex, parity, smoking, diabetes, and obesity. This objective finding is much harder to explain. Previous studies on clinical rates of FI hypothesized that differing rates of pelvic organ prolapse and pelvic organ dysfunction may account for differences in FI prevalence.1 At the current time we are unable to effective explain our findings. The AI population is known to have higher rates of diabetes, obesity, and smoking than other populations in Israel,26-28 and all of these are known risk factors for FI.1,20 However, we accounted for these variables in the study, and while all 3 medical conditions were more common in the AI group, they still did not explain the HR-ARM differences between the groups. This study serves as a reminder that FI is a complex process with many different etiologies and contributing factors, and we still do not fully understand all of the factors involved.

We also found a relatively high rate of “rectoanal areflexia” (11.3%). This may be related to low resting anal pressures noted in some cases which can make evaluation for rectoanal inhibitory reflex (RAIR) more difficult, as well as the high prevalence of diabetes which can also affect RAIR.29 No differences were noted between the ethnic groups.

This study has some limitations. Given the nature of the study, we were unable to collect all of the data that we would have wanted. For example, we were able to obtain information on parity and the number of children that each subject had, but we had no data on the method of childbirth or incidence of perineal trauma during delivery. No did we have data on other defecatory disorders such as constipation or diarrhea, prior abdominal or pelvic surgeries, or a history of pelvic organ dysfunction. All subjects were referred for HR-ARM to evaluate FI, but it is possible that some subjects may have had severe urgency or diarrhea and not true FI. We also had no data on the severity or characteristics of the FI, and no standardized incontinence score, such as the Wexner Continence Grading Scale or the St. Marks Incontinence Scare, was used.30,31 The normal values used in this study came from another institution,11 and they used different parameters to obtain these measurements than were recommended by the London classification.8 It is unclear how this may have affected our results. Additionally, no data on the subjects’ treatments or clinical outcomes was available. Finally, while there is data that clinical rates of FI vary by race or ethnicity in other populations, it is not clear what the rate of FI is in the overall Israeli population or if there are any differences in FI rates between the 3 ethnic groups in this study. Despite these limitations, this study benefits from its large number of subjects, diverse population, and use of the London classification.

In conclusion, this study shows that ethnicity impacts HR-ARM findings in patients with FI. AI subjects were more likely to have abnormalities in anal tone and contractility that could not be explained by known confounding variables such as age, sex, parity, smoking, diabetes, and obesity. Future studies on ethnically diverse populations evaluating the clinical relevance of these findings and the complex pathophysiology leading to FI are certainly warranted.

Supplementary Material

Note: To access the supplementary table mentioned in this article, visit the online version of Journal of Neurogastroenterology and Motility at http://www.jnmjournal.org/, and at https://doi.org/10.5056/jnm21233.

Financial support

None.

Conflicts of interest

None.

Author contributions

Daniel L Cohen: study concept and design, data acquisition and interpretation, writing the manuscript, and critical review; Amir Mari, Anton Bermont, and Dana Zelnik Yovel: data acquisition and interpretation, and critical review; and Vered Richter and Haim Shirin: study concept and design, and critical review.

References
  1. Menees SB, Almario CV, Spiegel BMR, Chey WD. Prevalence of and factors associated with fecal incontinence: results from a population-based survey. Gastroenterology 2018;154:1672-1681, e3.
    Pubmed KoreaMed CrossRef
  2. Markland AD, Goode PS, Burgio KL, et al. Incidence and risk factors for fecal incontinence in black and white older adults: a population-based study. J Am Geriatr Soc 2010;58:1341-1346.
    Pubmed KoreaMed CrossRef
  3. Berger MB, Delancey JO, Fenner DE. Racial differences in fecal incontinence in community-dwelling women from the EPI study. Female Pelvic Med Reconstr Surg 2013;19:169-174.
    Pubmed KoreaMed CrossRef
  4. Saldana Ruiz N, Kaiser AM. Fecal incontinence - challenges and solutions. World J Gastroenterol 2017;23:11-24.
    Pubmed KoreaMed CrossRef
  5. Sbeit W, Khoury T, Mari A. Diagnostic approach to faecal incontinence: what test and when to perform? World J Gastroenterol 2021;27:1553-1562.
    Pubmed KoreaMed CrossRef
  6. Pehl C, Seidl H, Scalercio N, et al. Accuracy of anorectal manometry in patients with fecal incontinence. Digestion 2012;86:78-85.
    Pubmed CrossRef
  7. Yeap ZH, Simillis C, Qiu S, Ramage L, Kontovounisios C, Tekkis P. Diagnostic accuracy of anorectal manometry for fecal incontinence: a meta-analysis. Acta Chir Belg 2017;117:347-355.
    Pubmed CrossRef
  8. Carrington EV, Heinrich H, Knowles CH, et al. The international anorectal physiology working group (IAPWG) recommendations: standardized testing protocol and the London classification for disorders of anorectal function. Neurogastroenterol Motil 2020;32:e13679.
    CrossRef
  9. Lee TH, Bharucha AE. How to Perform and interpret a high-resolution anorectal manometry test. J Neurogastroenterol Motil 2016;22:46-59.
    Pubmed KoreaMed CrossRef
  10. Lee HJ, Jung KW, Han S, et al. Normal values for high-resolution anorectal manometry/topography in a healthy Korean population and the effects of gender and body mass index. Neurogastroenterol Motil 2014;26:529-537.
    Pubmed CrossRef
  11. Oblizajek NR, Gandhi S, Sharma M, et al. Anorectal pressures measured with high-resolution manometry in healthy people-Normal values and asymptomatic pelvic floor dysfunction. Neurogastroenterol Motil 2019;31:e13597.
    Pubmed KoreaMed CrossRef
  12. Shadmi E, Admi H, Ungar L, et al. Cancer care at the hospital-community interface: perspectives of patients from different cultural and ethnic groups. Patient Educ Couns 2010;79:106-111.
    Pubmed CrossRef
  13. Ibrahim R, Eviatar Z, Aharon-Peretz J. Metalinguistic awareness and reading performance: a cross language comparison. J Psycholinguist Res 2007;36:297-317.
    Pubmed CrossRef
  14. Bentwich ME, Dickman N, Oberman A. Human dignity and autonomy in the care for patients with dementia: differences among formal caretakers from various cultural backgrounds. Ethn Health 2018;23:121-141.
    Pubmed CrossRef
  15. Israel Central Bureau of Statistics. Population, by population group. Available from URL: https://www.cbs.gov.il/en/publications/Pages/2021/Population-Statistical-Abstract-of-Israel-2021-No.72.aspx (accessed 15 June 2023).
  16. Israel Central Bureau of Statistics. Jews, by country of origin and age. Available from URL: https://www.cbs.gov.il/en/publications/Pages/2021/Population-Statistical-Abstract-of-Israel-2021-No.72.aspx (accessed 15 June 2023).
  17. Quander CR, Morris MC, Melson J, Bienias JL, Evans DA. Prevalence of and factors associated with fecal incontinence in a large community study of older individuals. Am J Gastroenterol 2005;100:905-909.
    Pubmed CrossRef
  18. Matthews CA, Whitehead WE, Townsend MK, Grodstein F. Risk factors for urinary, fecal, or dual incontinence in the Nurses' Health Study. Obstet Gynecol 2013;122:539-545.
    Pubmed KoreaMed CrossRef
  19. Brown HW, Wexner SD, Segall MM, Brezoczky KL, Lukacz ES. Accidental bowel leakage in the mature women's health study: prevalence and predictors. Int J Clin Pract 2012;66:1101-1108.
    Pubmed CrossRef
  20. Townsend MK, Matthews CA, Whitehead WE, Grodstein F. Risk factors for fecal incontinence in older women. Am J Gastroenterol 2013;108:113-119.
    Pubmed KoreaMed CrossRef
  21. Nygaard I, Barber MD, Burgio KL, et al. Prevalence of symptomatic pelvic floor disorders in US women. JAMA 2008;300:1311-1316.
    Pubmed KoreaMed CrossRef
  22. Varma MG, Brown JS, Creasman JM, et al. Fecal incontinence in females older than aged 40 years: who is at risk? Dis Colon Rectum 2006;49:841-851.
    Pubmed KoreaMed CrossRef
  23. Noelting J, Ratuapli SK, Bharucha AE, Harvey DM, Ravi K, Zinsmeister AR. Normal values for high-resolution anorectal manometry in healthy women: effects of age and significance of rectoanal gradient. Am J Gastroenterol 2012;107:1530-1536.
    Pubmed KoreaMed CrossRef
  24. Carrington EV, Grossi U, Knowles CH, Scott SM. Normal values for high-resolution anorectal manometry: a time for consensus and collaboration. Neurogastroenterol Motil 2014;26:1356-1357.
    Pubmed CrossRef
  25. Townsend DC, Carrington EV, Grossi U, et al. Pathophysiology of fecal incontinence differs between men and women: a case-matched study in 200 patients. Neurogastroenterol Motil 2016;28:1580-1588.
    Pubmed CrossRef
  26. Jaffe A, Giveon S, Wulffhart L, et al. Adult Arabs have higher risk for diabetes mellitus than Jews in Israel. PLoS One 2017;12:e0176661.
    Pubmed KoreaMed CrossRef
  27. Kalter-Leibovici O, Atamna A, Lubin F, et al. Obesity among Arabs and Jews in Israel: a population-based study. Isr Med Assoc J 2007;9:525-530.
  28. Israel Ministry of Health. Rates of smoking in Israel. Available from URL: https://www.health.gov.il/English/Topics/KHealth/smoking/Pages/SmokingRatesInIsrael.aspx (accessed 15 June 2023).
  29. Deen KI, Premaratna R, Fonseka MM, De Silva HJ. The recto-anal inhibitory reflex: abnormal response in diabetics suggests an intrinsic neuroenteropathy. J Gastroenterol Hepatol 1998;13:1107-1110.
    Pubmed CrossRef
  30. Jorge JM, Wexner SD. Etiology and management of fecal incontinence. Dis Colon Rectum 1993;36:77-97.
    Pubmed CrossRef
  31. Vaizey CJ, Carapeti E, Cahill JA, Kamm MA. Prospective comparison of faecal incontinence grading systems. Gut 1999;44:77-80.
    Pubmed KoreaMed CrossRef


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