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Percentage of body fat is associated with increased risk of diverticulosis: A cross sectional study

  • Chi-Wei Shih,

    Roles Data curation, Formal analysis, Writing – original draft

    Affiliation Department of Internal Medicine, Tri-Service General Hospital, School of Medicine, National Defense Medical Center, Taipei, Taiwan, Republic of China

  • Yu-Hsin Chen,

    Roles Data curation, Formal analysis, Writing – original draft

    Affiliations Department of Emergency Medicine, Hualien Armed Forces General Hospital, Tri-Service General Hospital, National Defense Medical Center, Taipei, Taiwan, Republic of China, Department of Emergency Medicine, Taichung Veterans General Hospital, Taichung, Taiwan, Republic of China

  • Wei-Liang Chen

    Roles Conceptualization, Data curation, Software, Writing – review & editing

    weiliang0508@gmail.com

    Affiliations Division of Family Medicine, Department of Family and Community Medicine, Tri-Service General Hospital, School of Medicine, National Defense Medical Center, Taipei, Taiwan, Republic of China, Division of Geriatric Medicine, Department of Family and Community Medicine, Tri-Service General Hospital; and School of Medicine, National Defense Medical Center, Taipei, Taiwan, Republic of China, Department of Biochemistry, National Defense Medical Center, Taiwan, Republic of China

Abstract

Background

Obesity has been indicated to be a risk factor of diverticulosis. However, plausible relationship remained controversial. This cross-sectional study elucidated the association between percentage of body fat and the risk of diverticulosis.

Methods

The study was conducted at a single medical center in Taiwan from 2000–2016 which enrolled 5557 adults with age above 20 years old receiving a health examination including self-reported questionnaires, measurement of percentage of body fat (PBF), blood test and colonoscopy at the Tri-Service General Hospital (TSGH). Logistic regressions were used to analyze the association between PBF and diverticulosis. Further stratification of participants was based on age and gender and three extended models were established for multivariable adjustment.

Results

243 of 3141 males and 103 of 2416 females were diagnosed with having diverticulosis. After covariates adjustment, only participants in the highest quartile of PBF (Q4 ≥33.8%) showed significantly positive association with the risk diverticulosis (OR 2.089, p <0.001). In subgroup analysis, the odds ratio for having diverticulosis in females was significantly higher than in males. In addition, We found that the odds ratio of having diverticulosis was higher in the group older than 60 years old compared to the younger group (OR 1.052; p<0.001; OR 1.043; p<0.001).

Conclusions

In conclusion, PBF was a potential risk factor of diverticulosis. Individuals with higher PBF exhibits increased risk of diverticulosis, especially in females. Furthermore, bioelectrical impedance analysis may create a simple, available and radiation-free way to assess the risk of diverticulosis.

Introduction

Colonic diverticulosis is a condition of having one or more diverticula protruding from mucosa and submucosa of colon. The real prevalence of diverticulosis remains unclear but it increases with age which has been reported in previous studies [1,2]. Besides, the incidence of diverticulosis has increased in Asia over the past decades [3]. In the past studies, frequent occurrence of constipation was thought to be a major cause of diverticulosis due to increased intraluminal pressure in colon. However, the hypothesis has been questioned by recent studies [4,5]. Most of patients with diverticulosis are asymptomatic. About 15% to 20% patients with diverticulosis develop clinical illness [6]. Three fourth of the symptomatic cases are presented with colicky abdominal pain without inflammation. The rest of one fourth develop diverticular bleeding, diverticulitis and a small number will complicate with bowel obstruction or abscess formation. The prevalence of diverticulosis is higher in old age than in young age, which is thought to be the most effective risk factor [7]. Several well-known risk factors of diverticulosis have also been reported in previous studies such as low dietary fiber, high total fat intake, physical inactivity and obesity [810]. As obesity is considered having a significant association with diverticulosis, many studies have been conducted with different methods of defining obesity. A retrospective study of Korean patients, Song et al. identified that there was no statistical significance between obesity and diverticulosis by multivariate analysis. [11]. In spite of Song’s study, a prospective cohort study conducted by Nagata reported that obesity defined by measuring visceral adipose tissue area had more sensitive correlation of diverticulosis than BMI [12]. Other parameters to define obesity, such as waist circumference and dietary habits have also been used in previous studies [13,14]. Furthermore, recent studies revealed that abdominal visceral fat measured by computed tomography provided a more predictive ability of diverticulosis than other parameters [12,15]. In our study, we measured percentage of total body fat to analyze the correlation between obesity and the incidence of diverticulosis. The aim of our study was to elucidate the relationship between the risk of diverticulosis and percentage of body fat by using bioelectrical impedance analysis.

Material and methods

Study sample

This cross-sectional study enrolled 5557 adults with age above 20 years old who underwent health examination at the TSGH from 2000–2016. The health examination included a laboratory data, body composition and detailed self-reported questionnaires. In addition, a diagnostic colonoscopy as a part of health examination was performed to identify any malignant polyps or other disease of colon such as diverticulosis. Before a diagnostic colonoscopy, all the participants were asked to complete detailed self-reported questionnaires. Those who reported any related abdominal symptom, such as abdominal tenderness or cramps, active rectal bleeding, fever, and nausea were not be able to have colonoscopy. All the colonoscopy was performed by experienced specialists after the participants had proper bowel preparation and fasted overnight. Any findings of diverticular bleeding, diverticulitis, familial polyposis syndrome or malignant tumors were excluded. All protocols in this cross-section study were approved by the Institutional Review Board (IRB) of TSGH. The TSGH IRB waived the need to obtain individual informed consent because these data were analyzed anonymously.

Measures

Bioelectrical impedance analysis (BIA) was a validated for assessing body composition analysis [16]. In comparison with other medical equipment, such as dual-energy X-ray absorptiometry, computerized tomography or magnetic resonance imaging, BIA was more maneuverable and less expensive and radiation exposure. We measured PBF by using BIA (InBody720, Biospace, Inc., Cerritos, CA, USA).

Assessments of covariates

The information of participants such as age, gender, smoking status and alcohol consumption were obtained by a self-completed questionnaire. We acquired smoking status by asking the question “Do you have a smoking habit”. For the alcohol consumption, we divided participants into two groups which were alcohol consumption and those who never consumed alcohol. All the participants had been fasting for at least 8 hours prior to blood draw. Blood samples such as total cholesterol, triglycerides, creatinine, and glucose were analyzed by standard methods.

Statistical analysis

Student’s t test was used to assess the differences in continuous variables, such as age, percentage of total body fat, serum cholesterol, triglycerides, creatinine, and fasting glucose. Smoking habit and alcohol consumption were regarded as categorical variables which were assessed by using Pearson’s chi-square tests. Three extended models were established for multivariable adjustment. The respective models were adjusted as follows: Model 1 = unadjusted; Model 2 = age, sex, total cholesterol, creatinine, triglyceride, fasting glucose; Model 3 = Model 2 + smoking, alcohol consumption. Logistic regression was applied to analyze the association between PBF and the risk of diverticulosis. Furthermore, we used receiving operator characteristic (ROC) curve analysis to determine the ideal gender-specific cut-off point for PBF to predict the risk of diverticulosis. We used the Youden’s index in order to find the ideal cut-off point which was regarded as the shortest distance between the upper left corner of the graph and the ROC curve. Two-side p values of less than or equal to 0.05 were considered as significant difference. All statistical analyses of this study were analyzed between June and August 2019 by using the Statistical Package for the Social Sciences, version18.0 (SPSS Inc., Chicago, IL, USA).

Results

5557 participants with 3141 males and 2416 females were enrolled in the study. Table 1 disclosed baseline characteristics of the study group. In our study, the females were prone to having higher percentage of body fat and total cholesterol and lower serum creatinine, triglyceride and fasting sugar. Smoking history and alcohol consumption were more prominent among males.

Table 2 showed the associations between diverticulosis and percentage of body fat. Among all participants, the odds ratio for having diverticulosis in unadjusted model 1 was 1.030 (95% CI 1.015–1.045, p<0.001). In adjusted model 2 and fully adjusted mode 3, the odds ratio were 1.045 (95% CI 1.025–1.064, p<0.001) and 1.045 (95% CI 1.025–1.065, p<0.001) which did not affect the statistical significance. We further divided the study population into two groups by gender in Table 2. In the fully adjusted model 3, the odds ratio for having diverticulosis in females was significantly higher than in males (odds ratio 1.076, p <0.001; odds ratio 1.029, p = 0.001, respectively).

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Table 2. Risks of diverticulosis between percentage of body fat and genders.

https://doi.org/10.1371/journal.pone.0264746.t002

Additionally, the participants were divided into two groups by age as shown in Table 3. Among the participants older than 60 years old, the odds ratios was 1.052 (p<0.001) for both mode1 2 and fully adjusted model 3 which were respectively significantly higher than the participants younger than 60 years old for having diverticulosis (odds ratio 1.042, p <0.001; odds ratio 1.043, p = 0.001, respectively). Moreover, we applied ROC curve to decide an optimal gender-specific cut-off point for percentage of body fat to predict the risk of diverticulosis. The results were shown in Table 4 and presented the significant associations with the risk of diverticulosis in each of the models of the two genders.

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Table 3. Risks of diverticulosis between percentage of body fat and age.

https://doi.org/10.1371/journal.pone.0264746.t003

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Table 4. Risks of diverticulosis between percentage of body fat and genders (according to gender-specific cut-off point).

https://doi.org/10.1371/journal.pone.0264746.t004

In Table 5, the participants were further divided into quartiles by PBF (Q1 < 24%; Q2: 24% to< 28.5%; Q3: 28.5% to< 33.8%; and Q4 ≥33.8%). We further displayed the association between the quartiles of PBF and the risk of diverticulosis. With fully adjustment of covariates, the odds ratios for diverticulosis among subjects with different PBF quartile were Q2: 1.304 (p = 0.117), Q3: 1.163 (p = 0.405) and Q4: 2.089 (p<0.001). Only participants in the highest quartile of PBF (Q4 ≥33.8%) showed significantly positive association with the risk diverticulosis (odds ratio: 2.089, p<0.001) after fully multivariate adjustments. In addition, the data were further analyzed separately by gender, as shown in Table 6. In Model 3, which was fully adjusted by multivariable analysis, there was a significant positive association between the highest quartile of PBF (Q4 ≥37.1%) and risk of diverticulosis in the female group with odds ratio of 2.522 (p = 0.014).

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Table 5. Risks of diverticulosis by quartile of percentage of body fat.

https://doi.org/10.1371/journal.pone.0264746.t005

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Table 6. Risks of diverticulosis between percentage of body fat and genders (by quartile of percentage of body fat).

https://doi.org/10.1371/journal.pone.0264746.t006

Discussions

Main findings

The present study showed a positive correlation between obesity and diverticulosis. In our analysis, participants with higher PBF were more likely to have diverticulosis. In addition, potential confounders were adjusted, such as age, gender, total cholesterol, triglyceride, creatinine, fasting glucose, alcohol consumption and smoking status. We found that females with higher PBF tended to have higher risk of diverticulosis in univariable analysis and the positive association was not displayed in males. Furthermore, we found that there was a stronger predictive ability for diverticulosis with a use of ROC curve analysis to decide an optimal gender-specific cut-off point for PBF.

Comparison with other studies

Few previous studies examined the impacts of BMI-defined obesity on diverticulosis and none of them revealed positive associations [11,17,18]. In contrast, a meta-analysis included 9 cross-sectional studies and 1 prospective cohort study through January 2017 reported an association between BMI-defined obesity and the risk of diverticulosis [19]. In spite of the positive relationship, the statistical heterogeneity of the meta-analysis was high and each of the studies from eastern countries revealed no association between obesity and diverticulosis which were opposite to the results of western countries. Two recent studies focused on the association with body fat, especially visceral body fat, on the risk of diverticulosis [12,15]. One study by Lee showed that total abdominal fat, abdominal visceral fat, and abdominal subcutaneous fat were significantly higher in the diverticulosis subgroup than in the controls. Besides, the other study by Nagata showed that diverticulosis was significantly associated with visceral adipose tissue area, even in people with normal weight [12]. The body fat of the two studies was both measured by CT scan.

Strengths

In our studies, bioelectrical impedance analysis was used as the measurement of PBF which created a non-invasive, maneuverable and radiation-free method to assess the risk of diverticulosis. Although the mechanism that linked obesity to diverticulosis still remained unclear, several connections behind the association had been promoted by previous studies. It was suggested that increasing intraluminal pressure was a plausible cause of diverticulosis. The speculated mechanism was intraluminal pressure caused diverticula protruding from mucosa and submucosa of colon. Besides, several studies identified obese individuals produced higher concentration of methane gas by gut bacterial flora than nonobese individuals. A higher concentration of methane gas in gut might lead to delaying transition of small bowel and decreasing motility of colon which was conjectured to increase intraluminal pressure and resulted in diverticulosis.

Besides, the correlation between gender and diverticulosis remained controversial in previous studies [17,20,21]. In a retrospective study of Japanese patients, Yamamichi et al. identified there was a significant positive correlation between diverticulosis and male subgroups in multivariate analysis [10]. However, in a prospective study of Korean patients, Song et al. reported no association between gender and diverticulosis [11]. We also found that the participants with older age were more likely to have diverticulosis than the younger participants which was in line with previous studies in Taiwan [20,21].

Limitations

Our study had four limitations needed to be considered. First, a few well-known lifestyles factors were not taken into account, such as dietary fiber intake and physical activity. However, the correlation between fiber intake and diverticulosis was still unclear. Several studies reported that low dietary fiber was associated with diverticulosis, but others revealed conflicting data [2224]. Physical activity was shown to have an inversely correlation with the risk of symptomatic diverticular disease in a large prospective study [9]. Despite that, to our knowledge, the association between dietary, physical activity and PBF should be existed. Thus, investigations of dietary and physical activity should be involved in the questionnaire in future studies. Second, it was well known that multiple risk factors were associated with diverticulosis. In our study, age, gender and PBF might be important risk factors in diverticulosis. However, the other risk factors needed to be considered as predictors and might have varying degrees of effects on diverticulosis. Third, self-election bias of the participants in the study might exist because all enrolments received health examination at their own expense, which meant that they intended to pay more attention to their health condition and higher economic status among population in Taiwan. Finally, we acquired smoking status by asking the question “Do you have a smoking habit”. For the alcohol consumption, we divided participants into two groups which were alcohol consumption and those who never consumed alcohol. However, without having information about duration and daily amount of alcohol consumption as well as smoking status might lower the power of these factors. And forth, the proportion of diverticulosis in our research was relatively lower than other researches. This might be due to the selection bias we mentioned above, and moreover, the sensitivity of colonoscopy to detect diverticulosis was less than radiological techniques [25].

Conclusions

In conclusion, PBF was a potential risk factor of diverticulosis. Individuals with higher PBF exhibits increased risk of diverticulosis, especially in females. PBF measured by bioelectrical impedance analysis may be a simple, available and radiation-free tool for assessing the risk of diverticulosis. Further longitudinal surveys and interventional designs are necessary to confirm the conclusions.

Acknowledgments

No financial disclosures were reported by the authors of this paper.

References

  1. 1. Stollman N, Raskin JB. Diverticular disease of the colon. Lancet (London, England). 2004;363(9409):631–9. Epub 2004/02/28. pmid:14987890.
  2. 2. Loffeld RJ, Van Der Putten AB. Diverticular disease of the colon and concomitant abnormalities in patients undergoing endoscopic evaluation of the large bowel. Colorectal disease: the official journal of the Association of Coloproctology of Great Britain and Ireland. 2002;4(3):189–92. Epub 2003/06/05. pmid:12780614.
  3. 3. Nagata N, Niikura R, Aoki T, Shimbo T, Itoh T, Goda Y, et al. Increase in colonic diverticulosis and diverticular hemorrhage in an aging society: lessons from a 9-year colonoscopic study of 28,192 patients in Japan. International journal of colorectal disease. 2014;29(3):379–85. Epub 2013/12/10. pmid:24317937.
  4. 4. Yamada E, Inamori M, Watanabe S, Sato T, Tagri M, Uchida E, et al. Constipation is not associated with colonic diverticula: a multicenter study in Japan. Neurogastroenterology and motility: the official journal of the European Gastrointestinal Motility Society. 2015;27(3):333–8. Epub 2014/12/04. pmid:25469640.
  5. 5. Braunschmid T, Stift A, Mittlbock M, Lord A, Weiser FA, Riss S. Constipation is not associated with diverticular disease—Analysis of 976 patients. International journal of surgery (London, England). 2015;19:42–5. Epub 2015/05/20. pmid:25980396.
  6. 6. Stollman NH, Raskin JB. Diagnosis and management of diverticular disease of the colon in adults. Ad Hoc Practice Parameters Committee of the American College of Gastroenterology. The American journal of gastroenterology. 1999;94(11):3110–21. Epub 1999/11/24. pmid:10566700.
  7. 7. De Cecco CN, Ciolina M, Annibale B, Rengo M, Bellini D, Muscogiuri G, et al. Prevalence and distribution of colonic diverticula assessed with CT colonography (CTC). European radiology. 2016;26(3):639–45. Epub 2015/06/25. pmid:26105021.
  8. 8. Aldoori WH, Giovannucci EL, Rimm EB, Wing AL, Trichopoulos DV, Willett WC. A prospective study of diet and the risk of symptomatic diverticular disease in men. The American journal of clinical nutrition. 1994;60(5):757–64. Epub 1994/11/01. pmid:7942584.
  9. 9. Aldoori WH, Giovannucci EL, Rimm EB, Ascherio A, Stampfer MJ, Colditz GA, et al. Prospective study of physical activity and the risk of symptomatic diverticular disease in men. Gut. 1995;36(2):276–82. Epub 1995/02/01. pmid:7883230; PubMed Central PMCID: PMC1382417.
  10. 10. Yamamichi N, Shimamoto T, Takahashi Y, Sakaguchi Y, Kakimoto H, Matsuda R, et al. Trend and risk factors of diverticulosis in Japan: age, gender, and lifestyle/metabolic-related factors may cooperatively affect on the colorectal diverticula formation. PloS one. 2015;10(4):e0123688. Epub 2015/04/11. pmid:25860671; PubMed Central PMCID: PMC4393308.
  11. 11. Song JH, Kim YS, Lee JH, Ok KS, Ryu SH, Lee JH, et al. Clinical characteristics of colonic diverticulosis in Korea: a prospective study. The Korean journal of internal medicine. 2010;25(2):140–6. Epub 2010/06/09. pmid:20526386; PubMed Central PMCID: PMC2880686.
  12. 12. Nagata N, Sakamoto K, Arai T, Niikura R, Shimbo T, Shinozaki M, et al. Visceral Abdominal Obesity Measured by Computed Tomography is Associated With Increased Risk of Colonic Diverticulosis. Journal of clinical gastroenterology. 2015;49(10):816–22. Epub 2014/11/21. pmid:25412157.
  13. 13. Dobbins C, Defontgalland D, Duthie G, Wattchow DA. The relationship of obesity to the complications of diverticular disease. Colorectal disease: the official journal of the Association of Coloproctology of Great Britain and Ireland. 2006;8(1):37–40. Epub 2006/03/08. pmid:16519636.
  14. 14. Seidell JC, Flegal KM. Assessing obesity: classification and epidemiology. British medical bulletin. 1997;53(2):238–52. Epub 1997/01/01. pmid:9246834.
  15. 15. Lee SP, Ahn YW, Lee OY, Lee KN. The relationship between colonic diverticulosis and abdominal visceral and subcutaneous fat accumulation measured by abdominal CT scan. The Turkish journal of gastroenterology: the official journal of Turkish Society of Gastroenterology. 2014;25(2):192–7. Epub 2014/07/09. pmid:25003681.
  16. 16. Coppini LZ, Waitzberg DL, Campos AC. Limitations and validation of bioelectrical impedance analysis in morbidly obese patients. Current opinion in clinical nutrition and metabolic care. 2005;8(3):329–32. Epub 2005/04/06. pmid:15809537.
  17. 17. Strate LL, Liu YL, Aldoori WH, Syngal S, Giovannucci EL. Obesity increases the risks of diverticulitis and diverticular bleeding. Gastroenterology. 2009;136(1):115–22.e1. Epub 2008/11/11. pmid:18996378; PubMed Central PMCID: PMC2643271.
  18. 18. Sharara AI, El-Halabi MM, Mansour NM, Malli A, Ghaith OA, Hashash JG, et al. Alcohol consumption is a risk factor for colonic diverticulosis. Journal of clinical gastroenterology. 2013;47(5):420–5. Epub 2012/11/21. pmid:23164685.
  19. 19. Wijarnpreecha K, Ahuja W, Chesdachai S, Thongprayoon C, Jaruvongvanich V, Cheungpasitporn W, et al. Obesity and the Risk of Colonic Diverticulosis: A Meta-analysis. 2018;61(4):476–83. 00003453-201804000-00013. pmid:29521829
  20. 20. Wang FW, Chuang HY, Tu MS, King TM, Wang JH, Hsu CW, et al. Prevalence and risk factors of asymptomatic colorectal diverticulosis in Taiwan. BMC gastroenterology. 2015;15:40. Epub 2015/04/19. pmid:25888375; PubMed Central PMCID: PMC4383068.
  21. 21. Yeo LX, Tseng TH, Chen WL, Kao TW, Wu LW, Fang WH, et al. Hypertension control and risk of colonic diverticulosis. Therapeutic advances in gastroenterology. 2019;12:1756284819855734. Epub 2019/06/28. pmid:31244897; PubMed Central PMCID: PMC6580716.
  22. 22. Crowe FL, Appleby PN, Allen NE, Key TJ. Diet and risk of diverticular disease in Oxford cohort of European Prospective Investigation into Cancer and Nutrition (EPIC): prospective study of British vegetarians and non-vegetarians. BMJ (Clinical research ed). 2011;343:d4131. Epub 2011/07/21. pmid:21771850; PubMed Central PMCID: PMC3139912.
  23. 23. Crowe FL, Balkwill A, Cairns BJ, Appleby PN, Green J, Reeves GK, et al. Source of dietary fibre and diverticular disease incidence: a prospective study of UK women. Gut. 2014;63(9):1450–6. Epub 2014/01/05. pmid:24385599; PubMed Central PMCID: PMC4145436.
  24. 24. Peery AF, Barrett PR, Park D, Rogers AJ, Galanko JA, Martin CF, et al. A high-fiber diet does not protect against asymptomatic diverticulosis. Gastroenterology. 2012;142(2):266–72.e1. Epub 2011/11/09. pmid:22062360; PubMed Central PMCID: PMC3724216.
  25. 25. Halligan S, Saunders B. Imaging diverticular disease. Best practice & research Clinical gastroenterology. 2002;16(4):595–610. Epub 2002/10/31. pmid:12406453.