Introduction

With the development of the economic level, people's diet structure has also changed, and digestive system diseases are increasing. The prevalence of chronic diarrhea in the United States is estimated to be 11–30% of the total population, affecting 6.6% of the U.S. population and affecting persons of all ages1,2. The global combined prevalence of chronic constipation is 14%, with little variation across geographic regions3. Chronic diarrhea and constipation have become one of the most common gastrointestinal disorders globally and have a serious impact on the quality of life.

According to reports, the prevalence of obesity among adults in the United States has reached 39.5% and is still increasing, and it is projected that nearly half of the adults in the United States will be obese by 20304,5. Along with the obesity epidemic, the prevalence and incidence of chronic inflammatory diseases of the gastrointestinal tract are on the rise globally. Some studies have reported an increased risk of chronic diarrhea in obese individuals compared to normal-weight individuals6,7, but others have reported a higher prevalence of constipation in class II and III obese adults8,9. Other studies have concluded that there is no significant association between obesity and functional constipation10,11.

These conflicting findings suggest that the past use of BMI to measure overall obesity may not adequately reflect associations with related diseases, and Park et al. proposed WWI as a new measure of obesity in 201812. WWI is an anthropometric indicator of central obesity, calculated as waist circumference (WC) divided by the square root of body weight, which can reflect fat and muscle mass components in different BMI categories13. Recent studies have reported that WWI is strongly associated with nephropathy, diabetes, and cardiovascular disease14,15,16. Chronic diarrhea and constipation are the most common gastrointestinal disorders, and exploring the association between WWI and them to clarify the role obesity plays in bowel habits is valuable and necessary.

Therefore, the purpose of this study was to investigate the association between WWI and chronic diarrhea and constipation in the U.S. population using the 2005–2010 NHANES database.

Methods

Survey description

Cross-sectional data are from NHANES, a program conducted by the National Center for Health Statistics (NCHS) to assess the health and nutritional status of children and adults in the United States. The stratified multi-stage probability strategy used in the study design of NHANES ensures a relatively representative enrollment of participants. The NHANES study protocol adheres to the ethical guidelines of the 1975 Helsinki Declaration and has been approved by the NCHS Research Ethical Review Board. Each study participant has signed an informed consent form.

Study population

The samples used were from three cross-sectional surveys (2005–2006, 2007–2008, and 2009–2010) from NHANES with data on "bowel health". A total of 31,034 adult participants (age ≥ 20 years) were enrolled in the study, from which we excluded patients with missing bowel habits (n = 16,415) and missing WWI (n = 381), we ended up with 14,238 eligible subjects, including those with normal bowel (n = 12,041), chronic diarrhea (n = 1099), and chronic constipation (n = 1098) (Fig. 1).

Figure 1
figure 1

Flowchart of the sample selection from NHANES 2005–2010, 2009–2010.

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Definition

Assessment of WWI

WWI was the exposure variable in this study. WWI is an anthropometric index that estimates central obesity by combining waist circumference(WC) and body weight data. WWI was calculated by dividing each participant's WC by the square root of their body weight, with the result rounded to two decimal places (WC in centimeters and body weight in kilograms). A higher WWI indicates a higher level of obesity.

Assessment of bowel habits

The bowel habits of the subjects were determined based on their responses to the Bowel Health Questionnaire. Participants were shown a card with a colorful picture and the Bristol Stool Form Scale (BSFS; Type 1-Type 7) and asked, "Please look at this card and tell me the number that corresponds to the type of stool that is usually or most commonly seen in your life". According to previous studies chronic constipation was defined as BSFS type 1 (hard lumps alone, such as nuts) or type 2 (sausage-like but lumpy), and chronic diarrhea was defined as BSFS type 6 (fluffy lumps with rough edges, pasty fecal matter) or type 7 (watery, no solid debris). Type 3, 4, 5 were defined as having normal bowel habits1,17,18,19.

Selection of covariates

The covariates in this study included demographic covariates such as gender, age, race (non-Hispanic white, non-Hispanic black, Mexican American, other), education level (less than high school, high school, or more than high school), and economic status (Low income: Poverty income ratio (PIR) < 1.3; Middle income: 1.3 ≤ PIR < 3.5; High income: PIR ≥ 3.5). In addition, we included several self-reported daily behavioral and laboratory covariates, including drinking status, smoking status, sleeping status, mental status (Not Depressed: Patient Health Questionnaire-9 (PHQ-9) score < 10; Depressed: PHQ-9 score ≥ 10), BMI (Underweight: BMI < 18.5; Normal weight: 18.5 ≤ BMI < 25; Overweight: 25 ≤ BMI < 30; Obese: BMI ≥ 30 kg/m2), as well as levels of C-reactive protein (mg/dL), HDL-C (mmol/L), Total cholesterol (mmol/L). Diabetes mellitus was also included in the analysis as a covariate, defined as self-reported being told and/or taking insulin and/or diabetes medication by a physician or health professional.

Statistical analysis

R (4.1.3) and EmpowerStats (2.0) were used for all statistical analyses. For all analyses, NHANES sampling weights were used. Means ± standard deviation (SD) were used for continuous variables and percentages for categorical variables. To investigate the association between WWI and chronic diarrhea and constipation, we used multivariate logistic regression analysis to calculate ORs and 95% confidence intervals. Multivariate regression analyses were constructed using three models: model 1: unadjusted for variables; model 2: adjusted for gender, age, and race; and model 3: adjusted for all covariates. For further sensitivity analysis, we categorized WWI into thirds to assess its robustness. Smooth curve fitting was used to address nonlinearities and a threshold effects analysis model was used to determine the presence of thresholds and breakpoints (K). Finally, subgroup analyses and interaction effect tests were performed to see if the results of the study were heterogeneous. Results were considered statistically significant at bilateral p < 0.05.

Ethics approval

This is an observational study. The NCHS Research Ethics Committee has confirmed that no ethical approval is required.

Results

Baseline characteristics of participants

We included a total of 14,238 subjects, of whom 12,041 had normal bowel habits, 1099 had chronic diarrhea, and 1098 had chronic constipation. The mean age of patients with chronic diarrhea and constipation was 50.07 ± 15.82, 45.50 ± 17.54 respectively, and the proportion of females was higher than that of males. Ethnicity was predominantly non-Hispanic white. The mean WWI values for chronic diarrhea and constipation were 11.16 ± 0.83, 10.92 ± 0.83, respectively.

Table 1 shows all the basic characteristics of the study population. We found statistical significance for gender, race, education level, socioeconomic status, drinking status, smoking status, sleep status, mental status, BMI, C-reactive protein, and WWI in diarrhea and constipation (p < 0.05).

Table 1 Basic characteristics of the study population.
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The association between WWI and chronic constipation

Table 2 shows the association between WWI and chronic constipation. In the Crude model and Fully adjusted model, WWI and chronic constipation had a significant positive correlation. In the Fully adjusted model, for every 1-unit increase in WWI score, subjects had a 16% increased risk of developing chronic constipation (OR [95% CI] 1.16 [1.04, 1.28]). When WWI was categorized into tertiles, the results were not statistically significant.

Table 2 The association between WWI and chronic constipation.
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Smoothed curve fitting showed a nonlinear relationship between WWI and chronic constipation (Fig. 2), and the breakpoint (K) was further calculated to be 9.77. On the left side of the breakpoint, the risk of chronic constipation increased 1.77-fold for every 1-unit increase in WWI (OR [95% CI] 2.77 [1.24, 6.17]), whereas no statistically significant results were found on the right side (OR [95% CI] 1.11 [1.00, 1.24]) (Table 3).

Figure 2
figure 2

Smoothed curve fit plot between WWI and chronic constipation.

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Table 3 Threshold effect analysis of WWI on chronic constipation.
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The association between WWI and chronic diarrhea

Table 4 shows the association between WWI and chronic diarrhea. We found a positive association between WWI and chronic diarrhea in all three models. In the Fully adjusted model, the risk of chronic diarrhea increased by 27% for every 1-unit increase in WWI score (OR [95% CI] 1.27 [1.14, 1.41]). Performing sensitivity analyses with WWI as a categorical variable (tertiles), we found that WWI remained positively associated with chronic diarrhea in the Fully adjusted model, with the highest WWI (tertile 3) having a 52% higher risk of developing chronic diarrhea than the lowest WWI (tertile 1) (OR [95% CI] 1.52 [1.23, 1.88]).

Table 4 The association between WWI and chronic diarrhea.
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Furthermore, we performed a smoothed curve-fitting test and did not detect nonlinear relationships.

Subgroup analysis

To assess whether the association between WWI and chronic diarrhea and constipation was influenced by a particular baseline characteristic, we performed subgroup analyses and interaction tests stratified by gender, economic status, sleep status, mental status, diabetes, and BMI. The results of the interaction test showed that none of the covariates had a significant effect on the association between WWI and chronic diarrhea and constipation (all p for interaction > 0.05). This suggests that the association between WWI and chronic diarrhea and constipation was consistent across all six subgroups, with stable results. Notably, we did not find a specific effect of BMI on the association between WWI and chronic constipation (Table 5).

Table 5 Subgroup analysis.
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Discussion

Based on our cross-sectional study of 14,238 subjects from 2005 to 2010, we found a significant positive correlation between WWI and chronic diarrhea. There was a nonlinear relationship between WWI and chronic constipation, with a positive correlation between the two on the left side of the breakpoint (9.77) and no statistical significance on the right side.

To our knowledge, this is the first study to assess the relationship between WWI and bowel habits. Previous studies have linked factors such as depression, sleep status, diabetes, and lipid levels to gastrointestinal symptoms17,20,21. After adjusting for these confounders as much as possible, we found a significant positive association between WWI and chronic diarrhea. Interestingly, after excluding confounders, we found a similar positive association between WWI and chronic constipation. Elevated WWI positively associated with both diarrhea and constipation? This may seem like contradictory results. However, the later threshold analysis gave us a reasonable explanation.

In the nonlinear association between WWI and chronic constipation, we found that elevated WWI was associated with an increased risk of chronic constipation only when the WWI was < 9.77. 9.77 belongs to the lowest tertile of WWI, from which we can infer that an increase in WWI is closely related to chronic constipation in people with insignificant obesity, while in people with high obesity whose WWI is higher than 9.77, a continued increase in WWI is more closely related to chronic diarrhea.

The association between obesity and bowel habits has been characterized by conflicting results in previous studies. Some studies have shown a higher prevalence of constipation in the obese population8,9, others have suggested that increased BMI is not significantly associated with constipation11,22, and some have shown that overweight is negatively associated with constipation (OR [95% CI] 0.4 [0.2, 0.9])23, while others have suggested that high levels of obesity are significantly associated with chronic diarrhea24,25,26.

In the past, BMI could not adequately reflect the association between obesity and bowel habits and could easily lead to conflicting findings. Our study used a novel obesity index, the WWI, which has a stronger ability to identify obesity than the traditional BMI, WC, and waist-to-hip ratio, and can reflect centripetal obesity independent of body weight. A series of studies further confirmed the advantages of WWI in accurately assessing central and visceral obesity27,28,29,30. In this study, we found a threshold for the association between WWI and chronic constipation, which may be one of the explanations for the fact that obesity is associated with both constipation and diarrhea and that different levels of obesity lead to different bowel habits.

Many studies have now explored the mechanisms underlying obesity and bowel habits. Regarding diarrhea, some studies have shown that bile acid malabsorption and colonic transit are faster in obese individuals thus predisposing them to diarrhea31,32,33, and some studies have found that both obese individuals and patients with irritable bowel syndrome-diarrhea type have an increased proportion of Bacteroides thickettsii/anaplasmosis, suggesting that dysfunctional flora may be one of the causes of diarrhea34. Regarding constipation, some studies have shown that obese individuals have reduced levels of growth hormone-releasing peptide, increased levels of leptin, limited gastric emptying, and slower gastric peristalsis leading to constipation35,36. Some studies have also pointed out that the increased amount of fat entering the intestine in obese patients affects the release of some hormones, causing relaxation of colonic smooth muscle and obstruction of the propulsion of intestinal contents, thus causing constipation37,38.

In conclusion, the rise in WWI is associated with abnormalities in bowel habits. Studies have shown that appropriate physical activity and prudent/healthy dietary patterns (containing plenty of fruit, vegetables, poultry, fish, low-fat dairy, and whole grains) help to maintain a healthy weight and correct poor bowel habits39,40. It has also been found that a higher intake of dietary galactooligosaccharides is associated with a reduction in body fat41 and that different forms of dietary fiber (total, insoluble, or soluble) can significantly reduce body weight in high-fat mice and have an effect on the intestinal flora thereby improving defecation42. This suggests that proper physical activity, a healthy dietary pattern, and a rich intake of dietary fiber may benefit normal bowel movements and help us maintain healthy bowel habits.

Finally, we performed subgroup analyses and interaction tests. The results showed that WWI was not affected by each confounding factor and the obtained results were stable. This proves that WWI is a stable indicator for assessing the association between obesity and chronic diarrhea and constipation.

Our study has several strengths. Firstly, we included a sufficiently large sample size and adjusted for known confounding covariates, strengthening the generalizability and reliability of our findings. Secondly, we comprehensively explored the association between WWI and bowel habits, identified breakpoints in the association between WWI and chronic constipation, and compared it with chronic diarrhea in an innovative way. Finally, we performed subgroup analyses and interaction tests to confirm the stability of the results. However, this study has some limitations. Firstly, the cross-sectional design of this study limits causal inferences between WWI and gut health. Secondly, although we adjusted for many important covariates, we could not eliminate the effects of other possible confounding variables. Thirdly, chronic constipation was defined through participants' self-reports, and the information collected may have been influenced by participants' subjective awareness. Fourthly, due to the limited information in the NHANES database, we were unable to further explore how WWI and bowel habits change over time, and more rigorous randomized controlled trials are needed to explore this in depth.

Conclusion

Elevated levels of WWI are associated with an increased risk of chronic diarrhea, and there is a nonlinear positive correlation with chronic constipation. WWI is a stable and valid indicator for assessing the gut health of adults in the U.S. We should be mindful of the importance of establishing healthy dietary and lifestyle habits in our daily lives to maintain a good level of body fat and sustain healthy bowel habits.