Association Between Dietary Phosphorus Intake and Chronic Constipation in Adults: Evidence from the National Health and Nutrition Examination Survey

Abstract

Background: Several studies suggest a link between micronutrients and constipation. However, the relationship between constipation and phosphorus has rarely been examined. Consequently, the main aim of this study was to investigate the link between changes in the prevalence of chronic constipation and changes in dietary phosphorus intake among adults in the NHANES (National Health and Nutritional Examination Survey).

Methods: Data were extracted from the NHANES database from 2005–2010. In total, after inclusion and exclusion, 13 948 people were included in the analysis. Dietary information was collected using the respondents’ 24-hour dietary records. We conducted several multiple logistic regression analyses to examine the correlation between phosphorus intake and poor bowel movement.

Results: After multi-variate adjustment in model Ⅲ, there was a statistically significant association between chronic constipation and each additional 0.1 g intake of dietary phosphorus (odds ratio (OR), 0.97; 95% confidence interval (CI), 0.95, 1.00; P=0.034 for stool consistency vs OR, 0.94; 95% CI, 0.90, 0.99; P=0.027 for stool frequency). After multi-variate adjustment in model Ⅲ, OR values and 95% CI from the second to fourth quartiles compared to the first quartile (reference group) were 0.92(0.66, 1.27), 0.73(0.47, 1.13), and 0.39(0.20, 0.76), respectively.

Conclusions: This study revealed a negative correlation between phosphorus intake and chronic constipation. Further studies in different settings should be considered to verify these findings.

Introduction

Constipation is clinically characterized by difficulty in defecation, less defecation, decreased frequency, or incomplete defecation and related discomfort[1]. It is well known that both stool frequency and consistency play a crucial role in the clinical manifestations of chronic constipation[2]. According to an article published in Nature Reviews Disease Primers in 2017, the overall prevalence of chronic constipation across all studies was 14%[1]. Besides this, the incidence of chronic constipation varies between genders, with women being approximately twice as likely to have constipation than men[3]. In addition, constipation is affected by age, socioeconomic status, etc.[1]. The preferred treatment option for people with chronic constipation is usually to regulate diet and lifestyle[1].

Phosphorus is an indispensable trace element in the human body[4]. Phosphate enemas are used to treat constipation because of their permeability, which increases stool bulk[5]. Sodium phosphate enemas therapy is effective in the treatment of chronic constipation[6]. Nevertheless, the relationship between the prevalence of chronic constipation and changes in dietary phosphorus intake has been poorly studied in the general population. Although related articles have reported a relationship between the intake of trace elements and chronic constipation, few studies focus on the relationship between the changes in phosphorus intake in trace elements and chronic constipation[7]. Trace element phosphorus is found in many foods, with the highest concentration in milk and its processed products, as well as in meat and poultry[8].

In articles published using the NHANES database, studies on constipation are mostly defined by stool frequency and consistency[9^, 10]. Different studies have shown that different definitions of constipation can lead to differences in prevalence[1^, 7]. Therefore, it is not known whether differences in the definition of constipation affect the relationship between the prevalence of chronic constipation and changes in dietary phosphorus intake.

The NHANES database is a large population-based database based in the United States and it provided invaluable information for this study. We used the NHANES database to statistically control for relevant confounding factors, and explore the relationship between the intake of trace element phosphorus and chronic constipation. This provides a reference for future research on the relationship between the relationship between the intake of trace element phosphorus and chronic constipation.

Methods

Study Participants

We extracted detailed data on respondents from the NHANES database of cross-sectional studies from 2005–2010 for analysis and research. The data for these three cycles included a bowel health questionnaire (BHQ). These data were collected using a hierarchical multilevel probability design, allowing for a weighted analysis of the population. The study was authorized by the National Center for Health Statistics’ Ethics Review Board. Each participant signed an informed consent form. The work on this database was organized by the National Center for Health Statistics of the Center for Disease Control and Prevention (Atlanta, GA, USA).

Data on 17 132 people aged 20 and older were collected. 

17132 people aged 20 and older were collected from 2005-2010 in NHANES. Data for 2541 individuals that lacked information on stool consistency and frequency were removed. We also excluded 237 people with dietary phosphorus deficiency, as well as 379 pregnant women. Further 27 participants with phosphorus levels > 4000mg were eliminated. The detailed flow chart of population selection is presented in Figure 1.

Definition of Constipation

We defined chronic constipation using the description of stool frequency and consistency in the detailed bowel health questionnaire used in the following three cycles: 2005–2006, 2007–2008, and 2009–2010. The Bristol Stool Form Scale divides stool consistency into 7 types. The first two categories were regarded as constipation, while the remaining types were considered as non-constipation.

When collecting information on stool frequency, participants were asked the following: “How many times a week do you usually have a bowel movement?” Constipation was defined when stool frequency was not more than two bowel movements per week, and non--constipation when stool frequency was more than two bowel movements per week.

A sensitivity analysis was implemented using three constipation-related symptoms. We classified non-constipation and constipation according to self-reported constipation questionnaires. Laxatives were divided into used and not used. If people answered most days, use was defined as frequent. The following situations were considered infrequent: use of laxatives 2–3 times a month, once a month or 1–3 times a month. Because these three parameters were only used in the 2009–2010 cycle, we carried out the sensitivity analysis for this cycle only[11].

Phosphorus Intake

The collection of dietary information has been previously described[12-14]. The multi-pass approach was used to collect 24-hour recall of dietary phosphorus intake. Accurate information on participants’ food and drink intake was collected during the 24-hour period. Participants were each interviewed twice, and their dietary recalls were collected on both occasions. The first was a face-to-face interview with participants at the Mobile Examination Center, and the second was conducted by telephone 3–10 days later. We used the mean of the two diet recalls for the calculation, and if the participants had information missing from the second diet, we used the information from the first.

Covariates

After referring to previous reports on phosphorus and gut-related diseases, we included the following relevant covariates: milk consumption, energy, total fat, dietary fiber, selenium, magnesium, calcium, sodium, potassium, smoking, alcohol consumption, diabetes, hypertension, depression, poor oral health, income-poverty ratio, physical activity, body mass index (BMI), education, age, sex, and ethnicity [13-15]. We divided age into three groups (<45, ≥45＜65, and ≥65 years old). Ethnicity included the following race categories: Non-Hispanic Black, Non-Hispanic White, Mexican American, Other Hispanic, and Other. Education level was divided into the following categories: grades 0-12, some college or above, and high school grad/GED. Income-poverty ratio (%) was classified into two types: <2 and ≥2. Based on the recommendations of the United States Departments of Health and Human Services, we used the weekly metabolic equivalent of task to classify physical activity as inactive (<500) or active (≥500). We defined participants who had smoked <100 cigarettes in their lifetime as never smoking, those who had smoked >100 cigarettes but did not smoke currently as former smokers, and those who smoked more than 100 cigarettes and still smoked on some days or every day as now smokers. We referred to participants who drank 12 or more alcoholic beverages per year as drinkers, otherwise not. We divided the frequency of milk consumption into never drinking, <once a week as rarely drinking, ≥once a week but <once a day as sometimes drinking, and ≥once a day as frequent drinking. BMI (kg/m²) was divided into three categories: obese (≥30), overweight (25–29.9), and under/normal weight (<25). In all of the following cases, we diagnosed the participants as having diabetes: First, the doctor diagnosed the participant with diabetes mellitus. Second, the test result of the oral glucose tolerance test or random blood glucose was greater than or equal to 11.1 mmol/L. Third, the participant’s fasting blood glucose value was greater than or equal to 7.0 mmol/L. Fourth, the glycohemoglobin HbA1 of the respondents was greater than or equal to 6.5%. Fifth, participants received oral diabetes medication or intramuscular insulin. We used hypertension medication use, hypertension-related questionnaires, and systolic and diastolic blood pressure readings to determine whether or not the participant had hypertension. Participants with a PHQ-9 score of 10 or greater were diagnosed with depression. Dietary information on total fiber (T1<11.6; T2, 11.6–18.0; T3≥18.1 g/day), total fat (T1<55.4; T2, 55.4–85.0; T3 ≥ 85.1 g/day), protein (T1<61.0; T2, 61.1–88.1; T3≥88.2 g/day), calcium (T1<644.5; T2, 644.5–1004.0; T3≥1004.1 mg/day), sodium (T1<2523.5; T2, 2523.5–3689.0; T3≥3689.1 mg/day), potassium (T1<2060.0; T2, 2060–2910.0; T3≥2910.1 mg/day), and total energy (T1<1590.0; T2, 1590.0–2247.0; T3≥2247.1 kcal/day) intake was collected by trained interviewers.

Statistical Analyses

We explored the relationship between changes in dietary phosphorus intake and the prevalence of chronic constipation in the NHANES dataset using statistical methods for weighted sampling. As oversampling had occurred in some populations, the weighted statistical method was applied to the data, in order to avoid bias and ensure the accuracy of results. We set the continuous variables as categorical variables through the study of relevant literature. Categorical variables are expressed as weighted percentages and confidence intervals (95% CI). Furthermore, we investigated the relationship between the two using several multiple logistic regression models adjusted for relevant confounders. Model Ⅰ is the unadjusted model. In model Ⅱ the data were adjusted for participants’ age (<45; ≥45＜65; ≥65 years old), sex, and ethnicity (Non-Hispanic White, Non-Hispanic Black, Mexican American, Other Hispanic, and Other). Model-Ⅲ continued to adjust for the following variables on the basis of model Ⅱ: income-poverty ratio (%) (<2, ≥2, or missing), physical activity (<500, ≥500, or missing), BMI (kg/m²) (<25, 25–29.9, and ≥30), poor oral health (yes, no), hypertension (yes, no), depression (yes, no), diabetes (yes, no), smoking (never, former, and now), alcohol consumption (yes, no), milk consumption (often, sometimes, rarely, never), and energy (T1<1590.0; T2, 1590.0–2247.0; T3≥2247.1 kcal/day).

In addition, we used smooth curve fitting after adjusting for confounding factors to show more intuitively the relationship between the two. In the curve fitting graph, the middle line represents the effect size, and the area on both sides of the line represents the 95% confidence interval. We further applied interaction, stratified analysis, and univariate analysis based on the variables, including age (<45, ≥ 45＜65, and ≥ 65 years old), sex, and ethnicity (Non-Hispanic White, Non-Hispanic Black, Mexican American, Other Hispanic and Other), BMI (kg/m²) (<25, 25–29.9, and ≥ 30), physical activity (<500, ≥500, or missing), poor oral health (yes, no), hypertension (yes, no), depression (yes, no), diabetes (yes, no), smoking(never, former, and now), alcohol consumption (yes, no), milk consumption (often, sometimes, rarely, never), energy (T1<1590.0; T2, 1590.0-2247.0; T3≥2247.1 kcal/day), and income-poverty ratio (%) (<2, ≥2, or missing). Dummy variables were used to indicate missing covariate values[16].

P<0.05 was considered statistically significant. All statistical analyses were performed using R packages (The R Foundation; http://www.r-project.org; version 3.4.3) and Empower (R) (www.empowerstats. com, X&Y solutions, inc. Boston, Massachusetts).

Results

Clinical Characteristics

When using the Bristol Stool Form Scale to define whether the population had chronic constipation, the weighted prevalence of chronic constipation was 6.9% (95% CI, 6.4–7.4%) in the United States; when we defined constipation by stool frequency, the prevalence of constipation was 3.3% (95% CI, 2.8–3.9%) in the United States. Table 1 and Supplementary Table 2 show the basic characteristics of the population with constipation defined by the Bristol Stool Form Scale and stool frequency, respectively. Table 1 shows that chronic constipation is associated with sex, ethnicity, BMI, education, income-poverty ratio, poor oral health, physical activity, depression, smoking, alcohol consumption, milk consumption, and dietary phosphorus intake (P < 0.05); however, age, hypertension, and diabetes were not related. Results defined using stool consistency were slightly changed from those defined using stool frequency. Only the following differences were observed (Supplementary Table 2): age was shown to be relevant, while BMI and physical activity were found to be irrelevant.

Table 2 presents the prevalence of chronic constipation by definition and sex. The results show that the prevalence of different definitions of chronic constipation differs (6.9%, 95% confidence interval (CI) 6.4, 7.4 for stool consistency vs 3.3%, 9.5% CI 2.8, 3.9 for stool frequency). In constipation defined by stool frequency, the prevalence of chronic constipation varies by sex (5.5%, 95% CI 4.6, 6.5 in women vs 1.1%, 95% CI 0.8, 1.5 in men).

In Figs. 2 and 3, the fitting curve describing the relationship between dietary phosphorus and constipation slopes downward, including a negative relationship between two. We used multiple logistic regression models to further demonstrate this relationship as shown in Table 3, which defined constipation by stool consistency, and Table 4, in which it was defined by stool frequency. The unadjusted model in Table 3 showed that dietary phosphorus intake (every additional 0.1 g) was observably related to constipation, as defined by the Bristol Stool Form Scale (0.94, 0.92–0.96, P < 0.001). Table 4 shows that we obtained a similar result for constipation defined by different bowel movements (0.89, 0.86–0.92, P < 0.001). Model Ⅱ showed that the two were still correlated after adjusting for sex, age, and race (0.97, 0.95–0.98; P < 0.001 for stool consistency vs 0.93, 0.90–0.97, P < 0.001 for stool frequency). Model Ⅲ showed a clear association after adjusting for more confounders (0.97, 0.95–1.00, P = 0.045 for stool consistency vs 0.94, 0.90–0.99, P = 0.034 for stool frequency). In model Ⅲ, the OR (95% CI) for the second to fourth quartiles compared with the reference group were 0.92(0.66, 1.27), 0.73(0.47, 1.13), and 0.39(0.20, 0.76), respectively using the stool frequency definition (Table 4). The prevalence of constipation gradually decreased as the quartile increased (P for trend = 0.012). We found values for the trend test for similar trends in men (P = 0.032 for stool consistency vs P = 0.001 for stool frequency). However, similar results were not observed in the general population defined by stool consistency (P for trend = 0.181), nor in women (P for trend = 0.413 for stool consistency vs P for trend = 0.335 for stool frequency).

To reduce the bias caused by different definitions, we performed sensitivity analysis (Supplementary Table 1) with three other relevant conditions including use of laxatives, self-reported constipation and frequency of laxative use that may affect the prevalence of constipation. Dietary phosphorus intake was not associated with these three conditions.

Rude association of constipation with demography, comorbidity, physical activity, smoking, alcohol consumption, and diet

Supplementary Table 3 for stool consistency and Supplementary Table 4 for stool frequency present the rough associations of constipation with demography, comorbidity, physical activity, smoking, alcohol consumption, and diet. Supplementary Table 3 shows that poor oral health, and depression are each associated with increased constipation, whereas being male, having a higher level of education, a higher income-poverty ratio, larger BMI, higher level of physical activity, hypertension, diabetes, smoking, alcohol consumption, and higher dietary phosphorus intake were associated with decreased constipation. In Supplementary Table 4, we found similar trends, except that now smoking was associated with an increase in constipation, while often milk consumption and higher age were associated with a decrease in constipation.

Stratified analysis of dietary phosphorus and chronic constipation

Supplementary Tables 5 and 6 show the results of stratified analysis of unadjusted variables to define constipation by the Bristol Stool Form Scale and different bowel movements, showing the relationship between the two in different layers. We carried out different layers based on the relevant covariates. The relationship between dietary phosphorus and chronic constipation showed a decreasing trend, despite the application of two different definitions of chronic constipation. In Supplementary Table 5, significant interactions were observed when stratified by hypertension (P = 0.022), smoking (P = 0.028), income-poverty ratio (P = 0.042), and drinking (P = 0.036). In Supplementary Table 6, the interaction was only observed with depression (P = 0.038).

Discussion

We screened data from 2005–2010 in the NHANES database to research whether dietary phosphorus intake was associated with chronic constipation, in people aged 20 years and older. After controlling for other relevant confounding factors, increased dietary phosphorus intake still relieved chronic constipation. The prevalence of chronic constipation defined in this study (6.9%, 95% CI 6.4, 7.4 for stool consistency vs 3.3%, 9.5% CI 2.8, 3.9 for stool frequency) was lower than that defined using the Rome criteria (15.3%, 95% CI 8.1, 24.4, in Rome Ⅰ vs 11.2%, 95% CI 7.9, 14.9, in Rome Ⅱ vs 11.4%, 95% CI, 6.5, 14.9, in Rome Ⅲ vs 10.1%, 95% CI, 8.7, 11.6 in Rome Ⅳ) [17]. In an epidemiological survey study, the prevalence of functional constipation according to Rome Ⅳ was 7.9–8.6% in the UK, US, and Canada[18].

Differences in the prevalence of chronic constipation may be influenced by the definition of constipation, the study population, and the methodology of the survey study. Our definition of chronic constipation was based on stool frequency and consistency, which were derived from the number of bowel movements and the Bristol Stool Form Scale, respectively[19]. In calculating the prevalence of chronic constipation, constipation defined by stool frequency was lower than that defined by stool consistency (3.3%, 9.5% CI 2.8, 3.9 vs 6.9%, 95% CI 6.4, 7.4, respectively). This was similar to what was observed in other studies[12^, 20]. However, defining constipation by combining stool frequency and stool consistency reduces the prevalence of constipation[11^, 20].

Sources of dietary phosphorus include meat, dairy products, and grain products (especially, bread and non-diary snacks and sweets), with grain products being the most abundant dietary source.[21]. Some studies have shown that bread can improve the symptoms of chronic constipation [22^, 23]. Recently, large scale research has shown that the dietary intake of microelement is related to the prevalence of chronic constipation [7^, 11^, 12^, 24]. One previous small case-control study of 46 patients found[25] that in the MCI-196 group, a phosphate binder, serum phosphorus was reduced and gastrointestinal symptoms, such as constipation, were exacerbated. In one study, girls with inflammatory bowel disease (IBD) consumed significantly higher amounts of phosphorus than girls in the control group[26]. Studies showed that the main adverse effect of lanthanum carbonate, an oral phosphate binder, was gastrointestinal and included severe constipation[27–29]. Sodium-phosphate enemas are widely used to treat constipation and are rarely associated with side effects[5]. Nevertheless, few studies have quantified dietary phosphorus intake to look at its association with chronic constipation. Phosphorus is an indispensable part of trace elements and participates in many physiological activities. Constipation is also a common disease that plagues people. Therefore, further studies were proposed to examine the relationship between constipation and phosphorus. The following conditions can lead to a reduction in phosphorus in the body: reduced oral intake, excess loss due to diarrhea, reduced intake due to poor absorption, heavy alcohol consumption, and heavy use of antacids[30].

Our study showed that regardless of the type of chronic constipation, based on this study, the prevalence of chronic constipation gradually decreases with increasing dietary phosphorus intake after adjustment for relevant confounders (0.97, 0.95–1.00 for stool consistency; 0.94, 0.90–0.99 for stool frequency). The negative correlation was evident in all groups without adjustment.

By looking at other cross-sectional studies on chronic constipation, we found some factors that were similar to those reported previously[1]. Overall, we found that several factors were associated with the increased prevalence of constipation using the stool consistency definition, for instance, female sex, lower educational status, lower BMI, low activity levels, poor oral health, no hypertension, depression, no diabetes, never smoking, no alcohol consumption, and lower dietary intake. We found similar trends in constipation defined by stool frequency, differing only for smoking and milk consumption. Although a multitude of articles have been published on the relationship between phosphorus and constipation, the results could not be aggregated due to age group limitations[31^, 32].

Previous studies have found statistical discrepancies in the prevalence of chronic constipation in different sexes. The prevalence of constipation was up to two times higher in women, irrespective of the definition used[31]. One study showed that men had easier bowel movements than women[33]. The results of our study also showed a noticeable difference in the prevalence of chronic constipation between men and women. In chronic constipation defined by stool frequency, women had a much higher prevalence than men (5.5%, 4.6–6.5 in women; 1.1%, 0.8–1.5 in men), and similar results were found in constipation defined by stool consistency (9.6%, 95% CI 8.9, 10.4 in women vs 4.0%, 95% CI 3.3, 4.9 in men). There is currently no clear mechanism to explain the difference in the prevalence of chronic constipation caused by differences in sex, and further research is required to explain this phenomenon[34].

This study has some limitations. First, because it is a cross-sectional study, we could not infer a causal relationship. Therefore, we cannot conclude that an increase in dietary phosphorus reduces the occurrence of chronic constipation. Second, the relevant information of BHQ110, BHQ100, and BHQ080 in the questionnaire only exists for the 2009–2010 cycle. Therefore, for further in-depth research, the sample size should be increased. Third, the Rome diagnostic criteria for chronic constipation cover other content in addition to stool frequency and consistency. Therefore, we performed a sensitivity analysis for constipation symptoms. However, the current findings still cannot determine the real chronic constipation population. Fourth, dietary data were provided by patients through recall and self-statement, and recall bias was prone to occur. Moreover, the participants’ dietary data were only recalled within 24 hours; respondents’ long-term eating habits were not included in the database. Fifth, the conclusion is only applicable to the population of this study and cannot be extrapolated to other populations. This study has some strengths. First, the data compiled in this database is a representative sample of the whole of the United States and contains a large amount of detailed information on participants including diet, lifestyle, disease, demographics, etc. Second, the database is large and representative, which further enhances its applicability. Third, in the different regression models, we adjusted for confounding factors that may have affected the results based on other relevant studies.

In conclusion, decreased prevalence of chronic constipation in the population was associated with increased dietary phosphorus intake. The findings of this study should be verified by more diverse and rigorous studies.

Declarations

Acknowledgments All authors thank the NHANES database for providing data.

Funding This research was not supported by any funds and institutions.

Competing Interests None

Author Contributions Both authors of this study participated in the data extraction and the writing of the paper.

Data Availability All data in this study were obtained from the public database NHANES database.

Ethical Approval NHANES was authorized by the National Center for Health Statistics Ethics Review Board.

Patient and Public Involvement No patient involved.

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