Abstract
Backgroundsː
Dietary phytochemical index (DPI) is an inexpensive method for estimating the amounts of phytochemicals in foods. No study has investigated the association between DPI and gallstones disease (GSD). Therefore, we conducted a case-control study in adults to assess the relationship between DPI and the risk of gallstones.
Methods
The study was conducted at the general surgical consultation departments of two major multispecialty hospitals in Baghdad: Al-Yarmook and Al Karama Teaching Hospitals. It involved 250 patients with gallstones and 250 controls. DPI was calculated based on data collected from a 168-item validated food frequency questionnaire. Sociodemographic data, physical activity, and anthropometric measures were determined.
Results
In the initial analysis, the highest tertile of total PI compared to the lowest tertile was found to be associated with a lower risk of galleston (OR and 95% CI = 0.61 (0.41–0.93), p for trend = 0.027). This significant association remained even after adjusting for age and sex, and the odds ratio slightly strengthened. In the final adjusted model, which accounted for additional confounders such as physical activity, BMI, smoking, socioeconomic status (SES), and dietary intake of energy, participants in the highest tertile of total PI still had a lower risk of gallston compared to those in the lowest tertile (OR and 95% CI = 0.51 (0.28–0.90), p for trend = 0.031.
Conclusion
We found evidence of a negative relationship between the dietary phytochemical index and the risk of gallstones, even after accounting for potential confounding variables. As a result, it may be advisable to include more phytochemical-rich foods in dietary approaches aimed at preventing gallstones. However, additional studies are needed to confirm the link between the dietary phytochemical index and gallstone.
Keywords: Dietary phytochemical index, DPI, Gallstone, GSD, Phytochemical
Background
Cholelithiasis, commonly known as gallstones, is a prevalent condition that affects the biliary system and often requires hospitalization [1]. There are three types of gallstones based on their biochemical composition: cholesterol, pigment, and mixed gallstones [2]. The majority of gallstones are made of cholesterol, with the most common type being yellow-gray stones made of crystalline cholesterol monohydrate [1]. Initially, gallstones may be asymptomatic, but once they exceed 8 mm in size, symptoms begin to appear [3]. These stones can block the flow of bile or digestive enzymes, leading to severe, acute pain in the upper right abdomen, along with nausea, vomiting, and inflammation [4]. Gallstones impose a significant financial burden, especially in Western countries, with over 20 million adults in the US between ages 20 and 74 estimated to be affected by this condition [5]. The formation of gallstones is a complex process that varies depending on the type and is believed to be influenced by a combination of genetic, dietary, and environmental factors (high energy intake, high fat intake, simple sugars and saturated fat intake, tobacco,…etc.) [6].
The pathophysiology of gallstone disease (GSD) involves an abundance of free radicals and oxidative stress, which results in an increase in lipid and protein oxidation products and a decrease in antioxidant enzymes and vitamins [7]. Bile elements such as bile acids, cholesterol, and bilirubin can interact with free radicals, leading to oxidative stress [7]. Patients with gallbladder disease often have reduced antioxidant defense mechanisms in both the gallbladder wall and their circulation, which can affect the activity of important enzymes involved in cholesterol and bilirubin metabolism in mucosal cells. This, in turn, impacts the absorption and secretion of bile mucins and glycoproteins in the gallbladder, ultimately increasing the risk of bile saturation and contributing to gallstone formation [8]. Animal models and theoretical considerations suggest that the absence of micronutrient antioxidants and polyphenols in the diet may play a role in the development of gallstones in humans [9]. Many foods contain various antioxidant and polyphenol compounds, and there is evidence from clinical and experimental studies supporting the influence of dietary components in both the induction and prevention of GSD [10].
Research has shown that oxidative stress plays a significant role in the development of gallstones. Gallstone patients have been found to have elevated levels of oxidative stress in the lining of their gallbladders [11]. In the case of cholesterol gallstones, it has been confirmed that free radicals contribute to their formation by altering the composition of bile lipids and proteins. Interestingly, a deficiency of vitamin C can increase the risk of gallstone formation by interfering with free radicals. On the other hand, melatonin can potentially reduce the risk of gallstone formation by counteracting the harmful effects of free radicals [12]. The interaction of reactive oxygen species with bilirubin can cause damage to cells and membranes, as well as pigment polymerization. This can ultimately lead to the formation of pigment gallstones and trigger inflammatory events. Factors like iron or melatonin can respectively increase or decrease the oxidative stress process in the development of these types of gallstones [7].
Sipos et al. [13] established a correlation between free radical reactions, the number of stones, and the severity of cholecystitis. The most well-known antioxidant micronutrients are vitamin E, carotenes, vitamin C, and selenium. One possible explanation for this inverse relationship is that individuals with higher levels of vitamin E experience greater protection against oxidative stress. Another factor could be the emulsification of dietary lipids, including fat-soluble vitamins, by bile acids [14].
McCarty proposed the dietary phytochemical index (DPI) as a way to measure the phytochemical content of diets. Determining this content directly is impractical [15]. The DPI is calculated by determining the percentage of calorie intake that comes from foods rich in phytochemicals [16]. This index serves as an indicator of overall phytochemical content in the diet and can measure diet quality [16]. Previous studies have found links between DPI and various chronic diseases, such as obesity, oxidative stress, hypercholesterolemia, insulin resistance, hypertension, and breast cancer [16–22]. However, despite several reported dietary factors, there is limited information on the association between DPI and gallstone disease. Therefore, we conducted a case-control study in adults to assess the relationship between DPI and the risk of gallstones.
Methods
Study population
The study was conducted at the general surgical consultation departments of two major multispecialty hospitals in Baghdad: Al-Yarmook and Al Karama Teaching Hospitals. These hospitals are tertiary care referral centers that receive patients from Baghdad and the surrounding governorates. The study took place between February 2022 and February 2023. It involved 250 patients with gallstones and 250 controls. The selection criteria for cases included being at least 20 years old, willingness to participate in the study, approval from the patient’s guardian (GSD), and a recent diagnosis of gallstones within the past month. Exclusion criteria consisted of a history of other diseases or intestinal disorders, known autoimmune diseases or cancer, pregnancy or lactation in women, changes in the patient’s medication type or dosage, and unwillingness to continue cooperation.
The control group for this study consisted of patients from other departments of the same two hospitals who matched the age and gender criteria. These subjects underwent an ultrasound to confirm that they did not have any gallbladder disorders or liver problems. Data collection for each pair of cases and controls occurred simultaneously, and all participants provided written informed consent. Participants who completed less than 35 items on the food frequency questionnaire and reported an under- or over-reported daily energy intake were excluded. Specifically, participants with a daily energy intake of less than 800 kcal or more than 4500 kcal were not included in the study. Cases and controls were chosen through a random selection process, ensuring that the selection was unbiased and representative of the broader population.
Physical activity and other variable assessments
Information on age, sex, marital status, socioeconomic status (SES), and current smoking status was obtained using a demographic questionnaire. In the study, we used a Seca scale with an accuracy of 100 g to measure body weight and a Seca stadiometer with an accuracy of 0.5 cm to measure height (Seca Scale Corp., Munich, Germany). We then calculated the body mass index (BMI) by dividing the body weight (in kg) by the square of the height (in m). To assess the physical activity levels of the participants, we conducted interviews using the short form of the International Physical Activity Questionnaire, and the results were expressed as metabolic equivalent hours per week [23].
Dietary assessment
In the study, we used a 168-item unmodified semi-quantitative food frequency questionnaire (FFQ) to assess dietary intake [24]. Participants were requested to indicate their typical dietary consumption over the past year by selecting one of the following options: never or less than once a month, 3–4 times a month, once a week, 2–4 times a week, 5–6 times a week, once daily, 2–3 times daily, 4–5 times daily, and 6 or more times daily. The portion sizes for each food item were converted into grams using standard household measurements. Subsequently, the frequencies of food consumption were adjusted to reflect daily intakes. The nutrient profiles of all food items were obtained through the use of modified Nutritionist IV software [25].
Phytochemical Index calculation
The Phytochemical Index (PI) was calculated using McCarty’s method. PI is determined by dividing the daily energy obtained from foods rich in phytochemicals (in kilocalories) by the total daily energy intake (in kilocalories), and then multiplying by 100. The food items considered for this calculation include fruits, vegetables (excluding potatoes), legumes (including soy), whole grains, nuts, olives, and olive oil. Natural fruit and vegetable juices, as well as tomato sauces, were also included in the fruit and vegetable categories due to their high phytochemical content. In addition, the PI of each food component (fruits, vegetables, legumes, whole grains, nuts, olives) was determined by dividing the energy intake from each component by the total energy consumption [15, 16].
 |
Statistical analysis
Statistical analysis was conducted using Statistical Package Software for Social Science, version 21 (SPSS Inc., Chicago, IL, USA), and p-values < 0.05 were considered statistically significant. We assessed the normality of variables through the utilization of the Kolmogorov-Smirnov test and histogram chart. For quantitative variables, we expressed the baseline characteristics and dietary intakes as mean ± SD or median (25–75 interquartile range), while for qualitative variables, we presented numbers and percentages. In order to examine the disparities between cases and controls in terms of continuous and categorical variables, we employed the independent sample t-test and chi-square test, respectively. The participants were categorized into tertiles based on the total PI and its components. Across the tertiles of total PI, we provided a comprehensive overview of the general and dietary data, and assessed the trend of continuous and categorical variables using linear regression and chi-square test. To evaluate the association between gallstone odds and both the total PI and its components, we utilized logistic regression.
Results
The characteristics of control and case participants are presented in Table 1. The age and BMI of the participants were reported as mean ± SD. The average age in the case group was 37.6 ± 7.2 years, while in the control group it was 38.3 ± 7.8 years. Additionally, the average BMI in the case group was 27.31 ± 5.1 Kg/m2, compared to 26.84 ± 4.7 Kg/m2 in the control group. In terms of BMI, gallstone patients had a higher value compared to the controls. However, there were no significant differences in age and gender distribution between the two groups. The total PI for.
Table 1.
Characteristics of control and gallstone patient*
| Variables | Controls (n = 250) (mean ± SD) |
Cases (n = 250) (mean ± SD) |
P-Value† |
|---|---|---|---|
| Age (year) | 38.3 ± 7.8 | 37.6 ± 7.2 | 0.124 |
| Weight(Kg) | 72.37 ± 13.27 | 74.75 ± 18.16 | 0.095 |
| BMI(Kg/m2) | 26.84 ± 4.7 | 27.31 ± 5.1 | 0.178 |
| Total PI | 18.1 ± 7.8 | 16.6 ± 8.2 | 0.088 |
| Physical activity (MET) | 34.37 ± 9.14 | 32.91 ± 3.24 | 0.341 |
| Sex, n (%) | 0.97 | ||
| male | 121(48.4%) | 119 (47.9%) | |
| female | 129(51.6%) | 131 (53.1%) | |
| Smoking, n (%) | 0.62 | ||
| No | 232(92.8%) | 223(88.9%) | |
| yes | 18(7.2%) | 27(11.1%) | |
| Carbohydrate (% of energy) | 57.1 ± 6.7 | 57.3 ± 6.9 | 0.654 |
| Protein (% of energy) | 13.7 ± 2.2 | 13.6 ± 2.1 | 0.741 |
| Fat (% of energy) | 31.8 ± 6.6 | 32.1 ± 7.2 | 0.810 |
| Fiber (g/1000 Kcal) | 15.7 ± 6.4 | 16.5 ± 8.1 | 0.141 |
| Whole grains (g/day) | 64.0 (30.7–115.3) | 53.8 (25.1–112.8) | 0.652 |
| Refined grains (g/day) | 313 ± 151 | 332 ± 189 | 0.084 |
| High fat dairy products (g/d) | 82.6 ± 7.2 | 91 ± 8.1 | 0.213 |
| Fruits (g/day) | 316 ± 217 | 325 ± 226 | 0.578 |
| Vegetables (g/day) | 298 ± 142 | 261 ± 130 | 0.091 |
| Nuts and legume (g/d) | 19.6 (9.1–26.7) | 18.8 (8.9–28.5) | 0.472 |
| Olive(g/d) | 0.67 (0.18–1.96) | 0.82 (0.26–2.23) | 0.094 |
BMI, body mass index; PI, phytochemical index; MET, metabolic equivalent task
*All values are mean ± SD, † independent t-test was used for continuous variables and Chi-squared test for categorical variables
P-value ≤ 0.05 was considered significant
gallstone patients and controls had mean ± SD values of 16.6 ± 8.2 and 18.1 ± 7.8, respectively.
Table 2 presents the baseline characteristics of the study population, organized according to tertiles of total PI. Results showed that age and dietary intake of protein, carbohydrate, fiber, and total PI increased significantly (P < 0.05) across tertiles of total PI. Conversely, the intake of fat decreased significantly (P < 0.05). No significant differences were found among tertiles of total PI for other covariates (all P for trend > 0.05).
Table 2.
Characteristics and dietary intakes across tertiles of dietary phytochemical index among the study participants
| Tertiles of dietary PI | |||||
|---|---|---|---|---|---|
| T1(n = 167) | T2(n = 167) | T3(n = 166) | P-trend* | ||
| Demographic variables | |||||
| Age(year) | 37.2 ± 7.6 | 38.3 ± 7.5 | 39.1 ± 8.2 | 0.063 | |
| Male, n (%) | 79 (47.4) | 82 (49.5) | 75 (45.3) | 0.412 | |
| BMI(Kg/m2) | 27.1 ± 4.1 | 26.7 ± 4.4 | 26.8 ± 4.4 | 0.512 | |
| Smoking, n (%) | 17 (10.1) | 16 (9.5) | 12 (7.2) | 0.274 | |
| Physical activity (MET/min/week) | 1451 ± 804 | 1469 ± 823 | 1391 ± 846 | 0.415 | |
| socioeconomic status (SES), n (%) | 0.872 | ||||
| Low | 62 (37.3) | 53 (31.6) | 55 (33.1) | ||
| Middle | 69 (41.4) | 72 (43.2) | 79 (47.7) | ||
| High | 36 (21.3) | 42 (25.2) | 32 (19.2) | ||
| Dietary intake | |||||
| Energy intake (Kcal/d) | 2261 ± 602 | 2287 ± 625 | 2321 ± 641 | 0.411 | |
| Carbohydrate (% of energy) | 50.7 ± 7.1 | 57.2 ± 6.3 | 59.3 ± 6.4 | < 0.001 | |
| protein (% of energy) | 12.8 ± 2.2 | 13.1 ± 1.9 | 13.9 ± 2.3 | < 0.001 | |
| fat (% of energy) | 33.6 ± 7.8 | 31.3 ± 6.1 | 29.3 ± 5.5 | < 0.001 | |
| Fibre (g/1000 Kcal) | 14.9 ± 7.8 | 16.5 ± 6.4 | 17.7 ± 6.2 | < 0.001 | |
| Total PI | < 0.001 | ||||
| PI components | |||||
| Vegetable PI | 2.6 ± 1.3 | 3.3 ± 1.6 | 3.4 ± 1.6 | < 0.001 | |
| Fruit PI | 2.9 ± 1.5 | 5.1 ± 3.0 | 7.2 ± 4.6 | < 0.001 | |
| Whole grain PI | 2.3 ± 1.6 | 5.2 ± 3.2 | 12.9 ± 8.9 | < 0.001 | |
| Legume PI | 0.5 (0.3–1.0) | 0.7 (0.4–1.3) | 0.8 (0.4–2.1) | < 0.001 | |
| Nuts PI | 0.3 (0.1–0.7) | 0.4 (0.1–1.1) | 0.7 (0.3–1.5) | < 0.001 | |
| Olives | 0.06 (0.00–0.21) | 0.14 (0.02–0.49) | 0.14 (0.02–0.56) | 0.027 | |
P-value ≤ 0.05 was considered significant
* P- Values were determined using linear regression and the chi-square test for continuous and categorical variables
Table 3 illustrates the dietary intake of different food groups in tertiles of total PI. Across tertiles of total PI, there was a significant increase (P < 0.05) in the consumption of vegetables, fruits, whole grains, nuts, legumes, and olives. In contrast, there was a significant decline (P < 0.05) in the consumption of refined grains, high-fat dairy products, as well as red and processed meat.
Table 3.
Dietary food groups across tertiles of phytochemical index among the study participants
| Tertiles of dietary phytochemical index | ||||
|---|---|---|---|---|
| Food groups | T1(n = 167) | T2(n = 167) | T3(n = 166) | p-value* |
| Fruits(g/day) | 221 ± 132 | 311 ± 214 | 404 ± 227 | < 0.001 |
| Vegetables(g/day) | 241 ± 127 | 291 ± 124 | 307 ± 142 | 0.012 |
| Nuts and legume (g/d) | 16.1 ± 12.6 | 22.1 ± 15.8 | 29.2 ± 24.1 | < 0.001 |
| Refined grains (g/day) | 387 ± 181 | 327 ± 127 | 258 ± 139 | 0.007 |
| Whole grains (g/day) | 22.7 ± 17.5 | 45.3 ± 33.7 | 101.0 ± 73.2 | < 0.001 |
| High fat dairy products (g/d) | 169 ± 154 | 151 ± 135 | 137 ± 118 | < 0.001 |
| Red and process meat(g/day) | 24.1 ± 19.3 | 22.7 ± 19.2 | 19.4 ± 15.2 | 0.003 |
| Olive(g/d) | 0.52 (0.05–1.57) | 0.97 (0.16–2.81) | 0.97 (0.20–3.02) | < 0.001 |
P-value ≤ 0.05 was considered significant
* P- Values were determined using logistic regression
The association of total PI and gallstone is presented in Table 4. In the initial analysis, the highest tertile of total PI compared to the lowest tertile was found to be associated with a lower risk of galleston (OR and 95% CI = 0.61 (0.41–0.93), p for trend = 0.027). This significant association remained even after adjusting for age and sex, and the odds ratio slightly strengthened. In the final adjusted model, which accounted for additional confounders such as physical activity, BMI, smoking, socioeconomic status (SES), and dietary intake of energy, participants in the highest tertile of total PI still had a lower risk of gallston compared to those in the lowest tertile (OR and 95% CI = 0.51 (0.28–0.90), p for trend = 0.031).
Table 4.
Odds ratios (ORs) and 95% confidence intervals (CIs) for gallstone based on tertiles dietary phytochemical index
| Tertiles of dietary phytochemical index | ||||
|---|---|---|---|---|
| T1 | T2 | T3 | P for trend | |
| phytochemical index(median) | 10.12 | 15.34 | 25.61 | |
| gallstone /Total | 93 / 167 | 81 / 167 | 76 / 166 | |
| Crude model | 1.00 (Ref) | 0.75(0.49–1.09) | 0.61 (0.41–0.93) | 0.027 |
| Model 1* | 1.00 (Ref) | 0.69 (0.44–1.04) | 0.58 (0.40–0.89) | 0.018 |
| Model 2 † | 1.00 (Ref) | 0.78 (0.50–1.35) | 0.51 (0.28–0.90) | 0.031 |
| Model 3^ | 1.00 (Ref) | 0.82 (0.59–1.12) | 0.63 (0.43–0.91) | 0.039 |
*Model 1: adjusted for age and sex
†Model 2: Additionally, adjusted for physical activity, smoking, BMI, SES, dietary intake of energy
^ Model 3: Additionally, adjusted for sugar, vegetable oil and/or olive oil, fast food, fish, total fat
P- Values were determined using logistic regression
Discussion
This case-control study suggested that, a higher PI score is associated with a reduced odds of gallstone. Moreover, the consumption of vegetables, fruits, whole grains, nuts, legumes, and olives significantly increased across the tertiles of total PI.
Several studies have found that the phytochemical index (PI) is associated with better health status and a lower risk of various chronic diseases. These diseases include non-alcoholic fatty liver disease [16], oxidative stress [26], obesity [27], hypertension [22], hypertriglyceridemia [20], and insulin resistance [18].
In a case-control study, Salehi-sahlabadi et al. demonstrated that a higher PI score is linked to a lower risk of non-alcoholic fatty liver disease (NAFLD) [16]. A study conducted by Castro-Torres et al. demonstrated that the black radish (Raphanus sativus L. var niger), known for its medicinal properties, is a valuable source of phytochemicals. In Mexican traditional medicine, it is commonly used to treat gallstones. Research has proven that the juice of black radish can effectively lower cholesterol levels in the bloodstream and dissolve gallstones in mice. The primary compounds found in black radish, known as glucosinolates, can convert into isothiocyanates, which possess antioxidant properties and can reduce cholesterol levels in the liver. These therapeutic effects are beneficial in preventing the formation of cholesterol gallstones, which is a significant health concern [28].
A study conducted by Vincent et al. showed that the PI is negatively associated with adiposity and oxidative stress in healthy young adults. It is also responsive to changes in body weight. This straightforward index could be valuable as a target for consuming nutrient-rich foods in weight reduction or management programs [29].
Previous studies have investigated the relationship between phytochemical-rich foods (such as fruits, vegetables, whole grains, and nuts) and the risk of developing gallstones. In a case-control study conducted by Neshatbini et al., it was found that a higher intake of dietary fiber was significantly linked to a lower risk of gallstone disease [30]. Similarly, Chung-Jyi Tsai et al. suggested that consuming nuts is associated with a reduced risk of developing gallstones [31]. Furthermore, a systematic review and meta-analysis demonstrated that the consumption of vegetables and fruits is significantly associated with a decreased risk of gallstone disease [32].
Regarding the sources of PI, individuals in the highest tertile consumed more fruits, vegetables, whole grains, nuts, and olives compared to those in the lowest tertile. Furthermore, they consumed fewer refined grains, high-fat dairy products, and red and processed meat. Therefore, increasing the consumption of phytochemical-rich foods is likely to have beneficial effects in preventing gallstones. In the past decade, several studies have examined the effects of healthy dietary patterns on gallstones. These patterns are characterized by adequate intake of vegetables, fruits, legumes, fish, and nuts, as well as low consumption of hydrogenated fats and salt. These patterns have demonstrated protective effects against gallstones. On the other hand, western dietary patterns, which involve a high intake of processed meat, alcohol, high-fat dairy, hydrogenated fats, and salt, increase the risk of gallstones [33–35].
Our study had several strengths. Firstly, it was the first study to investigate the association between dietary PI and the odds of gallstones. Additionally, we also examined the association of each PI component with the risk of gallstones for the first time. Lastly, the use of trained dieticians conducting face-to-face interviews to collect dietary intake data helped to minimize measurement bias.
There were several limitations in our study. First, the case-control study design prevented us from determining cause-and-effect relationships. Second, there may have been measurement error when participants recalled their dietary intake, despite using a validated semi-quantitative FFQ. Additionally, although we adjusted for several potential confounding variables, our study design could not fully eliminate all possible confounding effects. Therefore, there may still be residual confounding variables that could have influenced our results.
Conclusions
We found evidence of a negative relationship between the dietary phytochemical index and the risk of gallstones, even after accounting for potential confounding variables. As a result, it may be advisable to include more phytochemical-rich foods in dietary approaches aimed at preventing gallstones. However, additional studies are needed to confirm the link between the dietary phytochemical index and gallstone.
Acknowledgements
The researchers express their gratitude towards all the individuals who volunteered to take part in the study.
Author contributions
MA and GL conceptualized and designed the study. GL and HM analyzed and interpreted the data. AH, HM, and IH drafted the initial manuscript. M.A. supervised the project. All authors read and approved the final manuscript.MA and GL conceptualized and designed the study. GL and HM analyzed and interpreted the data. AH, HM, and IH drafted the initial manuscript. M.A. supervised the project. All authors read and approved the final manuscript.
Funding
This research received no external funding.
Data availability
Upon reasonable request, the corresponding author can provide the datasets that were produced and analyzed during the current study.Upon reasonable request, the corresponding author can provide the datasets that were produced and analyzed during the current study.
Declarations
Ethics approval and consent to participate
This study was performed in line with the principles of the Declaration of Helsinki. Informed consent was obtained from all participants or their legal guardians. Approval was granted by the ethics committee of College of Science, Mustansiriyah University (Approval number: MEDICINE.MU.12.147).
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors declared no conflicts of interest.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Upon reasonable request, the corresponding author can provide the datasets that were produced and analyzed during the current study.Upon reasonable request, the corresponding author can provide the datasets that were produced and analyzed during the current study.