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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 13  |  Issue : 1  |  Page : 66

Healthy dietary pattern reduces risk of gallstones: Results of a case-control study in Iran


1 Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
2 Department of Clinical Nutrition and Dietetics, Faculty of Nutrition and Food Technology, National Nutrition and Food Technology, Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran
3 Department of Community Nutrition, National Nutrition and Food Technology Research Institute Faculty of Nutrition Sciences and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, Iran

Date of Submission12-Dec-2019
Date of Acceptance18-May-2020
Date of Web Publication08-Apr-2022

Correspondence Address:
Amir Sadeghi
Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijpvm.IJPVM_455_19

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  Abstract 


Background: Nutrition-related factors have been of great interest as one of risk factors of biliary stones. This study evaluated the association of dietary patterns with biliary stone among Iranians. Methods: This is a hospital-based case-control study, which was conducted in a general hospital in Tehran, Iran. A total of 110 patients with gallstone or common bile duct (CBD) stone confirmed by Ultrasonography within the last 6 months before collecting data were recruited. Controls were age-matched patients admitted to the other wards of the same hospital for a broad spectrum of disorders including traumas and orthopedic conditions, or elective surgeries, or throat/ear/nose disease and had no gallbladder disorders, participated in this study. We used a valid and reliable food frequency questionnaire to assess dietary intakes of participants. Dietary patterns were determined by factor analysis. Results: By design, age was similar in both groups (57.66 ± 16.39 years vs. 56.00 ± 10.64 years in cases and controls, respectively). Two dietary patterns were extracted; “Unhealthy” (high consumption of artificial juice, processed meats, refined grains, sweets and desserts, pickles, snacks, and red meats), and “Healthy” (high consumption of vegetable oils, vegetables, fruits, fish, legumes, and nuts, as well as low consumption of hydrogenated fats and salt). Participants in the highest tertile of “Healthy” dietary pattern were significantly less likely to have the gallstones disease (OR: 0.33, 95% CI = 0.120.89) compared to the reference group (low tertile of “Healthy” dietary pattern) (P = 0.02). Conclusions: High consumption of vegetable oils, vegetables, fruits, fish, legumes, and nuts, as well as low consumption of hydrogenated fats and salt in context of healthy dietary pattern are inversely associated with risk of gallstones.

Keywords: Cholecystectomy, dietary, gallbladder diseases, gallstones, Iran, patterns


How to cite this article:
Naseri K, Saadati S, Asadzadeh-Aghdaei H, Hekmatdoost A, Sadeghi A, Sobhani SR, Abhari K, Bahrami A, Rahimi_Sakak F, Jamshidfar N, Zali M. Healthy dietary pattern reduces risk of gallstones: Results of a case-control study in Iran. Int J Prev Med 2022;13:66

How to cite this URL:
Naseri K, Saadati S, Asadzadeh-Aghdaei H, Hekmatdoost A, Sadeghi A, Sobhani SR, Abhari K, Bahrami A, Rahimi_Sakak F, Jamshidfar N, Zali M. Healthy dietary pattern reduces risk of gallstones: Results of a case-control study in Iran. Int J Prev Med [serial online] 2022 [cited 2022 Oct 3];13:66. Available from: https://www.ijpvmjournal.net/text.asp?2022/13/1/66/342762




  Introduction Top


Gallstones disease is a prevalent health issue among gastrointestinal diseases worldwide,[1],[2],[3],[4] with ~1520% prevalence rate in the western populations.[3],[5] Old age, female gender, ethnicity (Western Caucasian, Native Americans and Hispanics), genetic component and family history, obesity and rapid weight loss, pregnancy, reduced physical activity and history of total parenteral nutrition are known risk factors that closely linked with gallstones formation.[3],[4],[6]

Cholesterol and pigment gallstones are two main types of gallstones. In western countries in contrast to Asian ones, there are higher prevalence of cholesterol gallstones than pigment ones.[7] Saturation of cholesterol in bile and subsequently cholesterol crystallization and gallbladder stasis is associated with cholesterol form development of gall stone,[8] whereas release of β-glucuronidase from bacterial infections triggers the pigment stones formation.[9]

Diet and nutrition related factors have been of great interest as one of risk factors of gallstones.[10] Nutritional epidemiologic studies propose that dietary patterns assessment instead of focusing on a single dietary component can clarify the association between diet and health status more completely[11] because dietary patterns provide a snapshot of dietary habits including the interactions among dietary nutrients. Using a multivariate approach like dietary patterns might reduce concerns about confounding factors and interactions of foods and nutrients. Thus, we designed this study to assess the association between dietary patterns and risk of gallstones.


  Methods Top


Study design

This case-control study was carried out in Taleghani hospital (Tehran, Iran) from November 2017 to October 2018. Case subjects (aged 2191 years) were recruited from patients with gallstone or common bile duct (CBD) stone confirmed by Ultrasonography within the past 6 months before collecting data. Control subjects (aged 2384 years) were patients admitted to the other wards of the same hospital for a broad spectrum of disorders including traumas and orthopedic conditions, or elective surgeries, or throat/ear/nose disease and have no gallbladder disorders, participated in this study. Controls were matched to cases based on age (±5 years) and sex. Overall, after excluding 5 cases whose reported energy intakes were outside the range of ± 3 SD from mean energy intakes of population and those with missing data, 110 cases and 230 controls (n = 340) remained in final analysis. This protocol of study was approved by Research Institute of Gastroenterology and Liver Diseases Ethics Committee (IR.SBMU.RIGLD.REC.1396.159) and a written informed consent was obtained from each individual before the interview.

Dietary assessment

To evaluate the dietary intake of subjects during 1 year before gallstones diagnosis in cases or hospital admission in controls, we used a valid and reproducible semi-quantitative food frequency questionnaire (FFQ).[12] Interviewer asked subjects to clarify the frequency of consumption on a daily, weekly, monthly or yearly for each food item and data from the questionnaire were converted to daily frequency. For calculating daily intake of each food group, intakes of food items within that group was summed. Food items of the questionnaire were categorized into 28 food groups with respect to similarity of their nutrient contents [Table 1].
Table 1: Food groups

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Data collection

Trained interviewer carried out all measurements and filled out the questionnaires, including socio-demographic data, anthropometric measurements, physical activity, comorbidities, smoking status, and consumption of alcohol in last year by face-to-face interview. Physical activity was assessed by interviewer, using a questionnaire that was previously validated and represented as metabolic equivalents hour/day (METs h/d) in which 9 different MET levels were ranged from sleep/rest (0.9 METs) to high intensity physical activities (>6 METs).[13],[14]

Measurement of weight was done, whereas participants standing on digital scales (Soehnle, Berline, Germany) with accuracy of 100g.[15] Height was measured using tape-meter fixed to a wall to the nearest 0.5 cm weight in kg divided by the square of height in meter to calculate body mass index (BMI) [Table 2].
Table 2: Baseline characteristics, biochemical parameters and dietary intakes of study participants based on the patients with biliary stone disease and control group

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Statistical analysis

Statistical analysis was conducted using SPSS software version 16 (SPSS Inc., Chicago, Illinois). Major dietary patterns were determined on 24 food groups using principal components analysis (PCA) with Varimax rotation. By taking relevant criteria into consideration, such as changing process of scree plot, the percentage of attended variance and the ability of the identified factors to be interpreted by two main factors out of 9 factors that had an Eagain value greater than 1, were identified as the major dietary patterns.[16] Each participant's score was obtained based on consumption value and the load factor of 24 different food groups for each of the two major dietary patterns. Individuals were classified based on tertiles of dietary patterns. Baseline characteristics, biochemical parameters, and dietary intakes of study participants between case and control group were compared t-test for quantitative variables and Chi-square test for qualitative variables. Logistic regression was used to calculate the odds ratio of gallstones disease as the dependent variable in relation to the different dietary patterns as independent variables. Physical activity and total energy intake were adjusted in the model. When the first tertile of the dietary patterns was considered as the reference, the odds ratios of the outcomes were determined with 95% confidence interval.


  Results Top


A total of 110 cases and 230 controls (n = 340) remained in final analysis. By design, age was similar in both groups (57.66 ± 16.39 years vs. 56.00 ± 10.64 years in cases and controls, respectively).

Two dietary patterns were determined. “Unhealthy” dietary pattern (high consumption of Artificial juice, Processed meats, Refined grains, Sweets and desserts, Pickles, Snacks, and Red meats) and “Healthy” dietary pattern (high consumption of Vegetable oils, Vegetables, Fruits, Fish, Legumes, and Nuts, as well as low consumption of Hydrogenated fats and salt) were identified after performing the principal components analysis [Table 3]. In total, these two factors explained 18.36% of the total variance.
Table 3: Factor loading matrix for the two dietary patterns identified in the study population

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Baseline characteristics, biochemical parameters, and dietary intakes of study participants were shown based on case and control group [Table 2]. Individuals in the case group as compared with those in the control group were higher in total energy intake and prevalence of type-2 diabetes and lower in physical activity, protein intake, dietary cholesterol, and dietary fiber (P value <0.05).

[Table 4] shows the odds ratios for the gallstones disease for male, female, and both sex together. There was a significant relationship between gallstones disease and “Healthy” dietary pattern when both sexes analyzed together. Participants in the highest tertile of “Healthy” dietary pattern were significantly less likely to have the gallstones disease (OR: 0.33, 95% CI = 0.120.89) compared with the reference group (low tertile of “Healthy” dietary pattern) (P for trend = 0.02). Physical activity and total energy intake were adjusted in the model.
Table 4: Odds ratios of biliary stone disease for dietary patternsa

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  Discussion Top


In the present study, we identified two major dietary patterns named as “healthy” and “unhealthy”. Our results revealed that healthy or prudent dietary pattern with high intake of vegetable oils, vegetables, fruits, fish, legumes, and nuts, as well as low intake of hydrogenated fats and salt, inversely associated with risk of all types of gallstones and this significance after adjusting for total energy intake and physical activity permanently existed. Unhealthy dietary pattern including high intake of artificial juice, processed meats, refined grains, sweets and desserts, pickles, snacks, and red meats appeared to increase the incident cases of gallstones.

Few studies have addressed the association between dietary patterns and risk of gallstones in different populations.[1],[2],[10] In Mexican-American men, a traditional Mexican diet including high consumption of beans, corn tortillas, and chili peppers was associated with reduced prevalence of gallbladder diseases.[10] Jessri et al.[1] reported that among Iranian women, unhealthy dietary pattern including high consumption of high-fat dairy products, solid fats, baked potatoes, red and processed meats, eggs, snacks and refined grains was positively linked with the risk of gallstones. In a study that conducted among Korean population, association between dietary patterns with cholesterol and pigment gallstone has been investigated separately. In this study, increased risk of gallstone was related to dietary pattern consuming pork, beef and fried foods, although there was not any relation between dietary pattern and risk of pigment stone.[2] All of these studies were cross sectional, but they were conducted on different populations with heterogeneous sample sizes. In Mexican-American study, both sexes were evaluated but association of dietary patterns with incidence cases of GBD were considerable only among men.[10] Assessed dietary patterns in Iranian population were among women only, as well.[1] In Korean study,[2] dietary factors evaluated with two types of gallstone distinctly. It is important and considerable to note that results of a large prospective cohort study showed that vegetarian diet did not have any protective association with risk for symptomatic gallstones, but after adjusting for BMI, this association became significant.[17] There are some differences among these dietary patterns but all of them focused on this outcome that unhealthy dietary pattern including fried foods, red and processed meats can raise the risk of gallstones disease.

Other studies reported evidence for protective effect of fruits,[1],[2] vegetables,[2],[18] and vegetable oil[19] against risk of gallbladder disease. Findings from the woman's health initiative prospective cohort showed that vegetable protein consumption inversely associated with risk of gallbladder diseases.[20] As well as, among women aged 48-60 years, intake of fruit and vegetables reduced the risk of cholecystectomy.[21],[22] Magnesium, vitamin C and folate content of fruits and vegetables negatively linked to risk of gall stone.[23],[24],[25]

In our study, healthy dietary pattern contained high amounts of fish and vegetable oils. Some of previous studies have brought attention to n-3 fatty acids as protective factors against gallstones.[1],[2],[26],[27] A major mechanism of this effect attributed to the improvement in cholesterol saturation index (CSI) and nucleation time by n-3 fatty acids, which can prevent cholelithiasis.[28] Moreover, the healthy dietary pattern was high in vegetables, fruits, legumes, and nuts, which are the main sources of fiber. It has been shown that dietary fiber can reduce the absorption of cholesterol, which might reduce the risk of cholelithiasis.[29]

In this study we showed that individuals in case group had significantly lower protein intake and dietary cholesterol. There are some studies that proposed dietary cholesterol[30] and animal protein[31] increase the biliary cholesterol saturation and in this way formed cholesterol gallstones.

The present study had several strengths; this study was among the few studies to evaluate the association of dietary patterns with risk of gallstones conducted among Iranian population. Previous studies in this field assessed just gallstone patients, but this was the first evaluation of biliary stone (gallstone and CBD stone and history of last 6 months cholecystectomy). As well as, data was collected by the same interviewer, so interview bias was diminished. To decrease the recall bias, all case subjects were newly diagnosed (within 6 months).

This study has a few limitations. First, the study population was concentrated in capital city of Iran and we could not assess the other cities with different socioeconomic properties. Second, the sample size was small, which could restrict the statistical power to describe differences in the diet. Third, limitations of the using FFQ (such as measurement errors including under- and/or over –reporting of intakes of certain foods, relying on memory and misclassification error)for assessing dietary intakes should be considered.[12]


  Conclusions Top


In conclusion, high consumption of vegetable oils, vegetables, fruits, fish, legumes, and nuts, as well as low consumption of hydrogenated fats and salt in context of healthy dietary pattern are inversely associated with risk of gallstones among Iranian individuals. These findings need to be confirmed in prospective studies.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Acknowledgments

We would like to acknowledge patients who participated in this research and made it possible, and to the colleagues from Research Institute for Gastroenterology and Liver Diseases and staff of Taleghani Hospital, Shahid Beheshti University of Medical Sciences, who provided insight and expertise that greatly assisted the research.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Jessri M, Rashidkhani B. Dietary patterns and risk of gallbladder disease: A hospital based case control study in adult women. J Health Popul Nutri 2015;33:39-49.  Back to cited text no. 1
    
2.
Park Y, Kim D, Lee JS, Kim YN, Jeong YK, Lee KG, et al. Association between diet and gallstones of cholesterol and pigment among patients with cholecystectomy: A case control study in Korea. J Health Popul Nutr 2017;36:39.  Back to cited text no. 2
    
3.
Brighi N, Lamberti G, Maggio I, Manuzzi L, Ricci C, Casadei R, et al. Biliary stone disease in patients receiving somatostatin analogs for neuroendocrine neoplasms. A retrospective observational study. Dig Liver Dis 2019;51:689-94.  Back to cited text no. 3
    
4.
Yoo EH, Lee SY. The prevalence and risk factors for gallstone disease. Clin Chem Lab Med 2009;47:795-807.  Back to cited text no. 4
    
5.
Di Ciaula A, Portincasa P. Recent advances in understanding and managing cholesterol gallstones. F1000 Res 2018:7. doi: 10.12688/f1000research. 15505.1.   Back to cited text no. 5
    
6.
Saldinger PE, Bellorin Marin O, Natural history of gallstones and asymptomatic gallstones. In Blumgart's Surgery of the Liver, Biliary Tract and Pancreas, 2Vol Set. 6th Edition. 2017.   Back to cited text no. 6
    
7.
Stringer MD, Fraser S, Gordon KC, Sharples K, Windsor JA. Gallstones in New Zealand: Composition, risk factors and ethnic differences. ANZ J Surg 2013;83:575-80.  Back to cited text no. 7
    
8.
Gustafsson U, Sahlin S Einarsson C. Biliary lipid composition in patients with cholesterol and pigment gallstones and gallstone-free subjects: Deoxycholic acid does not contribute to formation of cholesterol gallstones. Eur J Clin Invest 2000;30:1099-106.  Back to cited text no. 8
    
9.
Maki T. Pathogenesis of calcium bilirubinate gallstone: Role of E. coli, beta glucuronidase and coagulation by inorganic ions, polyelectrolytes and agitation. Annl Surg 1966;164:90-100.  Back to cited text no. 9
    
10.
Tseng M, DeVellis RF, Maurer KR, Khare M, Kohlmeier L, Everhart JE, et al. Food intake patterns and gallbladder disease in Mexican Americans. Public Health Nutr 2000;3:233-43.  Back to cited text no. 10
    
11.
Hu FB. Dietary pattern analysis: A new direction in nutritional epidemiology. Curr Opin Lipidol 2002;13:3-9.  Back to cited text no. 11
    
12.
Asghari G, Rezazadeh A, Hosseini Esfahani F, Mehrabi Y, Mirmiran P, Azizi F. Reliability, comparative validity and stability of dietary patterns derived from an FFQ in the Tehran lipid and glucose study. Br J Nutr 2012;108:1109-17.  Back to cited text no. 12
    
13.
Aadahl M, Jorgensen T. Validation of a new self report instrument for measuring physical activity. Med Sci Sports Exerc 2003;35:1196-202.  Back to cited text no. 13
    
14.
Heidari Z, Jalali S, Sedaghat F, Ehteshami M, Rashidkhani B. Dietary patterns and breast cancer risk among Iranian women: A case control study. Eur J Obstet Gynecol Reprod Biol 2018;230:73-8.  Back to cited text no. 14
    
15.
Lee RD, Nieman DC. Nutritional Assessment. 3rd ed.Columbus, OH: McGraw Hill; 2003. p. 165-8.  Back to cited text no. 15
    
16.
Brown J. Choosing the right number of components or factors in PCA and EFA. JALT Testing and Evaluation SIG Newsletter 2009;13.  Back to cited text no. 16
    
17.
McConnell TJ, Appleby PN Key TJ. Vegetarian diet as a risk factor for symptomatic gallstone disease. Eur J Clin Nutr 2017;71:731-5.  Back to cited text no. 17
    
18.
Pastides H, Tzonou A, Trichopoulos D, Katsouyanni K, Trichopoulou A, Kefalogiannis N, et al. A case control study of the relationship between smoking, diet, and gallbladder disease. Arch Inter Med 1990;150:1409-12.  Back to cited text no. 18
    
19.
Everson GT, McKinley C, Kern F. Mechanisms of gallstone formation in women. Effects of exogenous estrogen (Premarin) and dietary cholesterol on hepatic lipid metabolism. J Clin Invest 1991;87:237-46.  Back to cited text no. 19
    
20.
Lander EM, Wertheim BC, Koch SM, Chen Z, Hsu CH, Thomson CA. Vegetable protein intake is associated with lower gallbladder disease risk: Findings from the Women's Health Initiative prospective cohort. Prev Med 2016;88:20-6.  Back to cited text no. 20
    
21.
Nordenvall C, Oskarsson V Wolk A. Fruit and vegetable consumption and risk of cholecystectomy: A prospective cohort study of women and men. Eur J Nutr 2018;57:75-81.  Back to cited text no. 21
    
22.
Worthington HV, Hunt LP, McCloy RF, Maclennan I, Braganza JM. A pilot study of antioxidant intake in patients with cholesterol gallstones. Nutrition 1997;13:118-27.  Back to cited text no. 22
    
23.
Misciagna G, Centonze S, Leoci C, Guerra V, Cisternino AM, Ceo R, et al. Diet, physical activity, and gallstones—A population based, case control study in southern Italy. Am J Clin Nutr 1999;69:120-6.  Back to cited text no. 23
    
24.
Mendez Sanchez N, Gonzalez V, Aguayo P, Sánchez JM, Tanimoto MA, Elizondo J, et al. Fish oil (n 3) polyunsaturated fatty acids beneficially affect biliary cholesterol nucleation time in obese women losing weight. J Nutr 2001;131:2300-3.  Back to cited text no. 24
    
25.
Grundy SM, Mok H. Effects of diets and drugs on biliary cholesterol secretion in man. In Gallstones. Springer; 1979. pp. 283-98.  Back to cited text no. 25
    
26.
Worthington HV, Hunt LP, McCloy RF, Ubbink JB, Braganza JM. Dietary antioxidant lack, impaired hepatic glutathione reserve, and cholesterol gallstones. Clin Chim Acta 2004;349:157-65.  Back to cited text no. 26
    
27.
Tsai CJ, Leitzmann MF, Willett WC, Giovannucci EL. Long term intake of dietary fiber and decreased risk of cholecystectomy in women. Am J Gastroenterol 2004;99:1364-70.  Back to cited text no. 27
    
28.
Jorgensen T, Jorgensen LM. Gallstones and diet in a Danish population. Scand J Gastroenterol 1989;24:821-6.  Back to cited text no. 28
    
29.
Tandon RK, Saraya A, Paul S, Kapur BM. Dietary habits of gallstone patients in Northern India: A case control study. JClinGastroenterol 1996;22:23-7.  Back to cited text no. 29
    
30.
Ortega RM, Fernández Azuela M, Encinas Sotillos A, Andrés P, López Sobaler AM. Differences in diet and food habits between patients with gallstones and controls. JAm Coll Nutr 1997;16:88-95.  Back to cited text no. 30
    
31.
Marcus S, Heaton K. Intestinal transit, deoxycholic acid and the cholesterol saturation of bile three inter related factors. Gut 1986;27:550.  Back to cited text no. 31
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 1], [Table 2], [Table 3], [Table 4]



 

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