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JNFS 2023, 8(2): 298-305 |
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Naseri K, Saadati S, Pashayee-Khamene F, Hekmatdoost A, Asadzadeh-Aghdaei H, Sobhani S R, et al . Dietary Animal Protein vs. Plant Protein Sources in Relation to the Risk of Biliary Stone: A Case-Control Study. JNFS 2023; 8 (2) :298-305
URL: http://jnfs.ssu.ac.ir/article-1-555-en.html
URL: http://jnfs.ssu.ac.ir/article-1-555-en.html
Kaveh Naseri 
, Saeede Saadati , Fereshteh Pashayee-Khamene , Azita Hekmatdoost , Hamid Asadzadeh-Aghdaei , Seyyed Reza Sobhani , Mohammad Amin Shahrbaf , Komeil Esmaeilinejad , Fatemeh Hosseini-Oskuiee , Amir Sadeghi * , Shima Hadavi , Mohammad Nazari
, Saeede Saadati , Fereshteh Pashayee-Khamene , Azita Hekmatdoost , Hamid Asadzadeh-Aghdaei , Seyyed Reza Sobhani , Mohammad Amin Shahrbaf , Komeil Esmaeilinejad , Fatemeh Hosseini-Oskuiee , Amir Sadeghi * , Shima Hadavi , Mohammad Nazari
Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran
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Introduction
Discussion
In this study, the relationship of nutritional habits, physical activity and protein consumption, and the incidence rate of biliary stones were investigated. Lower rate of physical activity, lower protein intake, fiber intake, and dietary cholesterol were associated with the higher risk of biliary stone. In addition, energy intake, and the rate of type 2 diabetes were higher in the biliary stone patients.
Studies examining the differences between animal protein vs. plant protein intake and biliary stones are conflicting. Primary observational studies including some case-control studies (Misciagna et al., 1999, Pixley and Mann, 1988) and a prospective cohort study have shown total protein intake and biliary stones relationships, but not specific analyses for vegetable versus animal protein (Attili et al., 1998). However, some previous studies have reported that plant-based protein may be more beneficial properties for decreasing the rate of biliary stones. For example, Maclure et al. conducted a prospective cohort of 88,837 women aged 34–59 years. Their analysis was energy-adjusted, but established risk factors were not included as covariates (Maclure et al., 1989). According to their findings, biliary stones were less frequently among normal weight women (BMI < 25 kg/m2) in the highest quintile of vegetable protein intake (≥ 20.5 g/d). In contrast, in a case-control study, Mathew et al. showed no associations between vegetable or animal protein intake and biliary stones (Mathew and Ko, 2015).
It is worth mentioning that, in this study, male case subjects significantly consumed higher amount of animal protein and lower amount of plant protein compared to control subjects, which led to high risk of biliary stones. In general, many studies have reported that women showed higher risk for biliary stone disease than men. However, this increased risk is dependent on many factors such as the number of pregnancies and sex hormones (Novacek, 2006, Sun et al., 2009). Increased biliary cholesterol secretion can be brought about estrogen hormone, leading to super saturation of bile. A possible explanation for this finding of the present study may be that the main reason for higher rate of biliary stone among women is not related to high intake of animal protein. However, increased animal protein consumption can be considered as one of the main risk factors for biliary stone diseased among men.
The results of the present study must be considered in the larger context of several dietary and lifestyle risk factors for biliary stones. For example, the increased risk of biliary stones following animal-based protein may be related to exposures to other animal-based ingredients such as dietary saturated fat and cholesterol that are reflected in an animal-versus vegetable-rich diet. It is known that plant-based diets are associated with the lower intake of dietary triglycerides and cholesterol than animal-based diets (Lander et al., 2016). Cholesterol stones, constituting as high as 80% of all gallstones (Reshetnyak, 2012), occurs when cholesterol formation continually exceeds the solubilizing capacity of bile (Lander et al., 2016). Dietary saturated fatty acids increase cholesterol synthesis (Glatz and Katan, 1993). Therefore, higher intake of animal protein containing higher amount of cholesterol and saturated fats may elevate cholesterol to levels beyond bile solubilization capacity, a known pathogenesis of cholesterol gallstones (Feranchak et al., 2007).
It has been observed that the dietary patterns have an effect on biliary stone formation; in the study of Jessri et al., the rate of biliary stone was significantly lower in the individuals with healthy nutrition in comparison to unhealthy nutrition (Jessri and Rashidkhani, 2015). In addition, in the study of Goktas et al., the rate of biliary stone was significantly higher in patients who consumed liquid oil and did not consume milk (Goktas et al., 2016). Furthermore, Ortega et al. suggested that the prevalence of biliary stone is significantly higher in patients with high energy intake, high intake of fat, low fiber intake, and low rate of physical activity (Ortega et al., 1997). Moreover, in the study of Park et al., the rate of cholesterol biliary stone had a direct association with the high intake of lipid, meat, and fried food (Park et al., 2017). These results indicate the role of dietary pattern in the formation of biliary stone which is in line with the current study.
High animal protein intake significantly increased the biliary stone incidence in male sex in crude model, which remained significant after adjustment for energy intake, physical activity, BMI, history of diabetes, dietary cholesterol, and dietary fiber. However, high plant protein consumption led to significantly reduced rate of biliary stone in men in crude model and after adjustment for energy intake and physical activity.
In clinical investigations, high plasma level of triglyceride and low plasma level of HDL-C are correlated with higher risk of biliary stones (Méndez-Sánchez et al., 2007). In addition, proteins have an effective role in biliary stones prevention by increasing the HDL-C and decreasing triglyceride and body fat (Kritchevsky and Klurfeld, 1983, Parker et al., 2002, Zhang et al., 2005). This effect of proteins has been suggested by many animal studies. Ozban et al. suggested that the proteins in soya bean decrease the cholesterol level and have a negative effect on biliary stones formation (Ozben, 1989); moreover, Kritchevsky et al. demonstrated similar effect of vegetable protein on biliary stone formation (Kritchevsky and Klurfeld, 1983). The effect of plant protein and animal protein are different in the formation of biliary stones (Tsai et al., 2004). The possible reason for this difference may be related to the significant effect of the plant protein on the serum concentration of triglyceride (Anderson et al., 1995). The current study results suggest that the vegetable proteins in men are associated with lower risk of biliary stone compared to animal proteins. These results are aligned with previous studies. Lander et al. suggested that plant proteins are significantly related to lower risk of gallstone disease in post-menopausal female (Lander et al., 2016); moreover, in the study of Tsai et al. the risk of cholecystectomy due to biliary stone was inversely associated with vegetable proteins intake (Tsai et al., 2004).
This study has some limitations. Firstly, we designed a case-control approach which led to the inability to figure out the causal relationship between plant and animal protein consumption and biliary stone disease. Moreover, although family history is an obvious risk factor for biliary stone diseases, we did not collect any information of family history of biliary stone diseases. Moreover, the protein content of the food might be affected by some other factors like food preservation, agriculture conditions, etc. The other limitation of this study is the geographical issue; we evaluated the patients who were in Tehran, the capital of Iran. It will be better to conduct feature study as an epidemiologic evaluation with larger samples.
Despite these limitations, the present study has several strengths; this study was among the few studies to assess the association of protein intake with the risk of biliary stone among Iranian individuals. Previous related studies evaluated just gallstone patients, but this was the first evaluation of biliary stone (gallstone and CBD stone and history of last 6 months cholecystectomy). Furthermore, interview bias was declined, as the data was collected by the same interviewer. To decrease the recall bias that might have occurred regarding the frequency of food consumption and quantification of this questionnaire, all case subjects were recently diagnosed (within 6 months).
Conclusion
These results suggest that dietary habit is associated with biliary stone formation. The consumed type of proteins has a positive or negative effect on the formation of biliary stones. In this study, it was shown that the vegetable protein intake in male can act as a healthy contributor in biliary stone diseases, while the animal protein consumption positively affects biliary stone formation and this can be one of the major risk factors among men compared to women.
Acknowledgment
This study was funded by Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences. The authors thank the participants of this study, without whom this study was impossible.
Authors’ contributions
K. Naseri, F. Pashayee-Khamene, and H. Asadzadeh-Aghdaei designed the research; S.R Sobhani, M.A Shahrbaf, and K. Esmaeilinejad conducted the research; F. Hosseini-Oskuiee and S. Hadavi analyzed the data; A. Hekmatdoost, A. Sadeghi, and M. Nazari wrote the paper. S. Saadati had primary responsibility for final content. All authors read and approved the final manuscript.
Conflicts of interest
The authors declare that they have no conflicts of interest to declare.
References
Anderson JW, Johnstone BM & Cook-Newell ME 1995. Meta-analysis of the effects of soy protein intake on serum lipids. New england journal of medicine. 333 (5): 276-282.
Asghari G, et al. 2012. Reliability, comparative validity and stability of dietary patterns derived from an FFQ in the Tehran Lipid and Glucose Study. British journal of nutrition. 108 (6): 1109-1117.
Attili AF, et al. 1998. Diet and gallstones in Italy: the crossâsectional MICOL results. Hepatology. 27 (6): 1492-1498.
Brighi N, et al. 2018. Biliary stone disease in patients receiving somatostatin analogs for neuroendocrine neoplasms. A retrospective observational study. Digestive and liver disease. 51 (5): 689-694.
Catala I, et al. 2000. Cholesterol crystallization in gall-bladder bile of pigs given cholesterol–β-cyclodextrin-enriched diets with either casein or soyabean concentrate as protein sources. British journal of nutrition. 83 (4): 411-420.
Chen LY, et al. 2012. Metabolic syndrome and gallstone disease. World journal of gastroenterology. 18 (31): 4215-4220.
Cleland C, Ferguson S, Ellis G & Hunter RF 2018. Validity of the International Physical Activity Questionnaire (IPAQ) for assessing moderate-to-vigorous physical activity and sedentary behaviour of older adults in the United Kingdom. BMC medical research methodology. 18 (176): 1-12.
Di Ciaula A & Portincasa P 2018. Recent advances in understanding and managing cholesterol gallstones. F1000Research. 7.
Feranchak AP, Sokol RJ & Suchy F 2007. Medical and nutritional management of cholestasis in infants and children. Liver disease in children. 3: 190-231.
Glatz J & Katan M 1993. Dietary saturated fatty acids increase cholesterol synthesis and fecal steroid excretion in healthy men and women. European journal of clinical investigation. 23 (10): 648-655.
Goktas SB, Manukyan M & Selimen D 2016. Evaluation of Factors Affecting the Type of Gallstone. Indian journal of surgery. 78 (1): 20-26.
Hu FB 2002. Dietary pattern analysis: a new direction in nutritional epidemiology. Current opinion in lipidology. 13 (1): 3-9.
Jessri M & Rashidkhani B 2015. Dietary patterns and risk of gallbladder disease: a hospital-based case-control study in adult women. Journal of health, population and nutrition. 33 (1): 39-49.
Kritchevsky D & Klurfeld DM 1983. Gallstone formation in hamsters: effect of varying animal and vegetable protein levels. American journal of clinical nutrition. 37 (5): 802-804.
Lander EM, et al. 2016. Vegetable protein intake is associated with lower gallbladder disease risk: Findings from the Women's Health Initiative prospective cohort. Preventive medicine. 88: 20-26.
Maclure KM, et al. 1989. Weight, diet, and the risk of symptomatic gallstones in middle-aged women. New England journal of medicine. 321 (9): 563-569.
Mahfouz-Cercone S, Johnson JE & Liepa GU 1984. Effect of dietary animal and vegetable protein on gallstone formation and biliary constituents in the hamster. Lipids. 19 (1): 5-10.
Marschall HU & Einarsson C 2007. Gallstone disease. Journal of internal medicine. 261 (6): 529-542.
Mathew LK & Ko C 2015. Dietary fat and protein intake are not associated with incident biliary sludge and stones during pregnancy. Journal of parenteral and enteral nutrition. 39 (1): 124-128.
Méndez-Sánchez N, Zamora-Valdés D, Chávez-Tapia NC & Uribe M 2007. Role of diet in cholesterol gallstone formation. Clinica chimica acta. 376 (1-2): 1-8.
Misciagna G, et al. 1999. Diet, physical activity, and gallstones-a population-based, case-control study in southern Italy. American journal of clinical nutrition. 69 (1): 120-126.
Novacek G 2006. Gender and gallstone disease. Wiener medizinische wochenschrift. 156 (19): 527-533.
Ortega RM, Fernández-Azuela M, Encinas-Sotillos A, Andres P & Lopez-Sobaler AM 1997. Differences in diet and food habits between patients with gallstones and controls. Journal of the American college of nutrition. 16 (1): 88-95.
Ozben T 1989. Biliary lipid composition and gallstone formation in rabbits fed on soy protein, cholesterol, casein and modified casein. Biochemical journal. 263 (1): 293-296.
Panpimanmas S & Manmee C 2009. Risk factors for gallstone disease in a Thai population. Journal of epidemiology. 19 (3): 116-121.
Park Y, et al. 2017. Association between diet and gallstones of cholesterol and pigment among patients with cholecystectomy: a case-control study in Korea. Journal of health, population and nutrition. 36 (1): 39.
Parker B, Noakes M, Luscombe N & Clifton P 2002. Effect of a high-protein, high–monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes care. 25 (3): 425-430.
Pixley F & Mann J 1988. Dietary factors in the aetiology of gall stones: a case control study. Gut. 29 (11): 1511-1515.
Reshetnyak VI 2012. Concept of the pathogenesis and treatment of cholelithiasis. World journal of hepatology. 4 (2): 18.
Seddighi S, et al. 2018. Evaluation of the Cardiovascular Risk in Patients with Biliary Stones; a Descriptive Cross-Sectional Study. Gastroenterology and hepatology from bed to bench.
Stinton LM & Shaffer EA 2012. Epidemiology of gallbladder disease: cholelithiasis and cancer. Gut and liver. 6 (2): 172-187.
Sun H, et al. 2009. Gender and metabolic differences of gallstone diseases. World journal of gastroenterology. 15 (15): 1886-1891.
Tarantino G, et al. 2017. Surgery in biliary lithiasis: from the traditional "open" approach to laparoscopy and the "rendezvous" technique. Hepatobiliary & pancreatic diseases international. 16 (6): 595-601.
Tomotake H, et al. 2006. High protein buckwheat flour suppresses hypercholesterolemia in rats and gallstone formation in mice by hypercholesterolemic diet and body fat in rats because of its low protein digestibility. Nutrition. 22 (2): 166-173.
Tsai C-J, Leitzmann MF, Willett WC & Giovannucci EL 2004. Dietary protein and the risk of cholecystectomy in a cohort of US women: the Nurses’ Health Study. American journal of epidemiology. 160 (1): 11-18.
Tseng M, et al. 2000. Food intake patterns and gallbladder disease in Mexican Americans. Public health nutrition. 3 (2): 233-243.
Zhang J, et al. 2005. A high unsaturated fat, high protein and low carbohydrate diet during pregnancy and lactation modulates hepatic lipid metabolism in female adult offspring. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 288 (1): R112-R118.
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Dietary Animal Protein vs. Plant Protein Sources in Relation to the Risk of Biliary Stone: A Case-Control Study
Kaveh Naseri; PhD1, Saeede Saadati; MSc1, Fereshteh Pashayee-Khamene; MSc2, Azita Hekmatdoost; PhD2, Hamid Asadzadeh-Aghdaei; MD1, Seyyed Reza Sobhani; PhD3, Mohammad Amin Shahrbaf; MSc1, Komeil Esmaeilinejad; MSc1, Fatemeh Hosseini-Oskuiee; MSc2, Amir Sadeghi; MD*1, Shima Hadavi; MSc4 & Mohammad Nazari; BSc5
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 Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran; 4 Treatment Department of Tehran University of Medical Sciences, Tehran, Iran;
5 Student Research Committee, Shoushtar Faculty of Medical Sciences, Shoushtar, Iran.
5 Student Research Committee, Shoushtar Faculty of Medical Sciences, Shoushtar, Iran.
| ARTICLE INFO | ABSTRACT | |
| ORIGINAL ARTICLE | Background: Dietary intake is one of the modifiable risk factors for biliary stones. In recent studies, plant protein intake is associated with a lower risk of biliary stones in comparison to animal protein intake; however, the results are contradictory. The current study aims to compare the effect of animal protein and plant protein on the formation of biliary stone in one of the gastroenterology and liver disease centers in Iran. Methods: 110 participants who had a history of biliary stone and 230 controls who were normal in terms of biliary diseases and referred to the medical center from November 2017 to October 2018 enrolled in this study. Food frequency questionnaire (FFQ) was used for the nutritional assessment; moreover, demographic and anthropometric data, habitual history and comorbidities were collected. Statistical analysis was conducted by SPSS software. Results: Plant protein consumption was significantly lower (P=0.03) and animal protein intake was significantly higher (P=0.02) among men in case compared to controls. Furthermore, the relationship between biliary stone disease and animal protein intake was significant in crude model for men (OR: 1.03, 95% CI=1.01-1.05). In addition, the risk of biliary stone was significantly lower in patients with higher consumption of plant protein (for women: OR: 0.94, 95% CI=0.89-0.99, for both sexes: OR: 0.96, 95%CI=0.93-0.99). Conclusion: The present study suggested that consumption of animal protein sources increased the risk of biliary stone, and intake of plant protein sources decreased the risk of biliary stone. Keywords: Biliary stone; Plant protein; Animal protein |
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| Article history: Received: 10 Jan 2022 Revised: 16 Mar 2022 Accepted:27 Mar 2022 |
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| *Corresponding author amirsadeghimd@yahoo.com Gastroenterology and Liver Diseases Research Center, Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Postal code: 1115119857 Tel: : +982122432519 |
Introduction
| B |
iliary stones are one of the most common disorders of the biliary system in the world with a 15-20% prevalence rate in western countries (Brighi et al., 2018, Di Ciaula and Portincasa, 2018, Panpimanmas and Manmee, 2009, Seddighi et al., 2018). It is also one of the most common diseases affecting emergency-room patients with epigastric pain, nausea, vomiting, abdominal pain, and loss of appetite (Chen et al., 2012). The pathogenesis of biliary stones is believed to be multifactorial and probably develops from interactions between several genetic and environmental factors such as age, sex, ethnicity, family history, obesity, rapid weight loss, and pregnancy (Marschall and Einarsson, 2007, Tarantino et al., 2017).
One of the modifiable risk factors for biliary stones is nutritional intake (Jessri and Rashidkhani, 2015, Lander et al., 2016, Stinton and Shaffer, 2012). Dietary proteins have an influence on biliary cholesterol density and biliary stone formation (Catala et al., 2000, Tsai et al., 2004, Tseng et al., 2000). Some studies have suggested that plant protein intake is associated with a lower risk of biliary stones in comparison to animal protein intake (Mahfouz-Cercone et al., 1984, Tomotake et al., 2006). In addition, some studies have observed no significant association between protein intake and biliary stones (Attili et al., 1998, Misciagna et al., 1999). Assessing the dietary habit in biliary stones patients can determine the relationship between protein intake and biliary stones incident (Hu, 2002).
The study aims to compare dietary animal protein vs. plant protein sources in relation to the risk of biliary stone.
Materials and Methods
Study design: This case-control study was conducted in Research Institute for Gastroenterology and Liver Diseases of Taleghani hospital (Tehran, Iran) from November 2017 to October 2018. The samples consisted of 110 cases (aged 21-91 years) who had a history of gallstone or common bile duct (CBD) stone confirmed by ultrasonography and/or history of cholecystectomy in a 6-month period before their admission to gastrointestinal disease clinic and after obtaining the consent form to participate in this study. Furthermore, the control group consisted of 230 subjects (aged 23-84 years) who were admitted to the other wards of the hospital for a wide spectrum of diseases, such as orthopedic problems, ear/nose/throat diseases or elective surgeries, and did not have history of dieting and did not have a history of biliary stones. Moreover, the control group was matched to the case group based on age (±5 years) and sex and the number of controls was twice that of the cases.
Data collection: To assess the dietary consumption of samples during 1 year before biliary stone determination in the case group or hospital admission in the control group, a validated food frequency questionnaire (FFQ) was used (Asghari et al., 2012). Researchers asked the participants to explain the frequency of their dietary consumption on a daily, weekly, monthly, or yearly basis. Subsequently, dietary intakes were converted to daily frequency for each group of protein consumption. The data extracted from dietary intakes were analyzed by Nutritionist 4 software. The national food composition tables were used as a reference to analyze food intake.
Demographic data, anthropometric measurements, history of smoking, history of alcohol consumption and comorbidities were collected by a questionnaire. The physical activity questionnaire based on physical activity questionnaire (IPAQ) was used to measure the physical activity of the subjects. The validity and reliability of this questionnaire were previously confirmed (Cleland et al., 2018). Metabolic equivalent of task (MET) scores were calculated via face to face interviews with all eligible participants. One MET is defined as 1 kcal/kg/ hour, equivalent to the energy cost of sitting quietly while consuming 3.5 ml/kg/min of oxygen.
Furthermore, weight measurement was done in a standing position by digital scales (Soehnle®, Berlin, Germany) with an accuracy of 100 g. In addition, height was measured using a tape-meter which fixed to a wall with an accuracy of 0.5 cm. Body mass index (BMI) was calculated by dividing the weight by the square of height in meter.
Ethical considerations: This protocol of study was approved by Research Institute of Gastroenterology and Liver Diseases Ethics Committee (IR.SBMU.RIGLD.REC.1396.159).
Data analysis: Statistical analysis was conducted on the data by using SPSS software version 16 (SPSS Inc., Chicago, Illinois). Baseline characteristics and dietary intakes of the participants were compared between case and control groups by t-test or Mann-Whitney for quantitative variables and Chi-square test for qualitative variables. Logistic regression was used to calculate the odds ratio of biliary stone disease as the dependent variable in relation to the animal and plant protein as independent variables in 4 models: Crude model, model 2 (adjusted for energy intake and physical activity), model 3 (further controlled for BMI and history of diabetes) and, model 4 (additionally adjusted for dietary cholesterol and dietary fiber). The odds ratios of the outcomes were determined with a 95% confidence interval.
Results
Demographics: Baseline characteristics and dietary intakes of the participants are shown based on case and control group in Table 1. Individuals in the case group compared to 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 < 0.05).
Binary analysis of variables: Dietary intake of animal and plant protein base on case and control group for men, women and both sexes are shown in Table 2. Men in the case group compared to men in the control group consumed higher animal protein and lower plant protein (P<0.05). In females, there was no significant difference between case and control groups. When both sexes considered, case group consumed lower plant protein compared to control group (P<0.05).
Logistic regression analysis: Table 3 shows the odds ratios for the biliary stone disease for male, female and both sexes together in four models. In the crude model, there was a significant relationship between biliary stone disease and animal protein intake for males (OR: 1.03, 95% CI=1.01-1.05) and both sexes together (OR: 1.01, 95% CI=1.00 -1.01). In fact, patients with higher consumption of animal protein intake were significantly more likely to have the biliary stone disease. In model 2 (adjusted for energy intake and physical activity), model 3 (further controlled for BMI and history of diabetes), and model 4 (adjusted for dietary cholesterol and dietary fiber), these relationships were significant for males, females, and both sexes.
In the case of the plant protein intake, there was a significant relationship between biliary stone disease and plant protein intake for males in crude model (OR: 0.98, 95% CI=0.96-0.99) and model 2 (OR: 0.96, 95% CI=0.92-0.99). After adjustment for BMI and history of diabetes in model 3 and dietary cholesterol and dietary fiber in model 4, this relationship was not significant. For females and both sexes, although there was no significant relationship in crude and model 2, there was a significant relationship between biliary stone disease and plant protein intake in model 3 and model 4. Individuals with higher consumption of plant protein intake were significantly less likely to have the biliary stone disease (for females: OR: 0.94, 95% CI=0.89-0.99, for both sexes: OR: 0.96, 95% CI=0.93-0.99).
One of the modifiable risk factors for biliary stones is nutritional intake (Jessri and Rashidkhani, 2015, Lander et al., 2016, Stinton and Shaffer, 2012). Dietary proteins have an influence on biliary cholesterol density and biliary stone formation (Catala et al., 2000, Tsai et al., 2004, Tseng et al., 2000). Some studies have suggested that plant protein intake is associated with a lower risk of biliary stones in comparison to animal protein intake (Mahfouz-Cercone et al., 1984, Tomotake et al., 2006). In addition, some studies have observed no significant association between protein intake and biliary stones (Attili et al., 1998, Misciagna et al., 1999). Assessing the dietary habit in biliary stones patients can determine the relationship between protein intake and biliary stones incident (Hu, 2002).
The study aims to compare dietary animal protein vs. plant protein sources in relation to the risk of biliary stone.
Materials and Methods
Study design: This case-control study was conducted in Research Institute for Gastroenterology and Liver Diseases of Taleghani hospital (Tehran, Iran) from November 2017 to October 2018. The samples consisted of 110 cases (aged 21-91 years) who had a history of gallstone or common bile duct (CBD) stone confirmed by ultrasonography and/or history of cholecystectomy in a 6-month period before their admission to gastrointestinal disease clinic and after obtaining the consent form to participate in this study. Furthermore, the control group consisted of 230 subjects (aged 23-84 years) who were admitted to the other wards of the hospital for a wide spectrum of diseases, such as orthopedic problems, ear/nose/throat diseases or elective surgeries, and did not have history of dieting and did not have a history of biliary stones. Moreover, the control group was matched to the case group based on age (±5 years) and sex and the number of controls was twice that of the cases.
Data collection: To assess the dietary consumption of samples during 1 year before biliary stone determination in the case group or hospital admission in the control group, a validated food frequency questionnaire (FFQ) was used (Asghari et al., 2012). Researchers asked the participants to explain the frequency of their dietary consumption on a daily, weekly, monthly, or yearly basis. Subsequently, dietary intakes were converted to daily frequency for each group of protein consumption. The data extracted from dietary intakes were analyzed by Nutritionist 4 software. The national food composition tables were used as a reference to analyze food intake.
Demographic data, anthropometric measurements, history of smoking, history of alcohol consumption and comorbidities were collected by a questionnaire. The physical activity questionnaire based on physical activity questionnaire (IPAQ) was used to measure the physical activity of the subjects. The validity and reliability of this questionnaire were previously confirmed (Cleland et al., 2018). Metabolic equivalent of task (MET) scores were calculated via face to face interviews with all eligible participants. One MET is defined as 1 kcal/kg/ hour, equivalent to the energy cost of sitting quietly while consuming 3.5 ml/kg/min of oxygen.
Furthermore, weight measurement was done in a standing position by digital scales (Soehnle®, Berlin, Germany) with an accuracy of 100 g. In addition, height was measured using a tape-meter which fixed to a wall with an accuracy of 0.5 cm. Body mass index (BMI) was calculated by dividing the weight by the square of height in meter.
Ethical considerations: This protocol of study was approved by Research Institute of Gastroenterology and Liver Diseases Ethics Committee (IR.SBMU.RIGLD.REC.1396.159).
Data analysis: Statistical analysis was conducted on the data by using SPSS software version 16 (SPSS Inc., Chicago, Illinois). Baseline characteristics and dietary intakes of the participants were compared between case and control groups by t-test or Mann-Whitney for quantitative variables and Chi-square test for qualitative variables. Logistic regression was used to calculate the odds ratio of biliary stone disease as the dependent variable in relation to the animal and plant protein as independent variables in 4 models: Crude model, model 2 (adjusted for energy intake and physical activity), model 3 (further controlled for BMI and history of diabetes) and, model 4 (additionally adjusted for dietary cholesterol and dietary fiber). The odds ratios of the outcomes were determined with a 95% confidence interval.
Results
Demographics: Baseline characteristics and dietary intakes of the participants are shown based on case and control group in Table 1. Individuals in the case group compared to 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 < 0.05).
Binary analysis of variables: Dietary intake of animal and plant protein base on case and control group for men, women and both sexes are shown in Table 2. Men in the case group compared to men in the control group consumed higher animal protein and lower plant protein (P<0.05). In females, there was no significant difference between case and control groups. When both sexes considered, case group consumed lower plant protein compared to control group (P<0.05).
Logistic regression analysis: Table 3 shows the odds ratios for the biliary stone disease for male, female and both sexes together in four models. In the crude model, there was a significant relationship between biliary stone disease and animal protein intake for males (OR: 1.03, 95% CI=1.01-1.05) and both sexes together (OR: 1.01, 95% CI=1.00 -1.01). In fact, patients with higher consumption of animal protein intake were significantly more likely to have the biliary stone disease. In model 2 (adjusted for energy intake and physical activity), model 3 (further controlled for BMI and history of diabetes), and model 4 (adjusted for dietary cholesterol and dietary fiber), these relationships were significant for males, females, and both sexes.
In the case of the plant protein intake, there was a significant relationship between biliary stone disease and plant protein intake for males in crude model (OR: 0.98, 95% CI=0.96-0.99) and model 2 (OR: 0.96, 95% CI=0.92-0.99). After adjustment for BMI and history of diabetes in model 3 and dietary cholesterol and dietary fiber in model 4, this relationship was not significant. For females and both sexes, although there was no significant relationship in crude and model 2, there was a significant relationship between biliary stone disease and plant protein intake in model 3 and model 4. Individuals with higher consumption of plant protein intake were significantly less likely to have the biliary stone disease (for females: OR: 0.94, 95% CI=0.89-0.99, for both sexes: OR: 0.96, 95% CI=0.93-0.99).
| Table 1. Baseline characteristics and dietary intakes of study participants based on the patients with biliary stone disease and control group. | |||
| Variables | Cases (n=110) | Controls (n=230) | P-valuea |
| Age (year) | 57.66 ± 16.39b | 56.00 ± 10.64 | 0.072 |
| Body mass index (kg/m2) | 27.04 ± 5.46 | 26.70 ± 4.01 | 0.884 |
| Physical activity (MET) | 29.47 ± 3.33 | 40.00 ± 9.35 | <0.001 |
| Total energy (kcal) | 2448.28 ± 644.49 | 2302.27 ± 577.74 | 0.034 |
| Carbohydrate (% of total energy) | 48.27 ± 8.39 | 49.00 ± 6.67 | 0.079 |
| Fat (% of total energy) | 41.53 ± 9.02 | 40.91 ± 6.97 | 0.682 |
| Protein (% of total energy) | 12.59 ± 2.62 | 13.19 ± 2.12 | 0.004 |
| Dietary cholesterol (mg/d) | 236.99 ± 99.75 | 203.30 ± 89.65 | 0.001 |
| Saturated fat (g/d) | 25.49 ± 8.91 | 24.42 ± 5.76 | 0.142 |
| Monounsaturated fat (g/d) | 29.22 ± 12.69 | 29.74 ± 8.48 | 0.376 |
| Polyunsaturated fat (g/d) | 21.95 ± 9.75 | 22.79 ± 6.67 | 0.201 |
| Dietary fiber (g/d)⨠| 36.08 ± 21.08 | 40.33 ± 11.21 | 0.001 |
| Male | 53 (48.2)c | 129 (56.1) | 0.172 |
| Drank alcohol in past year | 6 (5.2) | 5 (2.2) | 0.190 |
| Diabetes type 2⨠| 18 (16.4) | 20 (8.7) | 0.036 |
| Current smokers | 29 (26.4) | 41 (17.8) | 0.069 |
| a: Student t-test for quantitative variables and Chi-square test for qualitative variables. b: Mean ± SD; c: N (%); Dietary intakes (except total energy) were adjusted for total energy intake. MET: Metabolic equivalent task. | |||
| Table 2. Animal and plant protein dietary intakes of study participants based on the patients with biliary stone disease and control group. | ||||||
| Protein intake protein | Males | P-valuea | Females | P-valuea | ||
| Cases (n=53) | Controls (n=129) | Cases (n=101) | Controls (n=57) | |||
| Animal (g/day) | 52.12 ± 34.84 | 40.37 ± 14.16 | 0.02 | 38.43 ±19.51 | 39.45 ± 14.79 | 0.32 |
| Plant (g/day) | 28.44 ± 36.19 | 38.56 ± 15.39 | 0.03 | 34.01 ± 21.35 | 32.97 ± 12.38 | 0.54 |
| a: Student t-test | ||||||
| Table 3. Odds ratios of biliary stone disease for animal and plant protein intake a | ||||||
| Males | Females | Both sexes | ||||
| Animal protein intake | OR | 95% CI | OR | 95% CI | OR | 95% CI |
| Crude | 1.03* | 1.01- 1.05 | 0.99 | 0.98 - 1.02 | 1.01* | 1.00 - 1.02 |
| Model 2 | 1.04* | 1.01 - 1.08 | 1.04* | 1.01 - 1.08 | 1.03* | 1.01 - 1.06 |
| Model 3 | 1.04* | 1.00 - 1.08 | 1.04* | 1.00 - 1.08 | 1.03* | 1.01 - 1.06 |
| Model 4 | 1.05* | 1.01 - 1.10 | 1.07* | 1.01 - 1.13 | 1.05** | 1.02 -1.08 |
| Plant protein intake | ||||||
| Crude | 0.98* | 0.96 - 0.99 | 1.00 | 0.98 -1.02 | 0.99 | 0.98 -1.01 |
| Model 2 | 0.96* | 0.92 - 0.99 | 0.94* | 0.89 - 0.98 | 0.96* | 0.94 - 0.99 |
| Model 3 | 0.96 | 0.92 - 1.01 | 0.93* | 0.88 - 0.98 | 0.96* | 0.94 - 0.99 |
| Model 4 | 0.96 | 0.92 - 1.01 | 0.94* | 0.89 - 0.99 | 0.96* | 0.93 - 0.99 |
| A: Crude model; B: Model 2, multivariate adjusted for energy intake and physical activity; C: Model 3, further controlled for, BMI and history of diabetes; D: Model 4, additionally adjusted for dietary cholesterol and dietary fiber. Data are presented as the odds ratio (95%CI). (* significant P value<0.05, ** significant P value<0.01) | ||||||
Discussion
In this study, the relationship of nutritional habits, physical activity and protein consumption, and the incidence rate of biliary stones were investigated. Lower rate of physical activity, lower protein intake, fiber intake, and dietary cholesterol were associated with the higher risk of biliary stone. In addition, energy intake, and the rate of type 2 diabetes were higher in the biliary stone patients.
Studies examining the differences between animal protein vs. plant protein intake and biliary stones are conflicting. Primary observational studies including some case-control studies (Misciagna et al., 1999, Pixley and Mann, 1988) and a prospective cohort study have shown total protein intake and biliary stones relationships, but not specific analyses for vegetable versus animal protein (Attili et al., 1998). However, some previous studies have reported that plant-based protein may be more beneficial properties for decreasing the rate of biliary stones. For example, Maclure et al. conducted a prospective cohort of 88,837 women aged 34–59 years. Their analysis was energy-adjusted, but established risk factors were not included as covariates (Maclure et al., 1989). According to their findings, biliary stones were less frequently among normal weight women (BMI < 25 kg/m2) in the highest quintile of vegetable protein intake (≥ 20.5 g/d). In contrast, in a case-control study, Mathew et al. showed no associations between vegetable or animal protein intake and biliary stones (Mathew and Ko, 2015).
It is worth mentioning that, in this study, male case subjects significantly consumed higher amount of animal protein and lower amount of plant protein compared to control subjects, which led to high risk of biliary stones. In general, many studies have reported that women showed higher risk for biliary stone disease than men. However, this increased risk is dependent on many factors such as the number of pregnancies and sex hormones (Novacek, 2006, Sun et al., 2009). Increased biliary cholesterol secretion can be brought about estrogen hormone, leading to super saturation of bile. A possible explanation for this finding of the present study may be that the main reason for higher rate of biliary stone among women is not related to high intake of animal protein. However, increased animal protein consumption can be considered as one of the main risk factors for biliary stone diseased among men.
The results of the present study must be considered in the larger context of several dietary and lifestyle risk factors for biliary stones. For example, the increased risk of biliary stones following animal-based protein may be related to exposures to other animal-based ingredients such as dietary saturated fat and cholesterol that are reflected in an animal-versus vegetable-rich diet. It is known that plant-based diets are associated with the lower intake of dietary triglycerides and cholesterol than animal-based diets (Lander et al., 2016). Cholesterol stones, constituting as high as 80% of all gallstones (Reshetnyak, 2012), occurs when cholesterol formation continually exceeds the solubilizing capacity of bile (Lander et al., 2016). Dietary saturated fatty acids increase cholesterol synthesis (Glatz and Katan, 1993). Therefore, higher intake of animal protein containing higher amount of cholesterol and saturated fats may elevate cholesterol to levels beyond bile solubilization capacity, a known pathogenesis of cholesterol gallstones (Feranchak et al., 2007).
It has been observed that the dietary patterns have an effect on biliary stone formation; in the study of Jessri et al., the rate of biliary stone was significantly lower in the individuals with healthy nutrition in comparison to unhealthy nutrition (Jessri and Rashidkhani, 2015). In addition, in the study of Goktas et al., the rate of biliary stone was significantly higher in patients who consumed liquid oil and did not consume milk (Goktas et al., 2016). Furthermore, Ortega et al. suggested that the prevalence of biliary stone is significantly higher in patients with high energy intake, high intake of fat, low fiber intake, and low rate of physical activity (Ortega et al., 1997). Moreover, in the study of Park et al., the rate of cholesterol biliary stone had a direct association with the high intake of lipid, meat, and fried food (Park et al., 2017). These results indicate the role of dietary pattern in the formation of biliary stone which is in line with the current study.
High animal protein intake significantly increased the biliary stone incidence in male sex in crude model, which remained significant after adjustment for energy intake, physical activity, BMI, history of diabetes, dietary cholesterol, and dietary fiber. However, high plant protein consumption led to significantly reduced rate of biliary stone in men in crude model and after adjustment for energy intake and physical activity.
In clinical investigations, high plasma level of triglyceride and low plasma level of HDL-C are correlated with higher risk of biliary stones (Méndez-Sánchez et al., 2007). In addition, proteins have an effective role in biliary stones prevention by increasing the HDL-C and decreasing triglyceride and body fat (Kritchevsky and Klurfeld, 1983, Parker et al., 2002, Zhang et al., 2005). This effect of proteins has been suggested by many animal studies. Ozban et al. suggested that the proteins in soya bean decrease the cholesterol level and have a negative effect on biliary stones formation (Ozben, 1989); moreover, Kritchevsky et al. demonstrated similar effect of vegetable protein on biliary stone formation (Kritchevsky and Klurfeld, 1983). The effect of plant protein and animal protein are different in the formation of biliary stones (Tsai et al., 2004). The possible reason for this difference may be related to the significant effect of the plant protein on the serum concentration of triglyceride (Anderson et al., 1995). The current study results suggest that the vegetable proteins in men are associated with lower risk of biliary stone compared to animal proteins. These results are aligned with previous studies. Lander et al. suggested that plant proteins are significantly related to lower risk of gallstone disease in post-menopausal female (Lander et al., 2016); moreover, in the study of Tsai et al. the risk of cholecystectomy due to biliary stone was inversely associated with vegetable proteins intake (Tsai et al., 2004).
This study has some limitations. Firstly, we designed a case-control approach which led to the inability to figure out the causal relationship between plant and animal protein consumption and biliary stone disease. Moreover, although family history is an obvious risk factor for biliary stone diseases, we did not collect any information of family history of biliary stone diseases. Moreover, the protein content of the food might be affected by some other factors like food preservation, agriculture conditions, etc. The other limitation of this study is the geographical issue; we evaluated the patients who were in Tehran, the capital of Iran. It will be better to conduct feature study as an epidemiologic evaluation with larger samples.
Despite these limitations, the present study has several strengths; this study was among the few studies to assess the association of protein intake with the risk of biliary stone among Iranian individuals. Previous related studies evaluated just gallstone patients, but this was the first evaluation of biliary stone (gallstone and CBD stone and history of last 6 months cholecystectomy). Furthermore, interview bias was declined, as the data was collected by the same interviewer. To decrease the recall bias that might have occurred regarding the frequency of food consumption and quantification of this questionnaire, all case subjects were recently diagnosed (within 6 months).
Conclusion
These results suggest that dietary habit is associated with biliary stone formation. The consumed type of proteins has a positive or negative effect on the formation of biliary stones. In this study, it was shown that the vegetable protein intake in male can act as a healthy contributor in biliary stone diseases, while the animal protein consumption positively affects biliary stone formation and this can be one of the major risk factors among men compared to women.
Acknowledgment
This study was funded by Research Institute for Gastroenterology and Liver Diseases, Shahid Beheshti University of Medical Sciences. The authors thank the participants of this study, without whom this study was impossible.
Authors’ contributions
K. Naseri, F. Pashayee-Khamene, and H. Asadzadeh-Aghdaei designed the research; S.R Sobhani, M.A Shahrbaf, and K. Esmaeilinejad conducted the research; F. Hosseini-Oskuiee and S. Hadavi analyzed the data; A. Hekmatdoost, A. Sadeghi, and M. Nazari wrote the paper. S. Saadati had primary responsibility for final content. All authors read and approved the final manuscript.
Conflicts of interest
The authors declare that they have no conflicts of interest to declare.
References
Anderson JW, Johnstone BM & Cook-Newell ME 1995. Meta-analysis of the effects of soy protein intake on serum lipids. New england journal of medicine. 333 (5): 276-282.
Asghari G, et al. 2012. Reliability, comparative validity and stability of dietary patterns derived from an FFQ in the Tehran Lipid and Glucose Study. British journal of nutrition. 108 (6): 1109-1117.
Attili AF, et al. 1998. Diet and gallstones in Italy: the crossâsectional MICOL results. Hepatology. 27 (6): 1492-1498.
Brighi N, et al. 2018. Biliary stone disease in patients receiving somatostatin analogs for neuroendocrine neoplasms. A retrospective observational study. Digestive and liver disease. 51 (5): 689-694.
Catala I, et al. 2000. Cholesterol crystallization in gall-bladder bile of pigs given cholesterol–β-cyclodextrin-enriched diets with either casein or soyabean concentrate as protein sources. British journal of nutrition. 83 (4): 411-420.
Chen LY, et al. 2012. Metabolic syndrome and gallstone disease. World journal of gastroenterology. 18 (31): 4215-4220.
Cleland C, Ferguson S, Ellis G & Hunter RF 2018. Validity of the International Physical Activity Questionnaire (IPAQ) for assessing moderate-to-vigorous physical activity and sedentary behaviour of older adults in the United Kingdom. BMC medical research methodology. 18 (176): 1-12.
Di Ciaula A & Portincasa P 2018. Recent advances in understanding and managing cholesterol gallstones. F1000Research. 7.
Feranchak AP, Sokol RJ & Suchy F 2007. Medical and nutritional management of cholestasis in infants and children. Liver disease in children. 3: 190-231.
Glatz J & Katan M 1993. Dietary saturated fatty acids increase cholesterol synthesis and fecal steroid excretion in healthy men and women. European journal of clinical investigation. 23 (10): 648-655.
Goktas SB, Manukyan M & Selimen D 2016. Evaluation of Factors Affecting the Type of Gallstone. Indian journal of surgery. 78 (1): 20-26.
Hu FB 2002. Dietary pattern analysis: a new direction in nutritional epidemiology. Current opinion in lipidology. 13 (1): 3-9.
Jessri M & Rashidkhani B 2015. Dietary patterns and risk of gallbladder disease: a hospital-based case-control study in adult women. Journal of health, population and nutrition. 33 (1): 39-49.
Kritchevsky D & Klurfeld DM 1983. Gallstone formation in hamsters: effect of varying animal and vegetable protein levels. American journal of clinical nutrition. 37 (5): 802-804.
Lander EM, et al. 2016. Vegetable protein intake is associated with lower gallbladder disease risk: Findings from the Women's Health Initiative prospective cohort. Preventive medicine. 88: 20-26.
Maclure KM, et al. 1989. Weight, diet, and the risk of symptomatic gallstones in middle-aged women. New England journal of medicine. 321 (9): 563-569.
Mahfouz-Cercone S, Johnson JE & Liepa GU 1984. Effect of dietary animal and vegetable protein on gallstone formation and biliary constituents in the hamster. Lipids. 19 (1): 5-10.
Marschall HU & Einarsson C 2007. Gallstone disease. Journal of internal medicine. 261 (6): 529-542.
Mathew LK & Ko C 2015. Dietary fat and protein intake are not associated with incident biliary sludge and stones during pregnancy. Journal of parenteral and enteral nutrition. 39 (1): 124-128.
Méndez-Sánchez N, Zamora-Valdés D, Chávez-Tapia NC & Uribe M 2007. Role of diet in cholesterol gallstone formation. Clinica chimica acta. 376 (1-2): 1-8.
Misciagna G, et al. 1999. Diet, physical activity, and gallstones-a population-based, case-control study in southern Italy. American journal of clinical nutrition. 69 (1): 120-126.
Novacek G 2006. Gender and gallstone disease. Wiener medizinische wochenschrift. 156 (19): 527-533.
Ortega RM, Fernández-Azuela M, Encinas-Sotillos A, Andres P & Lopez-Sobaler AM 1997. Differences in diet and food habits between patients with gallstones and controls. Journal of the American college of nutrition. 16 (1): 88-95.
Ozben T 1989. Biliary lipid composition and gallstone formation in rabbits fed on soy protein, cholesterol, casein and modified casein. Biochemical journal. 263 (1): 293-296.
Panpimanmas S & Manmee C 2009. Risk factors for gallstone disease in a Thai population. Journal of epidemiology. 19 (3): 116-121.
Park Y, et al. 2017. Association between diet and gallstones of cholesterol and pigment among patients with cholecystectomy: a case-control study in Korea. Journal of health, population and nutrition. 36 (1): 39.
Parker B, Noakes M, Luscombe N & Clifton P 2002. Effect of a high-protein, high–monounsaturated fat weight loss diet on glycemic control and lipid levels in type 2 diabetes. Diabetes care. 25 (3): 425-430.
Pixley F & Mann J 1988. Dietary factors in the aetiology of gall stones: a case control study. Gut. 29 (11): 1511-1515.
Reshetnyak VI 2012. Concept of the pathogenesis and treatment of cholelithiasis. World journal of hepatology. 4 (2): 18.
Seddighi S, et al. 2018. Evaluation of the Cardiovascular Risk in Patients with Biliary Stones; a Descriptive Cross-Sectional Study. Gastroenterology and hepatology from bed to bench.
Stinton LM & Shaffer EA 2012. Epidemiology of gallbladder disease: cholelithiasis and cancer. Gut and liver. 6 (2): 172-187.
Sun H, et al. 2009. Gender and metabolic differences of gallstone diseases. World journal of gastroenterology. 15 (15): 1886-1891.
Tarantino G, et al. 2017. Surgery in biliary lithiasis: from the traditional "open" approach to laparoscopy and the "rendezvous" technique. Hepatobiliary & pancreatic diseases international. 16 (6): 595-601.
Tomotake H, et al. 2006. High protein buckwheat flour suppresses hypercholesterolemia in rats and gallstone formation in mice by hypercholesterolemic diet and body fat in rats because of its low protein digestibility. Nutrition. 22 (2): 166-173.
Tsai C-J, Leitzmann MF, Willett WC & Giovannucci EL 2004. Dietary protein and the risk of cholecystectomy in a cohort of US women: the Nurses’ Health Study. American journal of epidemiology. 160 (1): 11-18.
Tseng M, et al. 2000. Food intake patterns and gallbladder disease in Mexican Americans. Public health nutrition. 3 (2): 233-243.
Zhang J, et al. 2005. A high unsaturated fat, high protein and low carbohydrate diet during pregnancy and lactation modulates hepatic lipid metabolism in female adult offspring. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 288 (1): R112-R118.
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Received: 2022/01/10 | Published: 2023/05/20 | ePublished: 2023/05/20
Received: 2022/01/10 | Published: 2023/05/20 | ePublished: 2023/05/20
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