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Cholecystectomy As a Risk Factor of Metabolic Syndrome: from Epidemiologic Clues to Biochemical Mechanisms Yongsheng Chen, Shuodong Wu and Yu Tian

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Cholecystectomy As a Risk Factor of Metabolic Syndrome: from Epidemiologic Clues to Biochemical Mechanisms Yongsheng Chen, Shuodong Wu and Yu Tian Laboratory Investigation (2018) 98, 7–14 © 2018 USCAP, Inc All rights reserved 0023-6837/18 $32.00 PATHOBIOLOGY IN FOCUS Cholecystectomy as a risk factor of metabolic syndrome: from epidemiologic clues to biochemical mechanisms Yongsheng Chen, Shuodong Wu and Yu Tian Cholecystectomy has long been regarded as a safe procedure with no deleterious influence on the body. However, recent studies provide clues that link cholecystectomy to a high risk for metabolic syndrome (MetS). In the present review, we describe the epidemiologic evidence that links cholecystectomy to MetS. Various components of MetS are investigated, including visceral obesity, dyslipidemia, elevated blood pressure, impaired fasting glucose, and insulin resistance. The possible mechanisms that associate cholecystectomy with MetS are discussed on the basis of experimental studies. Laboratory Investigation (2018) 98, 7–14; doi:10.1038/labinvest.2017.95; published online 11 September 2017 Gallstone disease is one of the most common biliary tract abnormalities among cholecystectomized patients, combined diseases in which both environmental and genetic factors have with the lack of data regarding metabolic changes that occur roles in its pathogenesis. Biliary cholesterol supersaturation after GB removal, has caused cholecystectomies to receive from metabolic defects in the liver and the subsequent increased scrutiny. As the roles of the GB and BAs in systemic physical–chemical imbalance of cholesterol solubility in bile metabolic regulation have become better understood,8–10 it is are thought to be the main cause of gallstone formation.1 important to re-examine the potential long-term negative Factors such as physical inactivity, obesity, and overnutrition outcomes of GB removal, and especially the associated risk for increase the risk of developing gallstones and form the basis of subsequent metabolic syndrome (MetS). In the present primary prevention by lifestyle changes.2 Although treatment review, we describe the epidemiologic evidence that links of asymptomatic gallstone patients is not routinely recom- cholecystectomy to MetS, and discuss some possible mechan- mended, current treatment algorithms for symptomatic isms for this linkage based on results of experimental studies. gallstone patients, by contrast, remain predominantly invasive and are based on surgery.3 Cholecystectomy is the best and most cost-effective treat- METABOLIC SYNDROME ment for gallstone disease, and one of the most commonly MetS refers to a constellation of metabolic disorders that performed operations worldwide. The short- and long-term include central obesity, dyslipidemia (raised triglycerides outcomes of cholecystectomy are excellent, and the surgical (TGs) and lowered high-density lipoprotein cholesterol), procedure has minimal rates of mortality and morbidity. It is raised blood pressure, and raised fasting glucose, and can be also accepted that gallbladder (GB) removal is a relatively diagnosed when any three of the above five components are 11 innocuous procedure with no deleterious influence on bile present (Table 1). The prevalence of MetS has increased acid (BA) metabolism or overall metabolic regulation. Follow- over time, and data gathered by the National Health and ing surgery, the size of the BA pool remains within a normal Nutrition Examination Survey (NHANES) indicate that range and dietary fat absorption remains unaffected.4,5 ~ 20% of the adult US population is currently affected by However, there is emerging evidence showing that MetS.12 In addition, there is a high prevalence of MetS and its cholecystectomy itself may lead to an excessive risk for the individual components in developing countries.13,14 It is surgical patient developing metabolic disorders and their notable that MetS adversely affects the health of increasing associated complications, including dyslipidemia, non- numbers of adolescents, as ~ 50% of them display at least one alcoholic fatty liver disease (NAFLD), and hyperglycemia.5–7 of its components.15 Because MetS directly promotes the The unexplained high incidence of these metabolic development of cardiovascular diseases, type 2 diabetes Department of General Surgery, Shengjing Hospital of China Medical University, Shenyang, China Correspondence: Dr Y Tian, MD, PhD, Department of General Surgery, Shengjing Hospital of China Medical University, No. 36, San Hao Street, Heping District, Shenyang, Liaoning 110004, China. E-mail: [email protected] Received 1 February 2017; revised 3 July 2017; accepted 9 July 2017 www.laboratoryinvestigation.org | Laboratory Investigation | Volume 98 January 2018 7 Cholecystectomy and MetS PATHOBIOLOGY IN FOCUS Y Chen et al Table 1 Criteria for diagnosis of metabolic syndrome Measure Categorical cutpoints Waist circumference Population- and country-specific definitions Triglycerides Triglycerides ≥ 150 mg/dl or drug treatment for elevated triglycerides High-density lipoprotein cholesterol (HDL-c) HDL-C o40 mg/dl in men or o50 mg/dl in women or drug treatment for reduced HDL-C Blood pressure Systolic BP ≥ 130 mm Hg, diastolic BP ≥ 85 mm Hg or antihypertensive drug treatment in a patient with history of hypertension Fasting glucose ≥ 100 mg/dl or drug treatment for elevated glucose Source: 2009 Joint Interim Statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity.11 mellitus (T2DM), stroke, and chronic kidney disease,16–18 it there was no significant difference in weight gain between has become a major public-health challenge worldwide.19,20 patients who remained on their preoperative low-fat diet and Despite years of investigation, the cause of MetS remains those who did not, with the former group showing an obscure. However, several risk factors are probably involved, increase of 2 kg/m2 in their mean BMI.30 Obesity increases the with visceral obesity and insulin resistance being the most likelihood of developing various diseases, including hyperten- important.21,22 An association between gallstone disease and sion, coronary heart disease, fatty liver disease, and T2DM. MetS was first reported by Mendez-Sanchez et al in 2005,23 Further increases in BMI can adversely affect the long term and their findings were confirmed by two other large sample health of these patients, because many of them are overweight studies.24,25 Moreover, patients with complicated gallstone prior to surgery. diseases, which often require cholecystectomy, are more likely In an attempt to investigate the effect of cholecystectomy to have MetS than those with uncomplicated gallstone on hepatic lipid metabolism, Amigo et al.5 reported signifi- disease.26 In a cross-sectional study, Shen et al. analyzed data cant increases in serum and hepatic TG concentrations, from 5672 subjects, and found that the prevalence of MetS hepatic very-low-density lipoprotein (VLDL)–TG levels, and was 53.2% among the subjects with gallstone disease and apoB-48 production in mice 2 months after cholecystectomy 63.5% among cholecystectomized subjects.27 These findings surgery. Interestingly, those mice also displayed an altered suggest that cholecystectomy by itself may be a risk factor rhythm of changes in their hepatic TG concentrations when for MetS. compared with sham-operated animals, by having higher TG concentrations at the beginning of the light phase of each CHOLECYSTECTOMY AND MetS COMPONENTS diurnal cycle, and then maintaining those high concentrations Numerous epidemiological studies have linked gallstones and throughout the day. Consistent with findings in mice, signifi- cholecystectomy to MetS. However, when compared with cant increases in VDLD–apoprotein B (VLDL–apoB) and gallstones, cholecystectomy is usually more closely, if not intermediate-density lipoprotein apoprotein B concentrations solely, associated with each of the MetS components when the were noticed in patients 3 years after cholecystectomy.32 In two conditions are studied separately. another case–control study, patients who underwent chole- An earlier study28 reported a significant weight gain among cystectomy had higher levels of plasma TGs, as well as higher cholecystectomized patients, with men and women gaining a levels of total and low-density lipoprotein cholesterol, but mean of 4.6% and 3.3%, respectively, of their preoperative lower levels of high-density lipoprotein cholesterol than control body weight at 6months after surgery. Other studies27,29 that subjects without GB disease or who had not undergone compared subjects with and without gallstones reported that, cholecystectomy33 (Table 2). These observations support a when compared with subjects without gallstones, the body still unknown role for the GB in regulating systemic lipid mass index (BMI) and waist circumference of subjects with metabolism, and suggest that GB removal may somehow gallstones tended to be higher, and these differences were result in a deranged lipid profile and stimulate accumulation even more pronounced in cholecystectomized subjects of fat in the liver. Thus, it is reasonable to speculate that (Table 2). The tendency for an increase in BMI after chole- cholecystectomized patients are more likely to develop fatty cystectomy was not seen in patients who had undergone non- liver disease when exposed to the metabolic stress produced biliary surgery.30 This weight gain was generally
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