Blood lipids in gallstone disease: associations with risk factors
https://doi.org/10.52727/2078-256X-2024-20-2-162-172
Abstract
Aim of the review – to present an analysis of the literature data on the association of serum lipids with the presence of gallstone disease (GSD), as well as with the main risk factors for GSD – age, female sex, obesity, type 2 diabetes mellitus (DM2), arterial hypertension (AH) over a 50-year period.
In numerous studies, hypertriglyceridemia (HTH), hypocholesterolemia of high-density lipoproteins (hypo-HDL) have been recognized as risk factors for GSD. In 1994–1995 in Novosibirsk (WHO MONICA project), in a population sample of women aged 25-64 (n = 870) and men aged 35–54 (n = 399) with sonographic diagnoses of GSD, GSD is much more common among men and women with lipid metabolism disorders: the highest frequency of GSD was noted in the 4th quartile of the distribution of total cholesterol (TC) levels (4.5 % for men and 12.4 % for women). For LDL cholesterol, the highest incidence of GSD was noted in the 5th quintile of the distribution (3.8 % in men and 10.9 % in women). When calculating by the largest χ2 method in women, the levels of TC (178 mg/dl), TG (177 mg/dl) in the blood were determined, exceeding which significantly increases the chance of GSD, for HDL cholesterol (68.5 mg/dl) the model is insignificant. There was a correlation between blood lipids and age, BMI, and DM2 in women with GSD, but not in men with GSD. The lipid profile in patients with GSD is not associated with AH. Most authors recognize GSD as a lipid-associated disease. However, the literature data are contradictory: there are opinions about a direct, inverse or absent association of blood lipids with GSD, perhaps due to differences in the design, size, and ethnicity of the subjects, as well as since the level of serum lipids is closely correlated with other risk factors for GSD, which significantly complicates the differentiated assessment of their contribution to the process of gallstone formation. Further studies of the contribution of lipid factors to the development of GSD are needed.
Keywords
About the Authors
I. N. Grigor’evaRussian Federation
Irina N. Grigor’eva, doctor of medical sciences, professor, chief researcher
630089; 175/1, Boris Bogatkov str.; Novosibirsk
Scopus Author ID: 7004630757; Web of Science Researcher ID JGE-0324-202; AuthorID: 96089
D. L. Nepomnyashchikh
Russian Federation
David L. Nepomnyashchikh, doctor of medical sciences, professor
chair for internal medicine of department of general medicine
630091; 52, Krasny av.; Novosibirsk
References
1. Grigor’eva I.N., Nikitin Yu.P. Prevalence of cholelithiasis in different regions. Clin. Med., 2007; 85 (9): 27–30. (In Russ.)
2. Hayat S., Hassan Z., Changazi S.H., Zahra A., Noman M., Zain U.l., Abdin M., Javed H., Ans A.H. Comparative analysis of serum lipid profiles in patients with and without gallstones: A prospective cross-sectional study. Ann. Med. Surg. (Lond), 2019; 42: 11–13. doi: 10.1016/j.amsu.2019.04.003
3. Portincasa P., di Ciaula A., Bonfrate L., Stella A., Garruti G., Lamont J.T. Metabolic dysfunction-associated gallstone disease: expecting more from critical care manifestations. Intern. Emerg. Med., 2023; 18 (7): 1897–1918. doi: 10.1007/s11739-023-03355-z
4. Zhang M., Mao M., Zhang C., Hu F., Cui P., Li G., Shi J., Wang X., Shan X. Blood lipid metabolism and the risk of gallstone disease: a multi-center study and meta-analysis. Lipids Health Dis., 2022; 21 (1): 26. doi: 10.1186/s12944-022-01635-9
5. Grigor’eva I.N., Ragino Yu.I., Romanova T.I., Malyutina S.K. Association between coronary heart disease and gallstone disease (epidemiological study). Ateroscleroz, 2019; 15 (2): 32–38. (In Russ.) doi: 10.15372/ATER20190205
6. Upala S., Sanguankeo A., Jaruvongvanich V. Gallstone disease and the risk of cardiovascular disease : a systematic review and meta-analysis of observational studies. Scand. J. Surg., 2017; 106 (1): 21–27. doi: 10.1177/1457496916650998
7. Grigor’eva I.N., Yamlikhanova A.Yu. The frequency of combination of gallstone disease and diabetes mellitus. Exp. Clin. Gastroenterol., 2011; 4: 99–102. (In Russ.)
8. Sun H., Warren J., Yip J., Ji Y., Hao S., Han W., Ding Y. Factors influencing gallstone formation : a review of the literature. Biomolecules, 2022; 12 (4): 550. doi: 10.3390/biom12040550
9. Grigor’eva I.N., Notova T.E. Apolypoprotein E gene polymorphism, gallstone disease, diabetes 2 type and lipid metabolism disorders. Ateroscleroz, 2023; 19 (1): 47–56. (In Russ.) doi: 10.52727/2078-256X-2023-19-1-47-56
10. Wang H.H., Portincasa P., Afdhal N.H., Wang D.Q. Lith genes and genetic analysis of cholesterol gallstone formation. Gastroenterol. Clin. North. Am., 2010; 39 (2): 185–207, vii-viii. doi: 10.1016/j.gtc.2010.02.007
11. Wang D.Q., Schmitz F., Kopin A.S., Carey M.C. Targeted disruption of the murine cholecystokinin-1 receptor promotes intestinal cholesterol absorption and susceptibility to cholesterol cholelithiasis. J. Clin. Invest., 2004; 114 (4): 521–528. doi: 10.1172/JCI16801
12. Ezhov M.V., Kukharchuk V.V., Sergienko I.V., Alieva A.S., Antsiferov M.B., Ansheles A.A., Arabidze G.G., Aronov D.M., Arutyunov G.P., Akhmedzhanov N.M., Balakhonova T.V., Barbarash O.L., Boytsov S.A., Bubnova M.G., Voevoda M.I., Galstyan G.R., Galyavich A.S., Gornyakova N.B., Gurevich V.S., Dedov I.I., Drapkina O.M., Duplyakov D.V., Eregin S.Ya., Ershova A.I., Irtyuga O.B., Karpov R.S., Karpov Yu.A., Kachkovsky M.A., Kobalava Zh.D., Koziolova N.A., Konovalov G.A., Konstantinov V.O., Kosmacheva E.D., Kotovskaya Yu.V., Martynov A.I., Meshkov A.N., Nebieridze D.V., Nedogoda S.V., Obrezan A.G., Oleinikov V.E., Pokrovsky S.N., Ragino Yu.I., Rotar O.P., Skibitsky V.V., Smolenskaya O.G., Sokolov A.A., Sumarokov A.B., Filippov A.E., Halimov Yu.Sh., Chazova I.E., Shaposhnik I.I., Shestakova M.V., Yakushin S.S., Shlyakhto E.V. Disorders of lipid metabolism. Clinical Guidelines 2023. Russian Journal of Cardiology, 2023; 28 (5): 5471. (In Russ.) doi: 10.15829/1560-4071-2023-5471
13. Grigor’eva I.N., Malyitina S.K.,Voevoda M.I. The role of hyperlipidemia in cholelithiasis. Exp. Clin. Gastroenterol., 2010; 4: 64–68. (In Russ.)
14. Ivashkin V.T., Mayev I.V., Baranskaya Ye.K., Okhlobystin A.V., Shulpekova Yu.O., Trukhmanov A.S., Sheptulin A.A., Lapina T.L. Gallstone disease diagnosis and treatment: guidelines of the Russian gastroenterological association. RJHGGK, 2016; 3: 64–80. (In Russ.)
15. Wang J., Shen S., Wang B., Ni X., Liu H., Ni X., Yu R., Suo T., Liu H. Serum lipid levels are the risk factors of gallbladder stones: a population-based study in China. Lipids. Health Dis., 2020; 19 (1): 50. doi: 10.1186/s12944-019-1184-3
16. Einarsson K., Hellström K., Kallner M. Gallbladder disease in hyperlipoproteinaemia. Lancet, 1975; 1 (7905): 484–487. doi: 10.1016/s0140-6736(75)92831-7
17. The epidemiology of gallstone disease in Rome, Italy. Part II. Factors associated with the disease. The Rome Group for Epidemiology and Prevention of Cholelithiasis (GREPCO). Hepatology, 1988; 8 (4): 907–913.
18. Jшrgensen T. Gallstones and plasma lipids in a Danish population. Scand. J. Gastroenterol., 1989; 24 (8): 916–922. doi: 10.3109/00365528909089235
19. Thijs C, Knipschild P, Brombacher P. Serum lipids and gallstones: a case-control study. Gastroenterology, 1990; 99 (3): 843–849. doi: 10.1016/0016-5085(90)90978-a
20. Attili A.F., Carulli N., Roda E., Barbara B., Capocaccia L., Menotti A., Okoliksanyi L., Ricci G., Capocaccia R., Festi D. Epidemiology of gallstone disease in Italy: prevalence data of the Multicenter Italian Study on Cholelithiasis (M.I.COL.). Am. J. Epidemiol., 1995; 141 (2): 158–165. doi: 10.1093/oxfordjournals.aje.a117403
21. Saraya A., Irshad M., Gandhi B.M., Tandon R.K. Plasma lipid profile in gallstone patients from North India. Trop. Gastroenterol., 1995; 16 (4): 16–21.
22. Chen C.Y., Lu C.L., Lee P.C., Wang S.S., Chang F.Y., Lee S.D. The risk factors for gallstone disease among senior citizens: an Oriental study. Hepatogastroenterology, 1999; 46 (27): 1607–1612.
23. Sun H., Tang H., Jiang S., Zeng L., Chen E.Q., Zhou T.Y., Wang Y.J. Gender and metabolic differences of gallstone diseases. World J. Gastroenterol., 2009; 15: 1886–1891.
24. Halldestam I., Kullman E., Borch K. Incidence of and potential risk factors for gallstone disease in a general population sample. Br. J. Surg., 2009; 96: 1315–1322. doi: 10.1002/bjs.6687
25. Zák A., Zeman M., Hrubant K., Vecka M., Tvrzická E. Effect of hypolipidemic treatment on the composition of bile and the risk or cholesterol gallstone disease. Cas. Lek. Cesk., 2007; 146: 24–34.
26. Channa N.A., Ghanghro A.B., Soomro A.M. Quantitative analysis of serum lipid profile in gallstone patients and controls. Pakistan J. Analyti. Environm. Chem., 2010; 11 (1): 7.
27. Smelt A.H. Triglycerides and gallstone formation. Clin. Chim. Acta, 2010; 411: 1625–1631. doi: 10.1016/j.cca.2010.08.003
28. Rao P.J., Jarari A., El-Awami H., Patil T.N., El-Saiety S.O. Lipid profile in bile and serum of cholelithiasis patients-A comparative study. J. Basic Med. Allied Sci., 2012; 1: 27–39.
29. Al-Saadi N., Al-Ardhi S. Biochemical and demographical study of lipid profile in sera of patients with gallstone. Iraqi J. Sci., 2012; 53 (4): 760–768.
30. Zamani F., Sohrabi M., Alipour A., Motamed N., Saeedian F.S., Pirzad R., Abedi K., Maadi M., Ajdarkosh H., Hemmasi G., Khonsari M. Prevalence and risk factors of cholelithiasis in Amol city, northern Iran: a population based study. Arch. Iran. Med., 2014; 17 (11): 750–754.
31. Shabanzadeh D.M., Sørensen L.T., Jørgensen T. Determinants for gallstone formation - a new data cohort study and a systematic review with meta-analysis. Scand. J. Gastroenterol., 2016; 51 (10): 1239–1248. doi: 10.1080/00365521.2016.1182583
32. Shinchi K., Kono S., Honjo S., Imanishi K., Hirohata T. Serum lipids and gallstone disease. A study of self-defense officials in Japan. Ann. Epidemiol., 1993; 3: 614–618. doi: 10.1016/1047-2797(93)90084-h
33. Chen C.H., Huang M.H., Yang J.C., Nien C.K., Etheredge G.D., Yang C.C., Yeh Y.H., Wu H.S., Chou D.A., Yueh S.K. Prevalence and risk factors of gallstone disease in an adult population of Taiwan: an epidemiological survey. J. Gastroenterol. Hepatol., 2006; 21 (11): 1737–1743. doi: 10.1111/j.1440-1746.2006.04381.x
34. Aulakh R., Mohan H., Attri A.K., Kaur J., Punia R.P. A comparative study of serum lipid profile and gallstone disease. Indian J. Pathol. Microbiol., 2007;50(2):308–312.
35. Tîrziu S., Bel S., Bondor C.I., Acalovschi M. Risk factors for gallstone disease in patients with gallstones having gallstone heredity. A case-control study. Rom. J. Intern. Med., 2008; 46: 223–228.
36. Cojocaru C., Pandele G.I. Metabolic profile of patients with cholesterol gallstone disease Rev. Med. Chir. Soc. Med. Nat. Iasi., 2010; 114: 677–682.
37. Öner C., Güneri M.C. Lipid profiles of patients with gallstones. Turk. J. Family Pract., 2012; 22: 123–126.
38. Batajoo H., Hazra N.K. Analysis of serum lipid profile in cholelithiasis patients. J. Nepal. Health Res. Counc., 2013; 11 (23): 53–55.
39. Weerakoon H.T., Ranasinghe S., Navaratne A., Sivakanesan R., Galketiya K.B., Rosairo S. Serum lipid concentrations in patients with cholesterol and pigment gallstones. BMC Res. Notes, 2014; 7: 548. doi: 10.1186/1756-0500-7-548
40. Gul H., Ayub M., Akhtar A. Mean serum calcium and lipid profile in patients with gallstone disease in southern Punjab. Pak. J. Med. Health Sci., 2016; 1: 548–551.
41. Shabanzadeh D.M., Holmboe S.A., Sørensen L.T., Linneberg A., Andersson A.M., Jørgensen T. Are incident gallstones associated to sex-dependent changes with age? A cohort study. Andrology, 2017; 5 (5): 931–938. doi: 10.1111/andr.12391
42. Dhamnetiya D., Goel M.K., Dhiman B., Pathania O.P. Gallstone disease and its correlates among patients attending teaching hospital of North India. J. Family Med. Prim. Care, 2019; 8 (1): 189–193. doi: 10.4103/jfmpc.jfmpc_358_18
43. Jonkers I.J., Smelt A.H., Ledeboer M., Hollum M.E., Biemond I., Kuipers F., Stellaard F., Boverho F.R., Meinders A.E., Lamers C.H., Masclee A.A. Gall bladder dysmotility: a risk factor for gall stone formation in hypertriglyceridaemia and reversal on triglyceride lowering therapy by bezafibrate and fish oil. Gut, 2003; 52: 109–115. doi: 10.1136/gut.52.1.109
44. Grigor’eva I., Romanova T., Naumova N., Alikina T., Kuznetsov A., Kabilov M. Gut microbiome in a russian cohort of pre- and post-cholecystectomy female patients. J. Pers. Med., 2021; 11 (4): 294. doi: 10.3390/jpm11040294
45. Grigor’eva I.N., Notova T.E., Romanova T.I. Physical activity and gallstone disease. Russian Journal of Gastroenterology, Hepatology, Coloproctology, 2023; 33 (1): 7–14. (In Russ.). doi: 10.22416/1382-4376-2023-33-1-7-14
46. Grigor’eva I.N., Slobodchikova M.A., Maksimov V.N., Denisova D.V., Zavyalova L.G. Polymorphism of the АРО Е gene and lithogenicity of bile in persons with hereditary burden of cholelithiasis. Bull. NSU, 2011; 1: 93–98. (In Russ.)
47. Grigorieva I.N., Romanova T.I., Lebedeva M.S. Lipid profile in patients with cholelithiasis in combination with arterial hypertension. Atherosclerosis, 2023; 19 (3): 205–207. (In Russ.). doi: 10.52727/2078-256X-2023-19-3-205-207
48. Grigorieva I.N. Arterial hypertension and gallstone disease: epidemiology, lipids and genetic polymorphism. In: Epidemiology of arterial hypertension in Siberia. Eds. G.I. Simonova, Yu.I. Ragino. Novosibirsk: Nauka, 2024. P. 227–236. (In Russ.)
49. Grigor’eva I.N. Gallstone disease, obesity and the firmicutes/bacteroidetes ratio as a possible biomarker of gut dysbiosis. J. Pers. Med., 2020; 11 (1): 13. doi: 10.3390/jpm11010013
50. Grigor’eva I.N. The main risk factors for cholelithiasis. RZHGGK, 2007; 6: 17–21. (In Russ.)
51. Einarsson K., Nilsell K., Leijd B., Angelin B. Influence of age on secretion of cholesterol and synthesis of bile acids by the liver. N. Engl. J. Med., 1985; 313 (5): 277–282. doi: 10.1056/NEJM198508013130501
52. Grigor’eva I.N., Notova T.E., Suvorova T.S., Nepomnyashchikh D.L. Polymorphisms of the ATP-binding cassette sterol efflux transporter genes g5 and g8 in cardiovascular diseases and type 2 diabetes mellitus. Ateroscleroz, 2024; 20 (1): 6–15. (In Russ.). doi: 10.52727/2078-256X-2024-20-1-6-15
53. Kurtin W.E., Schwesinger W.H., Diehl A.K. Agerelated changes in the chemical composition of gallstones. Int. J. Surg. Investig., 2000; 2 (4): 299–307.
54. Grigor’eva I.N., Nikitin Yu.P. Female sex hormones and some other factors in the pathogenesis of gallstone disease. Therapeutic Archive, 2005; 2; 49–52. (In Russ.)
55. di Ciaula A., Wang D.Q., Portincasa P. An update on the pathogenesis of cholesterol gallstone disease. Curr. Opin. Gastroenterol., 2018; 34 (2): 71–80. doi: 10.1097/MOG.0000000000000423
56. Valdivieso V., Covarrubias C., Siegel F., Cruz F. Pregnancy and cholelithiasis: Pathogenesis and natural course of gallstones diagnosed in early puerperium. Hepatology, 1993; 17: 1–4.
57. Petukhov V.A., Kuznetsov M.R., Lisin S.V., Kantemirova Z.N. Cholelithiasis and pregnancy: causal relationships. Ann. Surgery, 1998; 2: 14–20.(In Russ.)
58. Everson G.T. Liver problems in pregnancy: distinguishing normal from abnormal hepatic changes. Medscape Womens Health, 1998; 3 (2): 3.
59. Liu T., Wang W., Ji Y., Wang Y., Liu X., Cao L., Liu S. Association between different combination of measures for obesity and new-onset gallstone disease. PLoS ONE, 2018; 13: e0196457. doi: 10.1371/journal.pone.0196457
60. Lei Z.-M., Ye M.-X., Fu W.-G., Chen Y., Fang C., Li J. Levels of serum leptin, cholecystokinin, plasma lipid and lipoprotein differ between patients with gallstone or/and those with hepatolithiasis. Hepatobiliary Pancreat. Dis. Int., 2008; 7: 65–69.
61. Stahlberg D., Rudling M., Angelin B., Björkhem I., Forsell P., Nilsell K., Einarsson K. Hepatic cholesterol metabolism in human obesity. Hepatology, 1997; 25: 1447–1450. doi: 10.1002/hep.510250623
62. Salinas G., Velásquez C., Saavedra L., Ramírez E., Angulo H., Tamayo J.C., Orellana A., Huivin Z., Valdivia C., Rodríguez W. Prevalence and risk factors for gallstone disease. Surg. Laparosc. Endosc. Percutan. Tech., 2004; 14 (5): 250–253. doi: 10.1097/00129689-200410000-00003
63. Biddinger S.B., Haas J.T., Yu B.B., Bezy O., Jing E., Zhang W., Unterman T.G., Carey M.C., Kahn C.R. Hepatic insulin resistance directly promotes formation of cholesterol gallstones. Nat. Med., 2008; 14 (7): 778–782. doi: 10.1038/nm1785
64. Nakeeb A., Comuzzie A.G., Al-Azzawi H., Sonnenberg G.E., Kissebah A.H., Pitt H.A. Insulin resistance causes human gallbladder dysmotility. J. Gastrointest. Surg., 2006; 10: 940–949. doi: 10.1016/j.gassur.2006.04.005
65. Niemi M., Kervinen K., Rantala A., Kauma H., Päivänsalo M., Savolainen M.J., Lilja M., Kesäniemi Y.A. The role of apolipoprotein E and glucose intolerance in gallstone disease in middle aged subjects. Gut, 1999; 44 (4): 557–562. doi: 10.1136/gut.44.4.557
66. Zhang Y., Sun L., Wang X., Chen Z. The association between hypertension and the risk of gallstone disease: a cross-sectional study. BMC Gastroenterol., 2022; 22 (1): 138. doi: 10.1186/s12876-022-02149-5
67. Yu K.J., Zhang J.R., Li Y., Huang X., Liu T., Li C., Wang R.T. Gallstone disease is associated with arterial stiffness progression. Hypertens. Res., 2017; 40 (1): 314. doi: 10.1038/hr.2016.109
68. Lu S.C., Akanji A.O. Leptin, obesity and hypertension : review of pathogenetic mecha-nisms. Metab. Syndr. Relat. Disord., 2020; 18 (9): 399–405. doi:10.1089/met.2020.0065
69. Wen J., Jiang Y., Lei Z., He J., Ye M., Fu W. Leptin influence cholelithiasis formation by regulating bile acid metabolism. Turk. J. Gastroenterol., 2021; 32 (1): 97–105. doi: 10.5152/tjg.2020.19594
Review
For citations:
Grigor’eva I.N., Nepomnyashchikh D.L. Blood lipids in gallstone disease: associations with risk factors. Ateroscleroz. 2024;20(2):162-172. (In Russ.) https://doi.org/10.52727/2078-256X-2024-20-2-162-172