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Cholecystectomy Causes Ultrasound Evidence of Increased Hepatic Steatosis

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Abstract

Background

Cholecystectomy might contribute to the development of hepatic steatosis through metabolic changes. The biologic alteration of the enterohepatic circulation of bile acids and the alteration of the metabolic activity of bile acid that follows cholecystectomy may contribute to hepatic steatosis. This prospective study was conducted to clarify the possibility of steatosis development after cholecystectomy.

Methods

From October 2013 to July 2014, 82 consecutive patients with a presumptive diagnosis of gallbladder disease were cholecystectomized. Liver parenchymal steatosis was measured using ultrasound and the hepatic steatosis index.

Results

In all 82 patients, the hepatic steatosis index was found to be significantly correlated with the US fatty liver grade (Spearman’s correlation r 2 = 0.331, P < 0.001). A total of 62 patients were followed up for 3 months. Comparison with the initial grade showed that 12 (18.5 %) patients had worsened from normal to mild (n = 10), from mild to moderate (n = 1), and from mild to severe (n = 1). The other patients stayed at their initial grade except one patient who improved (from moderated to mild). Analysis of laboratory findings showed that white blood cell count, aspartate transaminase, alanine transaminase level, and total bilirubin level were decreased. However, serum albumin and high-density lipoprotein cholesterol levels significantly increased.

Conclusions

Hepatic steatosis significantly developed 3 months after cholecystectomy. Therefore, cholecystectomy might be considered a risk factor for hepatic steatosis, but the relationship should be confirmed with long-term follow-up from a large group of patients.

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Abbreviations

US:

Ultrasound

BMI:

Body mass index

WBC:

White blood cell

PLT:

Platelet

ALP:

Alkaline phosphatase

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

TG:

Triglyceride

HDL-C:

High-density lipoprotein cholesterol

LDL-C:

Low-density lipoprotein cholesterol

CRP:

C-reactive protein

HSI:

Hepatic steatosis index

References

  1. Chen LY, Qiao QH, Zhang SC et al (2012) Metabolic syndrome and gallstone disease. World J Gastroenterol WJG 18:4215–4220

    Article  CAS  PubMed  Google Scholar 

  2. Lockman KA, Nyirenda MJ (2010) Interrelationships between hepatic fat and insulin resistance in non-alcoholic fatty liver disease. Curr Diabetes Rev 6:341–347

    Article  CAS  PubMed  Google Scholar 

  3. Loria P, Lonardo A, Lombardini S et al (2005) Gallstone disease in non-alcoholic fatty liver: prevalence and associated factors. J Gastroenterol Hepatol 20:1176–1184

    Article  PubMed  Google Scholar 

  4. Ramos-De la Medina A, Remes-Troche JM, Roesch-Dietlen FB et al (2008) Routine liver biopsy to screen for nonalcoholic fatty liver disease (NAFLD) during cholecystectomy for gallstone disease: is it justified? J Gastrointest Surg 12:2097–2102 (Discussion 2102)

    Article  PubMed  Google Scholar 

  5. Koller T, Kollerova J, Hlavaty T et al (2012) Cholelithiasis and markers of nonalcoholic fatty liver disease in patients with metabolic risk factors. Scand J Gastroenterol 47:197–203

    Article  CAS  PubMed  Google Scholar 

  6. Nervi F, Miquel JF, Alvarez M et al (2006) Gallbladder disease is associated with insulin resistance in a high risk Hispanic population. J Hepatol 45:299–305

    Article  CAS  PubMed  Google Scholar 

  7. Bellentani S, Saccoccio G, Masutti F et al (2000) Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 132:112–117

    Article  CAS  PubMed  Google Scholar 

  8. Ruhl CE, Everhart JE (2013) Relationship of non-alcoholic fatty liver disease with cholecystectomy in the US population. Am J Gastroenterol 108:952–958

    Article  PubMed  Google Scholar 

  9. Ioannou GN (2010) Cholelithiasis, cholecystectomy, and liver disease. Am J Gastroenterol 105:1364–1373

    Article  CAS  PubMed  Google Scholar 

  10. Kullak-Ublick GA, Paumgartner G, Berr F (1995) Long-term effects of cholecystectomy on bile acid metabolism. Hepatology 21:41–45

    Article  CAS  PubMed  Google Scholar 

  11. Zweers SJ, Booij KA, Komuta M et al (2012) The human gallbladder secretes fibroblast growth factor 19 into bile: towards defining the role of fibroblast growth factor 19 in the enterobiliary tract. Hepatology 55:575–583

    Article  CAS  PubMed  Google Scholar 

  12. Amigo L, Husche C, Zanlungo S et al (2011) Cholecystectomy increases hepatic triglyceride content and very-low-density lipoproteins production in mice. Liver Int 31:52–64

    Article  CAS  PubMed  Google Scholar 

  13. Chalasani N, Younossi Z, Lavine JE et al (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Gastroenterological Association, American Association for the Study of Liver Diseases, and American College of Gastroenterology. Gastroenterology 142:1592–1609

    Article  PubMed  Google Scholar 

  14. American Diabetes Association (2012) Diagnosis and classification of diabetes mellitus. Diabetes Care 35(1):S64–71

    Article  PubMed Central  Google Scholar 

  15. Lee JH, Kim D, Kim HJ et al (2010) Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis 42:503–508

    Article  CAS  PubMed  Google Scholar 

  16. Lazo M, Hernaez R, Bonekamp S et al (2011) Non-alcoholic fatty liver disease and mortality among US adults: prospective cohort study. BMJ 343:d6891

    Article  PubMed  PubMed Central  Google Scholar 

  17. Brunt EM (2005) Pathology of nonalcoholic steatohepatitis. Hepatol Res 33:68–71

    Article  CAS  PubMed  Google Scholar 

  18. Matsuzawa N, Takamura T, Kurita S et al (2007) Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46:1392–1403

    Article  CAS  PubMed  Google Scholar 

  19. Wouters K, van Gorp PJ, Bieghs V et al (2008) Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology 48:474–486

    Article  PubMed  Google Scholar 

  20. Ioannou GN, Morrow OB, Connole ML et al (2009) Association between dietary nutrient composition and the incidence of cirrhosis or liver cancer in the United States population. Hepatology 50:175–184

    Article  CAS  PubMed  Google Scholar 

  21. Wang DQ, Lee SP (2008) Physical chemistry of intestinal absorption of biliary cholesterol in mice. Hepatology 48:177–185

    Article  CAS  PubMed  Google Scholar 

  22. Almond HR, Vlahcevic ZR, Bell CC Jr et al (1973) Bile acid pools, kinetics and biliary lipid composition before and after cholecystectomy. New Engl J Med 289:1213–1216

    Article  CAS  PubMed  Google Scholar 

  23. Shaffer EA, Small DM (1977) Biliary lipid secretion in cholesterol gallstone disease: the effect of cholecystectomy and obesity. J Clin Investig 59:828–840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Roda E, Aldini R, Mazzella G et al (1978) Enterohepatic circulation of bile acids after cholecystectomy. Gut 19:640–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Eren F, Kurt R, Ermis F et al (2012) Preliminary evidence of a reduced serum level of fibroblast growth factor 19 in patients with biopsy-proven nonalcoholic fatty liver disease. Clin Biochem 45:655–658

    Article  CAS  PubMed  Google Scholar 

  26. Drafahl KA, McAndrew CW, Meyer AN et al (2010) The receptor tyrosine kinase FGFR4 negatively regulates NF-kappaB signaling. PLoS One 5:e14412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Holt JA, Luo G, Billin AN et al (2003) Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev 17:1581–1591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kim I, Ahn SH, Inagaki T et al (2007) Differential regulation of bile acid homeostasis by the farnesoid X receptor in liver and intestine. J Lipid Res 48:2664–2672

    Article  CAS  PubMed  Google Scholar 

  29. Tomlinson E, Fu L, John L et al (2002) Transgenic mice expressing human fibroblast growth factor-19 display increased metabolic rate and decreased adiposity. Endocrinology 143:1741–1747

    Article  CAS  PubMed  Google Scholar 

  30. Abu-Elheiga L, Matzuk MM, Abo-Hashema KA et al (2001) Continuous fatty acid oxidation and reduced fat storage in mice lacking acetyl-CoA carboxylase 2. Science 291:2613–2616

    Article  CAS  PubMed  Google Scholar 

  31. Wang HG, Wang LZ, Fu HJ et al (2015) Cholecystectomy does not significantly increase the risk of fatty liver disease. World J Gastroenterol WJG 21:3614–3618

    Article  PubMed  Google Scholar 

  32. Hamaguchi M, Kojima T, Itoh Y et al (2007) The severity of ultrasonographic findings in nonalcoholic fatty liver disease reflects the metabolic syndrome and visceral fat accumulation. Am J Gastroenterol 102:2708–2715

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was carried out with the support of “Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ011002022015)” Rural Development Administration, Republic of Korea. This work was registered to U.S. National Institutes of Health (Clinicaltrials.gov Identifier: NCT02493153).

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Correspondence to Dongho Choi or Bo-Kyeong Kang.

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Dongho Choi and Bo-Kyeong Kang equally contributed to this journal as corresponding author.

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Yun, S., Choi, D., Lee, K.G. et al. Cholecystectomy Causes Ultrasound Evidence of Increased Hepatic Steatosis. World J Surg 40, 1412–1421 (2016). https://doi.org/10.1007/s00268-015-3396-7

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  • DOI: https://doi.org/10.1007/s00268-015-3396-7

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