Skip to main content
SpringerLink
Log in

Obese boys with low concentrations of high-density lipoprotein cholesterol are at greater risk of hepatosteatosis

  • Original Article
  • Published:
Hormones Aims and scope Submit manuscript

Abstract

Purpose

Non-alcoholic fatty liver disease (NAFLD) and associated morbidities have become a major public health problem, with a global three-fold increase in incidence among obese children over the last three decades. Although the gold standard for diagnosis of NAFLD is liver biopsy, it is not widely used in children. Imaging techniques, including magnetic resonance imaging (MRI) and ultrasound (US), can provide information on liver fat deposition, however, with variable sensitivity. A number of other predictors are therefore being investigated for pediatric screening and diagnostic purposes. The aim of this study was to assess easily measured parameters to prompt further investigation into NAFLD in obese children.

Methods

Obese children/adolescents with a body mass index (BMI) percentile > 95 were enrolled in the study (n = 353). After a 12-hour fast, venous glucose, insulin, cholesterol, triglycerides (TG), high-density lipoprotein (HDL), low-density lipoprotein (LDL), and uric acid were measured and a full blood count was performed in all subjects. TG/LDL ratio, AST/platelet ratio index (APRI score), and homeostatic model of assessment for insulin resistance (HOMA-IR) were calculated. All patients underwent an abdominal US examination to assess hepatosteatosis.

Results

Of 353 patients, median age 12.5 (range, 6–17.9) years, 210 patients (59%) had US-proven hepatosteatosis. Female gender reduced the risk of steatosis 2.08-fold (p = 0.005), a one-unit increase in HDL reduced the risk of steatosis 1.02-fold (p = 0.042), and a one-unit increase in BMI led to a 1.11-fold (p = 0.002) increase in the risk of steatosis.

Conclusion

Gender, BMI, and HDL were found to be predictors of steatosis. Male patients with low HDL and high BMI are at greater risk of steatosis and should be carefully examined for the presence of NAFLD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Chalasani N, Younossi Z, Lavine JE et al (2012) American Association for the Study of Liver Diseases; American College of Gastroenterology; American Gastroenterological Association. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Am J Gastroenterol. 107:811–826

    Article  Google Scholar 

  2. Schwimmer JB, Deutsch R, Kahen T et al (2006) Prevalence of fatty liver in children and adolescents. Pediatrics. 118:1388–1393

    Article  Google Scholar 

  3. Valerio G, Licenziati MR, Iannuzzi A, Franzese A, Siani P et al (2006) Insulin resistance and impaired glucose tolerance in obese children and adolescents from Southern Italy. Nutr Metab Cardiovasc Dis 16:279–284

    Article  CAS  Google Scholar 

  4. Day CP, Saksena S (2002) Non-alcoholic steatohepatitis: definitions and pathogenesis. J Gastroenterol Hepatol. 17:377–384

    Article  Google Scholar 

  5. Karlas T, Petroff D, Garnov N et al (2014) Non-invasive assessment of hepatic steatosis in patients with NAFLD using controlled attenuation parameter and 1H-MR spectroscopy. PLoS One 17(9):e91987

    Article  Google Scholar 

  6. Feldstein AE, Alkhouri N, De Vito R et al (2013) Serum cytokeratin-18 fragment levels are useful biomarkers for nonalcoholic steatohepatitis in children. Am J Gastroenterol. 108:1526–1531

    Article  CAS  Google Scholar 

  7. Lombardi R, Pisano G, Fargion S (2016 Apr 12) Role of Serum Uric Acid and Ferritin in the Development and Progression of NAFLD. Int J Mol Sci. 17(4):548

    Article  Google Scholar 

  8. Alkhouri N, McCullough AJ (2012) Noninvasive diagnosis of NASH and liver fibrosis within the spectrum of NAFLD. Gastroenterol Hepatol. 8:661–668

    Google Scholar 

  9. Kurtoglu S, Hatipoglu N, Mazicioglu M, Kendirci M, Keskin M, Kondolot M (2010) Insulin resistance in obese children and adolescents: HOMA-IR cut-off levels in the prepubertal and pubertal periods. J Clin Res Ped Endo 2(3):100–106

    Google Scholar 

  10. Sahin NM, Kinik ST, Tekindal MA (2013) OGTT results in obese adolescents with normal HOMA-IR values. J Pediatr Endocr Met 26(3-4):285–291

    CAS  Google Scholar 

  11. de Ridder CM, Bruning CF, Zonderland ML, Thijssen JHH, Bonfrer JMG, Blankenstein MA, Huisveld IA, Erich WBM (1990) Body fat mass, body fat distribution and plasma hormones in early puberty in females. J Clin Endocrinol Metab 70(4):888–893

    Article  Google Scholar 

  12. Cohen D, Gonzales-Pacheco D, Myers O (2016) Relationships between alanine aminotransferase, serum triglycerides, body mass index and nonalcoholic fatty liver disease in an outpatient pediatric clinic population. J Pediatr Nurs. 31:152–158

    Article  Google Scholar 

  13. Arslan N, Büyükgebiz B, Oztürk Y et al (2005) Fatty liver in obese children: prevalence and correlation with anthropometric measurements and hyperlipidemia. Turk J Pediatr. 47:23–27

    PubMed  Google Scholar 

  14. Fonvig CE, Chabanova E, Ohrt JD (2015) et al, Multidisciplinary care of obese children and adolescents for one year reduces ectopic fat content in liver and skeletal muscle. BMC Pediatr.:15–196

  15. Schwimmer JB, McGreal N et al (2003) Influence of gender, race, and ethnicity on suspected fatty liver in obese adolescents. The prevalence and etiology of elevated aminotransferase levels in the United States. Am J Gastroenterol. 98:960–967

    Article  Google Scholar 

  16. Tominaga K, Kurata JH, Chen YK et al (1995) Prevalence of fatty liver in Japanese children and relationship to obesity. An epidemiological ultrasonographic survey. Dig Sci 40:2002–2009

    Article  CAS  Google Scholar 

  17. Franzese A, Vajro P, Argenziano A et al (1997) Liver involvement in obese children. Ultrasonography and liver enzyme levels at diagnosis and during follow-up in an Italian population. Dig Dis Sci 42:1428–1432

    Article  CAS  Google Scholar 

  18. Wiegand S, Keller KM, Röbl M, L’Allemand D, Reinehr T, Widhalm K, Holl RW, APV-Study Group and the German Competence Network Adipositas (2010 Oct) Obese boys at increased risk for nonalcoholic liver disease: evaluation of 16,390 overweight or obese children and adolescents. Int J Obes (Lond). 34(10):1468–1474

    Article  CAS  Google Scholar 

  19. Motamed N, Sohrabi M, Ajdarkosh H, Hemmasi G, Maadi M, Sayeedian FS, Pirzad R, Abedi K, Aghapour S, Fallahnezhad M, Zamani F (2016 Mar 14) Fatty liver index vs waist circumference for predicting non-alcoholic fatty liver disease. World J Gastroenterol. 22(10):3023–3030

    Article  CAS  Google Scholar 

  20. Pimenta NM, Cortez-Pinto H, Melo X, Silva-Nunes J, Sardinha LB, Santa-Clara H (2017 Apr) Waist-to-height ratio is independently related to whole and central body fat, regardless of the waist circumference measurement protocol, in non-alcoholic fatty liver disease patients. J Hum Nutr Diet. 30(2):185–192

    Article  CAS  Google Scholar 

  21. Lo K, Wong M, Khalechelvam P, Tam W (2016 Dec) Waist-to-height ratio, body mass index and waist circumference for screening paediatric cardio-metabolic risk factors: a meta-analysis. Obes Rev. 17(12):1258–1275. https://doi.org/10.1111/obr.12456

    Article  CAS  PubMed  Google Scholar 

  22. Ozkol M, Ersoy B, Kasirga E et al (2010) Metabolic predictors for early identification of fatty liver using doppler and B-mode ultrasonography in overweight and obese adolescents. Eur J Pediatr. 169:1345–1352

    Article  CAS  Google Scholar 

  23. Alkassabany YM, Farghaly AG, El-Ghitany EM (2014) Prevalence, risk factors, and predictors of nonalcoholic fatty liver disease among schoolchildren: a hospital-based study in Alexandria. Egypt Arab J Gastroenterol. 15:76–81

    Article  Google Scholar 

  24. Chan DF, Li AM, Chu WC et al (2004) Hepatic steatosis in obese Chinese children. Int J Obes Relat Metab Disord. 28:1257–1263

    Article  CAS  Google Scholar 

  25. Eminoğlu TF, Camurdan OM, Oktar SO et al (2008) Factors related to non-alcoholic fatty liver disease in obese children. Turk J Gastroenterol. 19:85–91

    PubMed  Google Scholar 

  26. Fu CC, Chen MC, Li YM et al (2009) The risk factors for ultrasound-diagnosed non-alcoholic fatty liver disease among adolescents. Ann Acad Med Singapore. 38:15–17

    PubMed  Google Scholar 

  27. Sartorio A, Del Col A, Agosti F et al (2007) Predictors of non-alcoholic fatty liver disease in obese children. Eur J Clin Nutr. 61:877–883

    Article  CAS  Google Scholar 

  28. Uslusoy HS, Nak SG, Gülten M, Biyikli Z (2009 Apr 21) Non-alcoholic steatohepatitis with normal aminotransferase values. World J Gastroenterol. 15(15):1863–1868

    Article  CAS  Google Scholar 

  29. Posadas-Sánchez R, Posadas-Romero C, Zamora-González J et al (2007) Lipid and lipoprotein profiles and prevalence of dyslipidemia in Mexican adolescents. Metabolism. 56:1666–1672

    Article  Google Scholar 

  30. Ten S, Maclaren N (2004) Insulin resistance syndrome in children. J Clin Endocrinol Metab. 89:2526–2539

    Article  CAS  Google Scholar 

  31. Alkhouri N, Eng K, Lopez R, Nobili V (2014 Aug 5) Non-high-density lipoprotein cholesterol (non-HDL-C) levels in children with nonalcoholic fatty liver disease (NAFLD). Springerplus. 3:407

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Mr. Jeremy Jones for his help in the writing and revision of this manuscript.

Author information

Authors and Affiliations

  1. Department of Pediatric Endocrinology, Ankara University School of Medicine, Ataturk Sıtesi 15th Block No. 21 Flat 7 Door Number 14 Oran, Ankara, Turkey

    Elif Ozsu

  2. Department of Family Medicine, Samsun Obstetrics and Children Hospital, Samsun, Turkey

    Bahadır Yazıcıoğlu

Authors
  1. Elif Ozsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bahadır Yazıcıoğlu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elif Ozsu.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ozsu, E., Yazıcıoğlu, B. Obese boys with low concentrations of high-density lipoprotein cholesterol are at greater risk of hepatosteatosis. Hormones 18, 477–484 (2019). https://doi.org/10.1007/s42000-019-00152-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42000-019-00152-2

Keywords

Search

Navigation