Open access peer-reviewed chapter

Nonalcoholic Fatty Liver Disease: The Future Frontier of Hepatology for South Asia

Written By

Shahinul Alam, Thupten Kelsang Lama, Golam Mustafa, Mahabubul Alam and Nooruddin Ahmad

Submitted: 06 April 2017 Reviewed: 21 September 2017 Published: 20 December 2017

DOI: 10.5772/intechopen.71159

From the Edited Volume

Non-Alcoholic Fatty Liver Disease - Molecular Bases, Prevention and Treatment

Edited by Rodrigo Valenzuela

Chapter metrics overview

1,529 Chapter Downloads

View Full Metrics

Abstract

This review is to know the magnitude of nonalcoholic fatty liver disease (NAFLD) among general population and risk group populations of the South Asian countries. A thorough search of evidence-based literature was conducted using the PubMed database with key words. Databases searched from inception to February 2017. Systematic search of the literature was conducted for studies pertaining. Prevalence of NAFLD in South Asia varies from 13 to 34%. The Highest rate is in Bangladesh (34.34%) and lowest in Pakistan (13.5%). Prevalence of NAFLD is 15–80% among obese people, 25–60% with dyslipidemia and 33–55% in pre diabetics and diabetics. Nonalcoholic steatohepatitis (NASH) is present in about 50% of the NAFLD cases that can lead to fibrosis, cirrhosis or even hepatocellular carcinoma (HCC). NAFLD is not the disease for only obese people, but it is also common in nonobese in this region. About 11.11% hepatocellular carcinoma developed from NASH. Incidence rate of diabetes and coronary artery disease is high among NAFLD patients. NAFLD is becoming a future challenge for South Asia region. Prevalence and severity has been remarkably increasing for last few years. The health system should get ready to confront burden of NAFLD in future for South Asia.

Keywords

  • nonalcoholic fatty liver disease
  • nonalcoholic steatohepatitis
  • South Asia

1. Introduction

Nonalcoholic fatty liver disease (NAFLD) is a characterized by excessive accumulation of fat (defined as the presence of lipid in >5% of hepatocytes or a lipid content >5% of liver weight) [1] in the liver, who consume little (<20 g of alcohol/d) or no alcohol [1, 2]. It is the most common cause of chronic liver injury [3]. Worldwide millions of people are affected by the NAFLD and it is prophesied to be the following universal epidemic [4]. Universally its prevalence rate is 25.24 with highest in the Middle East and South America and lowest in Africa [5]. The NAFLD with necroinflammation, defined as nonalcoholic steatohepatitis (NASH) [2]. According to Younossi ZM, universally overall mortality for NAFLD is 1.05; and incidence of hepatocellular carcinoma (HCC) and liver-specific mortality among NAFLD is 0.44 and 0.77 per 1000 person-years respectively. About 30% NAFLD progress to NASH, it can be lead to fibrosis, cirrhosis or even hepatocellular carcinoma [6]. HCC is one of the most common cancers worldwide and its burden is highest in the South-East Asia [7]. Countries with higher economic status tend to present a higher prevalence of NAFLD [8]. But it is not uncommon in low economic countries like countries of South Asia. The prevalence of NAFLD has increased remarkably over the years in South Asia and South-East Asia affecting 5–34% of general population [9, 10]. Metabolic syndrome common in people from South Asia is an important risk factor for NAFLD and Bangladeshi ethnicity is an important independent risk factor for NAFLD [3]. It is commonly described as hepatic manifestation of metabolic syndrome and insulin resistance. Though prevalence of NAFLD markedly increased in obese population, presence of NAFLD is further more challenging to diagnose and manage in lean population. In this study we aimed to know the prevalence NAFLD among general population and risk group populations of the South Asian countries. We also explored the prevalence of NASH and its associated conditions.

Advertisement

2. Materials and methods

We performed a systematic PubMed/MEDLINE literature search with the following key words: “Non-alcoholic Fatty Liver Disease/epidemiology”[Mesh], “Non-alcoholic steatohepatitis” [Text word] AND “Liver Transplantation/etiology”[Mesh], “Obesity”[Mesh], “Diabetes Mellitus”[Mesh], “Global,” “Afghanistan,” “Pakistan,” “India,” “Sri Lanka,” “Maldives,” “Nepal,” “Bangladesh,” and “Bhutan.” Databases searched from inception to February 2017. Exclusions included data on alcohol consumption or other liver diseases. Relevant full article, abstract, review, mini review, editorial and conference proceeding are included in this review.

Advertisement

3. Global epidemiology

Nonalcoholic fatty liver disease (NAFLD) is the commonest liver disease with global prevalence of approximately 25.24% of the general population [5]. Nonalcoholic steatohepatitis (NASH) and NAFLD are not only a Western disease. NAFLD and NASH have increasingly been diagnosed in all regions of Asia [11]. A study using the National Health and Nutrition Examination Survey (NHANES) found a 30% prevalence of NAFLD in the United States between 2011 and 2012 [12]. NAFLD is the most common cause of chronic liver disease in Western countries. It affects about 1 billion individuals worldwide [13]. Increasing prevalence of NASH is closely associated with prevalence diabetes and obesity, which may defined as epidemic worldwide. At least 1.46 billion obese adult is persisting in the world. Approximately 6 million individuals in the USA are in the risk of developing NASH and about 0.6 million to develop NASH-related cirrhosis [14]. Table 1 shows estimated prevalence of NAFLD and NASH. Reports on the prevalence of NAFLD and NASH vary substantially due to varying definitions, differences in the populations studied, and the diagnostic methods used [14].

RegionPopulation studiedPrevalence of NAFLD in these populations (%)
USAPediatric population13–14
General population27–34
EuropePediatric population2.6–10
General population20–30
Middle EastGeneral population20–30
Far EastGeneral population15
South AsiaGeneral population5–30

Table 1.

Estimated prevalence of NAFLD and NASH among different areas of the word.

Advertisement

4. Delineation of South Asia and its population diversity

According to the United Nations geographic region ordering, South Asia comprised with Afghanistan, Bangladesh, Bhutan, India, Maldives, Nepal, Pakistan, and Sri Lanka (Figure 1). Topographically, it is dominated by the Indian Plate; the terms “Indian subcontinent” and “South Asia” are sometimes used interchangeably [15]. South Asia is the most populated region in the world [16]. Socially it is very mixed, consisting of many language groups and religions, and social practices in one region that are vastly different from those in another [17].

Figure 1.

Geographical position and area of South Asia [16].

Advertisement

5. Prevalence of NAFLD among South Asian people

Recent socioeconomic changes have resulted in an emerging epidemic of non-communicable diseases such as type 2 diabetes and nonalcoholic fatty liver disease. The prevalence of nonalcoholic fatty liver disease in Asian Pacific countries now approximates and even overrides levels encountered in Western countries in some studies [18]. NAFLD is the emerging challenge for public health issue in Asia [19]. This has a potential burden not only on liver disease but also on metabolic syndrome related morbidity: obesity, diabetes, and atherosclerotic cardiovascular disease [19]. Largest population of the world inhabiting in Asia are passing through an economic growth and shift of focus from a dominant physical activity to knowledge, capital and physical inactivity. An increasing GDP is paralleled by a rising body mass index (BMI) in an almost linear fashion [19]. Countries with higher economic status tend to present a higher prevalence of NAFLD [8]. It is believed to provide a distinctive epidemiologic perspective to global situation of NAFLD. Especially for South Asia, according to increasing with their economy the prevalence of NAFLD is increasing day by day.

Most of the available epidemiological studies in NAFLD from Asia are ultrasound based and hence detect prevalence of hepatic steatosis alone initially, correlating it with anthropometric, biochemical, and demographic features of the population (Table 2). The community prevalence of NAFLD in South Asia and South-East Asia ranges from 5 to 30% [9, 10]. Recently a hospital based study in Pakistan had shown a frequency of approximately 14%. In India, it varies from 5 to 28% in general population, especially those who are undergoing health check-ups. Indians have increased propensity for visceral fat accumulation which may present from birth [9]. Prevalence of NAFLD in general population of Bangladesh has been estimated to vary from 4 to 34.34% [20, 21], which exceeds previous reports and it jumps up to 49.8% in diabetic patients [22, 23]. And in Sri Lanka the prevalence rate was found 32.6 in an urban based study [24]. So it is seen that, among South Asian countries the highest magnitude of NAFLD is in Bangladesh and lowest is in Pakistan (Figure 2).

CountryPopulation and placeSample size (n)Prevalence of NAFL
IndiaSelected population Mumbai116816.6%
General population West Bengal (rural)1911167 (8.7%)
General population Chennai (urban)541173 (32%)
BangladeshGeneral population Nation wide2621900 (34.34%)
Selected Population Camilla (rural)665219 (33%)
Sri LankaGeneral population (urban)2985974 (32.6%)
PakistanTertiary care hospital, Karachi952129 (13.5%)

Table 2.

Prevalence of NAFLD among the Indian, Sri Lanka and Pakistani people.

Figure 2.

Prevalence of NAFLD in different countries of South Asia.

From the study of Alazawi et al. the prevalence of recorded NAFLD varied considerably by ethnic group. This study identified that Bangladeshi ethnicity as an independent risk factor for NAFLD. Diagnosed NAFLD was significantly more prevalent among people of Bangladesh ethnicity (1.8% of the adult population) than other ethnic group, including other South Asian groups. Among Bangladeshis, there are higher rates of type 2 diabetes and cardiovascular disease that may have a genetic basis. Transaminase were measured on 218,032 patients, of whom 31,627 had elevated serum transaminases. In a multivariate analysis, independent risk factors for NAFLD included Bangladeshi ethnicity, diabetes, raised BMI, hypertension, and hypercholesterolaemia. As expected, the prevalence of NAFLD was significantly lower in the African and Caribbean ethnic groups [19]. Female are predominant sufferers of NAFLD in Bangladesh [25]. So the prevalence of NAFLD in South Asia has been increased from previous reports and now it ranges from 14 to 34.34% in general population. In systematic searching in PubMed/MEDLINE database, we found research articles on epidemiology of NAFLD of India, Bangladesh, Sri Lanka and Pakistan. But we did not get any article relevant to the epidemiology of NAFLD of Afghanistan, Maldives, Nepal and Bhutan.

Advertisement

6. Prevalence of NASH and its progression

The active form of NAFLD is non-alcoholic steatohepatitis (NASH), which is characterized by hepatocyte injury with liver inflammation, and progression of fibrosis [26]. And it has emerged as one of the most important causes of liver failure and hepatocellular carcinoma. Up to 20% of cases NASH may progress to cirrhosis [27]. According to Alam et al. “Patients with NASH are at risk for progressive liver disease (which can progress to cirrhosis, hepatocellular carcinoma, and death from chronic liver disease), as well as cardiovascular mortality and type-2 diabetes” [25].

NASH is present in 42.4–53.1% cases of Bangladeshi NAFLD patients [25]. Diabetic is the principle cause to develop NASH. A study in Indian Diabetic Mellitus (DM) patient; it reported that severe NASH is present among 9.35% Indian DM patients [28]. Ultrasound based Indian study showed the prevalence of NAFLD to be 16.6%, while a study based on liver biopsy showed the presence of NASH was 53% [29, 30]. And in Sri Lanka a liver biopsy based study were performed on 296 patients and 100 (35.1%) were diagnosed as having NASH [31]. In another Asian study proven NASH at presentation was found in 32.6% patients of NAFLD [32].

Study from the West found that disease progression from NAFLD to NASH is 44% patients [33]. Multiple factors like obesity, insulin resistance, genetic factor, immune response and lipotoxicity are involved in the progression of NAFLD to NASH [34]. In patients with cirrhotic NASH, HCC and liver failure are the main causes of morbidity and mortality. A prospective Japanese study elucidated the progression from NASH to HCC is 11.3% [35]. The prevalence of NASH (9.35–59%) among NAFLD patients is much higher in South Asian countries than that of Western countries. Severity of NAFLD in the form of NASH is also highest in Bangladesh among the South Asian countries as evidenced by recent studies from tertiary level hospitals of the country.

Advertisement

7. Depiction of the magnitude among different risk group

According to Alam, one fourth of the Bangladeshi NAFLD patients are nonobese; among them 53.1% cases present NASH. Male are largely dominating in nonobese group, where female are in obese group [36]. High BMI, central obesity, triglyceridemia and age are important risk factors for Bangladeshi people, and risk factors contributed about 29% risk for the occurrence of NASH [37]. After adjusting the risk factors (BMI and TG) female gender is the independent risk for Bangladeshi [38]. Although insulin resistance (IR) is strongly associated with NAFLD, But IR is not the sole predictor in the pathogenesis of NAFLD [38, 39, 40].

In India the prevalence of NAFLD is 15–80% among obese people, 25–60% in patients with dyslipidemia and 33–55% in pre-diabetics and diabetics’ Indian people [41]. Most of the non-diabetic NAFLD patients are overweight/obese with higher insulin resistance, dyslipidemia, and subclinical inflammation [42]. Among 65.7% Morbidly Obese South Indian Patients has NAFLD. Among them 33.6% were of NASH, 31.3% shows fibrosis and 14.1% shows advanced fibrosis [43]. The polymorphism T-455C in APOC3 gene and elevated serum triglycerides are associated with Indian NAFLD patients [44]. In another series, 56.5% T2DM patients have NAFLD, and the prevalence is higher in females (60%) than males T2DM patients [45]. NAFLD is the commonest liver disease in Indian psoriatic patients also [46]. Coronary artery disease (CAD) is more prevalent in the NAFLD compared to non-NAFLD; It is a surrogate and fairly reliable marker of risk for CAD among type 2 diabetic patients [47]. According to Duseja NAFLD is the commonest cause of unexplained elevation of SGPT and cryptogenic cirrhosis and hepatocellular carcinoma in Indian patients. Insulin resistance and full blown metabolic syndrome are highly prevalent in Indian patients with NAFLD [48]; 51.4% of patients of NAFLD have metabolic syndrome [49]. And it is really threatening news that 3% of 5–12 years Indian children have NAFLD [50].

In Sri Lanka Incidence rate of diabetes are 64.2 per 1000 person-years among NAFLD persons [51]. NAFLD is an independent predictor of developing diabetes mellitus [51]. Increased age and presence of NAFLD conferred a higher mortality risk from ACS as predicted by GRACE score [52].

As like developed countries obesity, insulin resistance, diabetes, dyslipidemia are the major risk factors for development of NAFLD. But the paradox is that it could develop in nonobese population also and one fourth of NAFLD of South Asia is from nonobese people.

Advertisement

8. Global and South Asian publication trend on NAFLD

According to Zhang et al. study, with the globally increasing prevalence, nonalcoholic fatty liver disease (NAFLD) becomes the predominant cause of chronic liver disease. The global scientific research articles relevant to NAFLD revealed 6356 articles were published in 994 different journals during 1986–2013. Starting from the late 1980s, the publication on NAFLD grew slowly and entered into a highly developing period in the 21st century, especially in the last decade (Figure 3). Bibliometric results suggest that the obviously rapid growth of the articles in recent years appears to be associated with the accelerating incidence of NAFLD and its cofactors such as metabolic syndrome. In this study we found that, from inception to 2012 only 16 Indian research articles have been published in PubMed. Where from 2013 to 2016 total 85 research articles of India, Bangladesh, Sri Lanka and Pakistan has been published in PubMed (Figure 4). This phenomenon indicate that, how NAFLD is growing in South Asia.

Figure 3.

Trend of number of publication on NAFLD of South Asia (published in PubMed).

Figure 4.

Article on NAFLD publication in South Asia Trend in PubMed from inception-2016.

Advertisement

9. Conclusion

The increase in NAFLD will continue to burden the health care system, especially because of its association with obesity, IR and metabolic syndrome. Along with globalization the prevalence of NAFLD is increasing alarmingly. The prevalence of NAFLD has been increasing remarkably for the last 12 years. Currently it is not only a disease of the Western countries but also becoming a major challenge for South Asia region. NAFLD is not the disease for only obese people, but it is also common in nonobese. And if the condition remains untreated it can turn into cirrhosis and hepatocellular carcinoma. It is really a great threat for us that, NAFLD is being seeing among our subcontinent’s children also. The burden of NAFLD and its severity projects that obviously it will be the biggest frontier of Hepatology in South Asia in near future.

References

  1. 1. Arab JP, Candia R, Zapata R, Munoz C, Arancibia JP, Poniachik J, Soza A, Fuster F, Brahm J, Sanhueza E, Contreras J, Cuellar MC, Arrese M, Riquelme A. Management of nonalcoholic fatty liver disease: An evidence-based clinical practice review. World Journal of Gastroenterology. 2014;20:12182-12201 [PMID: 25232252]. DOI: 10.3748/wjg.v20.i34.12182
  2. 2. Zhang TS, Qin HL, Wang T, Li HT, Li H, Xia SH, Xiang XH. Global publication trends and research hotspots of nonalcoholic fatty liver disease: A bibliometric analysis and systematic review. SpringerPlus. 2015;4:776 [PMID: 26697286]. DOI: 10.1186/s40064-015-1542-1
  3. 3. Alazawi W, Mathur R, Abeysekera K, Hull S, Boomla K, Robson J, Foster GR. Ethnicity and the diagnosis gap in liver disease: A population-based study. The British Journal of General Practice. 2014;64:e694-e702 [PMID: 25348993]. DOI: 10.3399/bjgp14X682273
  4. 4. Sherif ZA, Saeed A, Ghavimi S, Nouraie SM, Laiyemo AO, Brim H, Ashktorab H. Global epidemiology of nonalcoholic fatty liver disease and perspectives on US Minority populations. Digestive Diseases and Sciences. 2016;61:1214-1225 [PMID: 27038448]. DOI: 10.1007/s10620-016-4143-0
  5. 5. Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology. 2016;64:73-84. [PMID: 26707365]. DOI: 10.1002/hep.28431
  6. 6. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ. 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. Hepatology. 2012;55:2005-2023 [PMID: 22488764]. DOI: 10.1002/hep.25762
  7. 7. Ashtari S, Pourhoseingholi MA, Zali MR. Non-alcohol fatty liver disease in Asia: Preventionand planning. World Journal of Hepatology. 2015;7:1788-1796 [PMID: 26167252]. DOI: 10.4254/wjh.v7.i13.1788
  8. 8. Zhu JZ, Dai YN, Wang YM, Zhou QY, CH Y, Li YM. Prevalence of nonalcoholic fatty liver disease and economy. Digestive Diseases and Sciences. 2015;60:3194-3202. [PMID: 26017679]. DOI: 10.1007/s10620-015-3728-3
  9. 9. Parkash O, Hamid S. Are we ready for a new epidemic of under recognized liver disease in South Asia especially in Pakistan? Nonalcoholic fatty liver disease. The Journal of the Pakistan Medical Association. 2013;63:95-99 [PMID: 23865141]
  10. 10. Chan WK, Tan AT, Vethakkan SR, Tah PC, Vijayananthan A, Goh KL. Low physical activity and energy dense Malaysian foods are associated with non-alcoholic fatty liver disease in centrally obese but not in non-centrally obese patients with diabetes mellitus. Asia Pacific Journal of Clinical Nutrition. 2015;24:289-298 [PMID: 26078246]. DOI: 10.6133/apjcn.2015.24.2.15
  11. 11. Rahman MM, Abedin T, Amin R, Rahman MR, Faiz MA. Nonalcoholic fatty liver disease—Is it always benign? Journal of Bangladesh College of Physicians and Surgeons. 2007;25(3):144-152. DOI: 10.3329/jbcps.v25i3.411
  12. 12. Ruhl CE, Everhart JE. Fatty liver indices in the multiethnic United States National Health and Nutrition Examination Survey. Alimentary Pharmacology & Therapeutics. 2015;41:65-76 [PMID: 25376360]. DOI: 10.1111/apt.13012
  13. 13. Munteanu MA, Nagy GA, Mircea PA. Current management of NAFLD. Clujul Medical. 2016;89:19-23. [PMID: 27004021]. DOI: 10.15386/cjmed-539
  14. 14. LaBrecque DR, Abbas Z, Anania F, Ferenci P, Khan AG, Goh KL, Hamid SS, Isakov V, Lizarzabal M, Penaranda MM, Ramos JF, Sarin S, Stimac D, Thomson AB, Umar M, Krabshuis J, LeMair A. World Gastroenterology Organisation global guidelines: Nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Journal of Clinical Gastroenterology. 2014;48:467-473. [PMID: 24921212]. DOI: 10.1097/mcg.0000000000000116
  15. 15. Pandit K, Goswami S, Ghosh S, Mukhopadhyay P, Chowdhury S. Metabolic syndrome in South Asians. Indian Journal of Endocrinology and Metabolism. 2012;16:44-55. [PMID: 22276252]. DOI: 10.4103/2230-8210.91187
  16. 16. United Nations, Department of Economic and Social Affairs, Population Division. World Urbanization Prospects: The 2014 Revision. The United Nations, New York; 2014
  17. 17. Baten J. A History of the Global Economy. Cambridge, UK: Cambridge University Press; 2016
  18. 18. Mahady SE, George J. The future liver of the Asia pacific: Fatter and firmer from more fructose and fortune? Journal of Clinical and Experimental Hepatology. 2013;3:106-113 [PMID: 25755484]. DOI: 10.1016/j.jceh.2012.10.011
  19. 19. Chowdhury A, Younossi ZM. Global epidemiology and risk factors for nonalcoholic fatty liver disease. Alcoholic and Non-Alcoholic Fatty Liver Disease: Springer. 2016:21-40
  20. 20. Alam S, Chowdhury MAB, Azam G, Ahsan M, Mustafa G, Hossain M, Khan M, Ahmed N. Prevalence of fatty liver in Bangladesh: A nation wide population based study. Hepatology International. 2017;11:S553. DOI: 10.1007/s12072-016-9783-9
  21. 21. Hoque MK, AMM, Islam MB. Prevalence of non-alcoholic fatty liver disease in rural population of Bangladesh. Hepatology International. 2017;11:S961. DOI: 10.1007/s12072-016-9783-9
  22. 22. Hoque MI. NAFLD in Bangladesh. Abstract Book 1st Conference of SASL2013. p. 69
  23. 23. Rahman MMKM, Begum H, Haque M, Sultana N, Akhter M. Prevalence and risk factors of nonalcoholic fatty liver disease in a rural Community of South Asia. Gastroenterology Research and Practice. 2015;148:S1045-S1046
  24. 24. Dassanayake AS, Kasturiratne A, Rajindrajith S, Kalubowila U, Chakrawarthi S, De Silva AP, Makaya M, Mizoue T, Kato N, Wickremasinghe AR, de Silva HJ. Prevalence and risk factors for non-alcoholic fatty liver disease among adults in an urban Sri Lankan population. Journal of Gastroenterology and Hepatology. 2009;24:1284-1288 [PMID: 19476560. DOI: 10.1111/j.1440-1746.2009.05831.x
  25. 25. Alam S, Noor EASM, Chowdhury ZR, Alam M, Kabir J. Nonalcoholic steatohepatitis in nonalcoholic fatty liver disease patients of Bangladesh. World Journal of Hepatology. 2013;5:281-287 [PMID: 23717739]. DOI: 10.4254/wjh.v5.i5.281
  26. 26. Wong VW-S, Chitturi S, Wong GL-H, Yu J, Chan HL-Y, Farrell GC. Pathogenesis and novel treatment options for non-alcoholic steatohepatitis. The Lancet Gastroenterology & Hepatology. 2016;1:56-67
  27. 27. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: A spectrum of clinical and pathological severity. Gastroenterology. 1999;116(6):1413-1419 [PMID: 10348825]
  28. 28. Gupte P, Amarapurkar D, Agal S, Baijal R, Kulshrestha P, Pramanik S, Patel N, Madan A, Amarapurkar A. Non-alcoholic steatohepatitis in type 2 diabetes mellitus. Journal of Gastroenterology and Hepatology. 2004;19:854-858
  29. 29. Yilmaz Y, Eren F. A Bayesian approach to an integrated multimodal noninvasive diagnosis of definitive nonalcoholic steatohepatitis in the spectrum of nonalcoholic fatty liver disease. European Journal of Gastroenterology & Hepatology. 2014;26:1292-1295 [PMID: 25171027]. DOI: 10.1097/meg.0000000000000184
  30. 30. Duseja A, Das A, Das R, Dhiman RK, Chawla Y, Bhansali A, Kalra N. The clinicopathological profile of Indian patients with nonalcoholic fatty liver disease (NAFLD) is different from that in the West. Digestive Diseases and Sciences. 2007;52:2368-2374 [PMID: 17420951]. DOI: 10.1007/s10620-006-9136-y
  31. 31. De Hewavisenthi SJ, Dassanayaka AS, De Silva HJ. Clinical, biochemical and histological characteristics of a Sri Lankan population of non-alcoholic steatohepatitis (NASH) patients. The Ceylon Medical Journal. 2005;50:113-116 [PMID: 16252575]
  32. 32. Wong VW, Wong GL, Choi PC, Chan AW, Li MK, Chan HY, Chim AM, Yu J, Sung JJ, Chan HL. Disease progression of non-alcoholic fatty liver disease: A prospective study with paired liver biopsies at 3 years. Gut. 2010;59:969-974. [PMID: 20581244]. DOI: 10.1136/gut.2009.205088
  33. 33. McPherson S, Hardy T, Henderson E, Burt AD, Day CP, Anstee QM. Evidence of NAFLD progression from steatosis to fibrosing-steatohepatitis using paired biopsies: Implications for prognosis and clinical management. Journal of Hepatology. 2015;62:1148-1155 [PMID: 25477264]. DOI: 10.1016/j.jhep.2014.11.034
  34. 34. Sharma M, Mitnala S, Vishnubhotla RK, Mukherjee R, Reddy DN, Rao PN. The riddle of nonalcoholic fatty liver disease: Progression from nonalcoholic fatty liver to nonalcoholic steatohepatitis. Journal of Clinical and Experimental Hepatology. 2015;5:147-158 [PMID: 26155043]. DOI: 10.1016/j.jceh.2015.02.002
  35. 35. Hashimoto E, Tokushige K. Prevalence, gender, ethnic variations, and prognosis of NASH. Journal of Gastroenterology. 2011;46:S63-S69 [PMID: 20844903]. DOI: 10.1007/s00535-010-0311-8
  36. 36. Alam S, Gupta UD, Alam M, Kabir J, Chowdhury ZR, Alam AK. Clinical, anthropometric, biochemical, and histological characteristics of nonobese nonalcoholic fatty liver disease patients of Bangladesh. Indian Journal of Gastroenterology. 2014;33:452-457 [PMID: 25023045]. DOI: 10.1007/s12664-014-0488-5
  37. 37. Majid N, Ali Z, Rahman MR, Akhter A, Rajib RC, Ahmad F, Sharmin S, Akond AK, Huq N. Histological scoring and associated risk factors of non-alcoholic fatty liver disease. Mymensingh Medical Journal. 2013;22:767-772 [PMID: 24292310]
  38. 38. Hossain IA, Akter S, Rahman MK, Ali L. Gender specific association of serum leptin and insulinemic indices with nonalcoholic fatty liver disease in prediabetic subjects. PLoS One. 2015;10:e0142165 [PMID: 26569494]. DOI: 10.1371/journal.pone.0142165
  39. 39. Alam S, Mustafa G, Alam M, Ahmad N. Insulin resistance in development and progression of nonalcoholic fatty liver disease. World Journal of Gastrointestinal Pathophysiology. 2016;7:211-217 [PMID: 27190693]. DOI: 10.4291/wjgp.v7.i2.211
  40. 40. Hossain IA, Rahman Shah MM, Rahman MK, Ali L. Gamma glutamyl transferase is an independent determinant for the association of insulin resistance with nonalcoholic fatty liver disease in Bangladeshi adults: Association of GGT and HOMA-IR with NAFLD. Diabetes and Metabolic Syndrome: Clinical Research and Reviews. 2016;10:S25-S29. [PMID: 26482965]. DOI: 10.1016/j.dsx.2015.09.005
  41. 41. Tandon RK. Emergence of non-alcoholic fatty liver disease (NAFLD). Journal of the Association of Physicians of India. 2013;61:445-446 [PMID: 24772745]
  42. 42. Bhatt SP, Misra A, Nigam P, Guleria R, Pasha MA. Phenotype, body composition, and prediction equations (Indian fatty liver index) for non-alcoholic fatty liver disease in non-diabetic Asian Indians: A case-control study. PLoS One. 2015;10:e0142260 [PMID: 26599361]. DOI: 10.1371/journal.pone.0142260
  43. 43. Praveenraj P, Gomes RM, Kumar S, Karthikeyan P, Shankar A, Parthasarathi R, Senthilnathan P, Rajapandian S, Palanivelu C. Prevalence and predictors of non-alcoholic fatty liver disease in morbidly obese south indian patients undergoing bariatric surgery. Obesity Surgery. 2015;25:2078-2087 [PMID: 25835982]. DOI: 10.1007/s11695-015-1655-1
  44. 44. Puppala J, Bhrugumalla S, Kumar A, Siddapuram SP, Viswa PD, Kondawar M, Akka J, Munshi A. Apolipoprotein C3 gene polymorphisms in Southern Indian patients with nonalcoholic fatty liver disease. Indian Journal of Gastroenterology. 2014;33:524-529 [PMID: 25319715]. DOI: 10.1007/s12664-014-0504-9
  45. 45. Kalra S, Vithalani M, Gulati G, Kulkarni CM, Kadam Y, Pallivathukkal J, Das B, Sahay R, Modi KD. Study of prevalence of nonalcoholic fatty liver disease (NAFLD) in type 2 diabetes patients in India (SPRINT). The Journal of the Association of Physicians of India. 2013;61:448-453 [PMID: 24772746]
  46. 46. Madanagobalane S, Anandan S. The increased prevalence of non-alcoholic fatty liver disease in psoriatic patients: A study from South India. Australian Journal of Dermatology. 2012;53:190-197 [PMID: 22672067]. DOI: 10.1111/j.1440-0960.2012.00905.x
  47. 47. Agarwal AK, Jain V, Singla S, Baruah BP, Arya V, Yadav R, Singh VP. Prevalence of non-alcoholic fatty liver disease and its correlation with coronary risk factors in patients with type 2 diabetes. The Journal of the Association of Physicians of India. 2011;59:351-354 [PMID: 21751587]
  48. 48. Duseja A. Nonalcoholic fatty liver disease in India—A lot done, yet more required! Indian Journal of Gastroenterology. 2010;29:217-225 [PMID: 21191681]. DOI: 10.1007/s12664-010-0069-1
  49. 49. Gaharwar R, Trikha S, Margekar SL, Jatav OP, Ganga PD. Study of clinical profile of patients of nonalcoholic fatty liver disease and its association with metabolic syndrome. The Journal of the Association of Physicians of India. 2015;63:12-16 [PMID: 26591121]
  50. 50. Chaturvedi K, Vohra P. Non-alcoholic fatty liver disease in children. Indian Pediatrics. 2012;49:757-758 [PMID: 23024085]
  51. 51. Kasturiratne A, Weerasinghe S, Dassanayake AS, Rajindrajith S, de Silva AP, Kato N, Wickremasinghe AR, de Silva HJ. Influence of non-alcoholic fatty liver disease on the development of diabetes mellitus. Journal of Gastroenterology and Hepatology. 2013;28:142-147 [PMID: 22989165]. DOI: 10.1111/j.1440-1746.2012.07264.x
  52. 52. Perera N, Indrakumar J, Abeysinghe WV, Fernando V, Samaraweera W, Lawrence JS. Nonalcoholic fatty liver disease increases the mortality from acute coronary syndrome: An observational study from Sri Lanka. BMC Cardiovascular Disorders. 2016;16:1

Written By

Shahinul Alam, Thupten Kelsang Lama, Golam Mustafa, Mahabubul Alam and Nooruddin Ahmad

Submitted: 06 April 2017 Reviewed: 21 September 2017 Published: 20 December 2017