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Clinical Lipidology

ISSN: 1758-4299 (Print) 1758-4302 (Online) Journal homepage: http://www.tandfonline.com/loi/tlip20

High prevalence of non-alcoholic fatty liver disease


(NAFLD) among Gujarati Indians in North London:
a population-based study

Karin Neukam, Sanjay Bhagani, Alison Rodger, Jude Oben, Divyabala Nirmal,
Anjly Jain & Devaki R. Nair

To cite this article: Karin Neukam, Sanjay Bhagani, Alison Rodger, Jude Oben, Divyabala Nirmal,
Anjly Jain & Devaki R. Nair (2017) High prevalence of non-alcoholic fatty liver disease (NAFLD)
among Gujarati Indians in North London: a population-based study, Clinical Lipidology, 12:1, 33-39

To link to this article: https://doi.org/10.1080/17584299.2017.1326709

© 2017 The Author(s). Published by Informa Published online: 25 May 2017.


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Clinical Lipidology, 2017
VOL. 12, NO. 1, 33–39
https://doi.org/10.1080/17584299.2017.1326709

OPEN ACCESS

High prevalence of non-alcoholic fatty liver disease (NAFLD) among Gujarati


Indians in North London: a population-based study
Karin Neukama,b, Sanjay Bhagania, Alison Rodgerc, Jude Obend,e, Divyabala Nirmalh, Anjly Jainf and
Devaki R. Nairf,g
a
Department of Infectious Diseases, Royal Free London NHS Foundation Trust, London, UK; bUnit of Infectious Diseases and Microbiology,
Hospital Universitario de Valme, Seville, Spain; cDepartment of Infection and Population Health, University College London, London, UK;
d
Institute for Liver and Digestive Health, University College London, London, UK; eGuy’s and St Thomas’ Hospital NHS Foundation Trust, London,
UK; fDepartment of Clinical Biochemistry, Royal Free London NHS Foundation Trust, London, UK; gSAS Centre for Cardiovascular Biomarkers,
Royal Free London NHS Foundation Trust, London, UK; hB.A.P.S. Healthcare, Swaminarayan Mandir, London, UK

ABSTRACT ARTICLE HISTORY


Background: The prevalence of non-alcoholic fatty liver disease (NAFLD) among Indian Asians Received 30 December 2016
in high-income countries is not well studied, but appears to be different from that for Western Revised 16 April 2017
populations. Design: Cross-sectional study of subjects recruited through a community cardiovascular Accepted 29 April 2017
(CV) screening programme at two London Hindu temples from 2010–2012. NAFLD was diagnosed KEYWORDS
using the fatty liver index (FLI) and fibrosis stage through the BARD (Body Mass Index (BMI), BARD score; non-alcoholic
Aspartate aminotransferase to Alanine aminotransferase ratio and Diabetes Mellitus) score. Results: fatty liver disease;
597 subjects were assessed; 306 (51%) female. Median (interquartile range) age and BMI were 49 liver fibrosis; aspartate
(40.6–55.0) years and 26.4 (23.5–29.2) kg/m2, respectively. NAFLD was diagnosed in 184 (30.8%) aminotransferase; alanine
cases, but 175 (29.3%) subjects could not be categorised. Overall, 117 (40.2%) men and 67 (21.9%) aminotransferase ratio;
women had evidence of NAFLD (p  <  0.001). In those with evidence of NAFLD, 142 (78.5%) had a Gujarati Indians; screening
BARD score suggestive of advanced fibrosis. Advanced fibrosis could be excluded in 5 (7.6%) women programme; lipids
and 34 (29.6%) men (p < 0.001). Total cholesterol (TC), triglycerides (TG) and non-HDL (high-density
lipoprotein cholesterol) were higher in the NAFLD group (p  <  0.001), whereas HDL-C was lower
(p < 0.001). Conclusion: There is evidence of a high prevalence of asymptomatic NAFLD, possibly
in combination with advanced liver damage, among UK-based Gujarati Indians living in London.
NAFLD is emerging as an independent risk factor for CV disease. Screening programmes should be
developed in order to decrease liver and CV mortality and morbidity in these high-risk patients.

Introduction
with NAFLD has been shown to increase cardiovascular
Over the last two decades, non-alcoholic fatty liver dis- (CV) risk; the possible mechanisms include oxidative stress,
ease (NAFLD) has become an increasingly diagnosed insulin resistance, inflammation, cytokines and endothelial
cause of liver disease particularly in Western countries abnormalities [4,7]. In 2012, the UK Chief Medical Officer
[1]. Depending on the population studied and the diag- highlighted the rising tide of serious liver disease in the
nostic method used, the estimated overall prevalence of UK caused by NAFLD [8].
NAFLD ranges from 6 to 35%, thus representing the com- NAFLD is recognised to be the main hepatic manifesta-
monest cause of hepatic disease [2,3] but there are also tion of the MetS and the principal risk factors for NAFLD are
studies mentioning NAFLD with a much higher prevalence obesity, type 2 diabetes mellitus, insulin resistance, hyperg-
(up to 100%) in populations with pre-existing metabolic lycaemia and hypertriglyceridaemia [2]. NAFLD is also seen
conditions characterised by insulin resistance (IR) such as in individuals with normal body mass index (BMI) who do
obesity, metabolic syndrome (MetS) or type 2 diabetes not necessarily have insulin resistance associated meta-
mellitus (T2DM) [4,5]. NAFLD can result in non-alcoholic bolic disorders [9,10]. Age, gender and lifestyle measures
steatohepatitis which may progress over a variable period, also impact on the prevalence of NAFLD [2,3,6] and a num-
in 25–40% patients to significant fibrosis, liver cirrhosis and ber of epidemiological studies clearly show an impact of
hepatocellular carcinoma [3,6]. Dyslipidaemia associated ethnic origin with a suggestion in some studies that Asian

CONTACT  Devaki R. Nair  Devaki.Nair@nhs.net


© 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
34   K. NEUKAM ET AL.

Indians are at an increased risk for NAFLD [10–13]. Thus, A negative predictive value of 96% was determined for
liver biopsy and/or ultrasound-based studies on NAFLD this index [21].
conducted in India have reported a prevalence ranging
from 9 to 32% [9–12] according to regional differences
Statistical analysis
and social status [10]. These numbers are similar to NAFLD
prevalence reported in other countries [3]. However, some Descriptive and inferential statistical analyses were per-
studies suggest that Indians have higher grade histological formed using SPSS 19.0 (IBM Corporation, Somers, NY, USA)
abnormalities and a different clinicopathological profile and STATA 9.0 (Stata Corp LP, College Station, TX, USA).
compared with Caucasian, Hispanics or African-American Data were checked for normality using histogram and
subjects [14,15]. Studies have suggested that Asian immi- scatterplots. Categorical variables were evaluated using
grants are at increased risk of NAFLD as compared with chi-square test or Fisher’s exact tests and continuous var-
their western counterparts [16,17]. iables were compared using the Mann–Whitney U-test or
There is limited data on the prevalence of NAFLD in the Student t-test, when applicable. The 95% confidence
those of Indian Asian ethnicity living in the Western coun- intervals (CI) were calculated for the prevalence of NAFLD
tries, and especially in the UK. The aim of this communi- and advanced fibrosis. All reported p values are two-sided
ty-based study was to describe the prevalence of NAFLD and a p < 0.05 was deemed significant.
among a cohort of first and second generation British
Indians of Gujarati origin residing in North London.
Results
Study population characteristics
Methods
Data from 597 sequentially recruited individuals from
Design, setting and subjects
2010 to 2012 were analysed; 306 (51.3%) were female.
This is a retrospective analysis on cross-sectional data rou- Three hundred and eighty-three (64.2%) subjects had a
tinely collected as part of a community cardiovascular risk BMI of ≥25  kg/m2 and 479 (80.2%) a BMI of ≥23  kg/m2.
programme conducted by the Healthy Hearts Team [18]. The aspartate aminotransferase (AST)/alanine aminotrans-
The cardiovascular screening programme was carried out ferase (ALT) ratio was >2 in 29 (4.9%) individuals and <1 in
in two Hindu temples (BAPS, Shri Swaminarayan Mandir, 181 (30.5%) subjects, respectively. The main characteris-
Neasden, London NW10 8LD, UK and Shri Swaminarayan tics of the study population are presented in Table 1. The
Temple, Willesden, London NW2 5RG, UK), situated in the presence and absence of DM form a part of the score so
borough of Brent in Greater London which has a 64% individuals with DM were not excluded.
ethnic minority population and 18% are of Indian origin Only 6.5% (39 individuals) of the above cohort consumed
[19]. The congregations of the temples (several thousand) alcohol. Of the 39 individuals who consumed alcohol, the
were mostly Gujaratis. The uptake of screening in our majority (36) consumed 7 units or less of alcohol per week.
programme was high and representative of single com- Of the remaining, 2 had intakes of >21 units/week.
munity [18]. A detailed description of the cardiovascular
programme and data collection has been previously pub-
Prevalence of NAFLD and advanced fibrosis
lished [18].
In the overall population, NAFLD was diagnosed in 30.8%
(184/597), with 39.9% (238/597) screening negative. A
Measurement of NAFLD and fibrosis stage
further 29.3% (175/597) were unable to be categorised
The prevalence of NAFLD was determined by the fatty by applying the FLI. The prevalence of NAFLD according
liver index (FLI) [20]. The mathematical equation on which to the gender is shown in Figure 1. Of those characterised
this index is based includes the BMI, plasma gamma-glu- as having NAFLD, 142 (78.5%; 95% CI: 71.7–84.2%) had a
tamyl transferase (gGT) and triglyceride levels, as well as BARD score >1 suggestive of advanced fibrosis. Evidence
waist circumference measurements. FLI score <30 “rules for advanced fibrosis was detected in 61 (92.4%) of the
out” NAFLD, while a score >60 “rules in” NAFLD. Subjects females and 81 (70.4%) of the male individuals [odds ratio
presenting a score of 30–60 are “unclassified”. In those (95% CI): 5.12 (1.89–13.9); p = 0.001]. The corresponding
subjects in whom NAFLD was diagnosed, the BARD index figures for the subpopulation with elevated ALT levels
(BMI, AST/ALT ratio and Diabetes Mellitus index) was cal- (>19  IU/L for females and >31  IU/L for males) were: 12
culated to evaluate the fibrosis stage [21]. A BARD score (10.4%) for females and 34 (52.3%) for males [odds ratio
from between 0 and 1 is indicative of absence of significant 9.41; 95% CI: 4.36–20.4); p < 0.001]. The BARD index could
fibrosis, while a score of 2–4 suggests advanced fibrosis. not be calculated in 3 (1.6%) individuals.
CLINICAL LIPIDOLOGY   35

Table 1. Characteristics of the study population (n = 597).


Parameter Overall population Female n = 306 Male n = 291 p (comparing females vs. males)
Age (years)* 49.0 (40.6–55.0) 49.7 (41.0–55.3) 48.8 (39.2–55.0) 0.215
Body mass index (kg/m2)* 26.4 (29.2–23.5) 26.6 (23.4–30) 26.3 (23.6–29.0) 0.623
Skeletal muscle mass (kg)¥* 22.9 (19.4–28.5) 19.6 (17.9–21.4) 28.5 (25.9–31.4) <0.001
Body fat mass (kg)¥* 24.8 (19.2–30.8) 26.7 (20.9–32.7) 22.5 (17.5–27.9) <0.001
Body fat (%)¥* 35.8 (28.8–43.2) 42.4 (36.3–46.9) 30.3 (25.9–35.2) <0.001
Waist circumference (cm)* 91 (85–99) 87 (80–94) 94 (89–102) <0.001
HbA1c (%)†* 5.6 (5.3–5.8) 5.5 (5.3–5.8) 5.6 (5.4–5.9) 0.255
Systolic BP (mmHg)¶* 130 (117–144) 127 (112–141) 132 (121–145) <0.001
Diastolic BP (mmHg)¶* 82 (74–90) 79 (72–87) 84 (76–91) <0.001
Total cholesterol (mmol/L)** 4.9 (1.0) 4.8 (0.9) 5.0 (1.0) 0.009
HDL cholesterol (mmol/L)#** 1.3 (0.4) 1.4 (0.3) 1.2 (0.4) 0.000
LDL cholesterol (mmol/L)±** 2.8 (0.8) 2.7 (0.8) 2.9 (0.9) 0.002
Triglycerides (mmol/L)** 1.8 (1.1) 1.5 (0.9) 2.1 (1.3) 0.000
Non-HDL cholesterol (mmol/l)** 3.6 (1.0) 3.4 (0.9) 3.8 (1.0) 0.000
AST (IU/L)§* 22 (20–27) 21 (18–25) 24 (21–28) <0.001
ALT (IU/L)$* 20 (15–26) 16.5 (13–21) 23 (18–30) <0.001
AST/ALT ratio* 1.1 (0.9–1.4) 1.3 (1.1–1.5) 1 (0.8–1.2) <0.001
gGT (IU/L)‡* 16 (12–23) 14 (11–18) 20 (15–27) <0.001
*
Median (interquartile range); **Mean (standard deviation); ¥Determined by bioelectrical impedance body fat measurement; †HbA1c: glycosylated haemoglobin;

BP: blood pressure; #HDL: high-density lipoprotein; ±LDL: low-density lipoprotein; §AST: aspartate aminotransferase; $ALT: alanine aminotransferase; ‡gGT: gamma-
glutamyl transferase.

Figure 1. Prevalence of non-alcoholic fatty liver disease (NAFLD) as determined by the fatty liver index (FLI).
Notes: Light bars: presence of NAFLD (FLI > 60); black bars: absence of NAFLD (FLI < 30); checked area: absence of advanced fibrosis, defined as BARD (Body
Mass Index, AST/ALT ratio and Diabetes Mellitus-index 2–4), among those patients with NAFLD. In 72 (23.5%) of the female and 103 (35.4%) of the male subjects,
presence or absence of NAFLD could not be characterised by FLI. The p-value for presence of NAFLD comparing male and female subjects was <0.001.

Lipid levels Discussion


We compared total cholesterol (TC), high-density lipopro- This study is the first to report the prevalence of NAFLD in
tein cholesterol (HDL-C), triglycerides (TG) and non-HDL-C a Gujarati Indian community setting in the UK. The high
(TC–HDL-C) in individuals with and without NAFLD. TC, TG prevalence of NAFLD (ie 30.8%) we found among the
and non-HDL-C were higher (p < 0.001), whereas HDL-C Gujarati Indian population of North London is alarming
was lower (p < 0.001) in the NAFLD group (Table 2). Within and indicates a need for detailed characterisation and
the NAFLD group, the individuals with advanced fibrosis assessment for NAFLD in this population. This could allow
using BARD scoring had lower levels of TC (p  =  0.008), intervention on potentially modifiable risk factors associ-
HDL-C (p = 0.403), TG (p = 0.160) and non-HDL-C (p = 0.029) ated with the MetS and NAFLD. It should be noted that
(Table 3). NAFLD is generally asymptomatic in the early stages [4].
36   K. NEUKAM ET AL.

Table 2. Lipid levels in individuals with and without NAFLD.


Lipid parameters Individuals without NAFLD^ n = 238 Individuals with NAFLD^ n = 184 p
Total cholesterol (mmol/l)* 4.8 (0.9) 5.1 (1.0) <0.001
HDL cholesterol (mmol/l)* 1.4 (0.3) 1.2 (0.4) <0.001
Triglycerides (mmol/l)* 1.2 (0.5) 2.6 (1.4) <0.001
Non-HDL cholesterol (mmol/l)* 3.3 (0.9) 3.9 (1.2) <0.001
*
Mean (sd), HDL: high-density lipoprotein; ^Non-alcoholic fatty liver disease.

Table 3. Lipid levels in individuals with and without fibrosis (as per BARD Score) in the NAFLD^ group.
Lipid parameters Individuals without fibrosis Individuals with fibrosis p
Total cholesterol (mmol/l)* 5.6 (1.2) 5.1 (0.9) 0.008
HDL cholesterol (mmol/l)* 1.2 (0.7) 1.1 (0.3) 0.403
Triglycerides (mmol/l)* 2.9 (1.6) 2.5 (1.4) 0.160
Non-HDL cholesterol (mmol/l)* 4.3 (1.4) 3.9 (0.9) 0.029
*
Mean (sd), HDL: high-density lipoprotein; ^Non-alcoholic fatty liver disease.

In this cohort, 15% of the subjects had a 10-year cardi- Nevertheless, this study clearly shows that NAFLD is
ovascular risk >20% [18] and almost all participants (92%) present in 30% of this population that are at risk of NAFLD
had at least one risk factor for cardiovascular disease [18] due to the reported high prevalence of factors associated
including obesity, MetS or DM [18]. These factors have been with the MetS [18]. Furthermore, advanced fibrosis could
identified as key risk factors for NAFLD both in Western only be excluded in as little as 8% of the female and 30%
populations and those living in India [10–12]. Lifestyle [22] of the male population. Thus, more accurate diagnostic
and dietary factors have also been shown to be important methods such as transient elastography [31] or liver biopsy
in subjects living in India with total calorie intake, per cent may be needed to further assess the prevalence of NAFLD
of carbohydrate and fat intake of NAFLD cases being sig- and liver fibrosis in this population. However, a previous
nificantly higher than controls in one study [23]. Increased study found that an AST/ALT ratio <1 is associated with
income was also associated with a greater prevalence of non-alcoholic steatohepatitis (NASH), while an AST/ALT
NAFLD in another Indian study [10]. However, NAFLD is not ratio >2 is associated with alcoholic steatohepatitis [32].
limited to the prosperous sections of Indian society or only Approximately one-third of subjects in this study had an
seen in those who are overweight [10,13], although it is rec- AST/ALT ratio <1 and only 5% showed an AST/ALT ratio >2,
ognised that Asians have an increased body fat compared thus making alcohol consumption as a cause for fatty liver
with Europeans even at the same BMI [24]. In this context, a disease in this population unlikely [32]. Furthermore, alco-
study involving almost 2000 subjects living in a rural region hol consumption is absent or minimal in this population
of East India reported that the only 25% of subjects with for traditional religious reasons.
NAFLD had a BMI in the obese range but 39% had abdom- In addition to liver disease, patients with NAFLD have
inal obesity which is associated with NAFLD [10]. an increased mortality compared with the general pop-
The prevalence of NAFLD described in this study is ulation primarily related to CVD or malignancy [33,34].
higher than that reported in previous studies conducted in The pathogenesis of dyslipidaemia in NAFLD is likely
populations living in India [10–13]. This may be the result related to imbalance between production/clearance of
of a combination of genetic predisposition among Indian the lipoproteins like hepatic FFA (free fatty acid) from
Asians to develop NAFLD and a change in lifestyle associ- the circulation [34,35]. This results in liver accumulation
ated with high calorie consumption and reduced physical of TG predisposing to fatty liver. The FFAs and its deriv-
activity in the Western world [23,25–28]. atives are mainly responsible for lipotoxicity and the
Indian heritage comprised approximately 2.5% of the resultant liver injury [35]. In the recent years, a better
population in the UK in 2011 [29]. In addition 2.6% are from understanding of the pathogenesis has resulted in the
Pakistan and Bangladesh, whose cardiovascular risk, risk discovery of medical therapies targeting various aspects
for diabetes and MetS are shown to be higher than the of TG deposition and hepatocellular injury. Medications
people of Indian origin [29]. Therefore, the future impact like peroxisome proliferator–activator receptors (PPARs),
of NAFLD in terms of progressive liver disease is of public volixbat, are targeted to reduce hepatic fat accumulation
health concern for the UK. and metabolic stress. Agents like vitamin E, pentoxifyl-
A higher prevalence of NAFLD in men than women was line and PXS-4728A are aimed at reducing inflamma-
observed in this study, which is in keeping with previously tion and injury associated with oxidative stress [35].
published findings [10,13,28,30]. With regard to lipid lowering agents, statins are safe in
CLINICAL LIPIDOLOGY   37

NAFLD (35–37). Statins not only improve dyslipidaemia address this important health issue to prevent future mor-
but are also associated with a decreased risk of NASH bidity and mortality, not only from the associated cardio-
and advanced fibrosis [36,37]. Rosuvastatin monother- vascular disease but also from severe liver disease.
apy was associated with resolution of NASH, regression
of MetS, reduction in plasma glucose and serum uric acid
Competing interests
levels. These results suggest a decreased risk of vascular
and liver morbidity and mortality-related NAFLD/NASH DRN has received grants from Pfizer (Pfizer Foundation
[38]. There is an interest in the role of ezetimibe, not only award 2008), Solvay, Merck Sharp & Dohme and Astra
in reducing cardiovascular risk but also in improvement Zeneca for this service (see funding below). DRN has
of biochemical markers of NAFLD and reduction in advisory board membership for Merck Sharp & Dohme,
hepatic steatosis [39]. Sanofi and Amgen. DRN is a speaker for Merck Sharp &
Combination drug therapy could be more effective Dohme, Sanofi and Amgen. KN is the recipient of a Miguel
in terms of NAFLD/NASH. Combining a potent statin (ie Servet research grant from the Instituto de Salud Carlos
atorvastatin and rosuvastatin)  with liraglutide has been III (grant number CP13/00187) and received lecture fees
suggested to maximise beneficial effects on liver and CVD from Merck. SB have served on Advisory Boards and been
morbidity and mortality in T2DM patients with NAFLD/ on the speaker bureau for Merck Sharp & Dohme. AR has
NASH [40]. received unrestricted grant from Gilead. AJ, JO and DN,
Glucagon like peptide 1(GLP1) analogues and Sodium– have no competing interests to disclose.
glucose co-transporter 2 (SGLT2) inhibitors alone or in
combination might have a beneficial effect on NASH pro-
Ethical approval
gression This may improve CVD-related morbidity and
mortality, as well as liver-related morbidity in patients Ethics approval was obtained from NHS Health Research
with NASH [41]. Authority Research Ethics Committee (REC reference: 13/
Drugs targeting gut microbial lipopolysaccharide (LPS) NW/0070).
which has been implicated as one of the mechanism of
liver injury for NAFLD are currently being evaluated in
Guarantor
clinical trials [35].
Although risk factors for progressive liver disease in DRN
the context of NAFLD are poorly characterised, there is
no doubt that the MetS contributes to the progression in
Contributors
liver inflammation [34]. Therefore, some of the measures
above, particularly weight loss and diabetes control may DRN developed the proposal for the outreach clinic and is
well have a protective effect in terms of hepatic disease the lead for the project. KN, SB and AJ planned the analysis,
progression [42,43]. drafted the paper, SB, AR, JO and DRN edited the paper.
The limitation of this community-based study is that DRN, AJ, DN, were responsible for the implementation of
only non-invasive algorithms, using a combination of blood the study and acquisition of data. All the authors gave their
biomarkers and anthropometric measures, were available intellectual input towards the preparation of manuscript
to evaluate NAFLD and fibrosis staging. This ­limitation may and approved the final version.
have over or underestimated the true prevalence. Although
the tests used in this study have been extensively validated
Acknowledgements
[20,21], approximately one-third of the population could
not be categorised by means of the FLI, suggesting that the We thank the staff of BAPS Swaminarayan Mandir, Neasden, for
prevalence of NAFLD could be even higher in this popula- their support.
tion. Additionally, while the BARD score reliably excludes
the presence of advanced fibrosis, its positive predictive Disclosure statement
value remains suboptimal [21].
No potential conflict of interest was reported by the authors.

Conclusion
Funding
Our data suggest a very high prevalence of NAFLD among
The study was financially supported by the Pfizer Foundation
the Gujarati Indian community living in North London, award 2008, Pfizer UK. We also received unrestricted educa-
with evidence of significant liver damage. Screening pro- tional grants from MSD, Solvay and AstraZeneca. The design
grammes are urgently needed to fully characterise and and conduct of the service and the analysis, interpretation and
38   K. NEUKAM ET AL.

presentation of the data were solely the responsibility of the au- [15] Duseja A, Das A, Das R, et al. The clinicopathological profile
thors. DRN has received grants from Pfizer (Pfizer Foundation of Indian patients with nonalcoholic fatty liver disease
award 2008), Solvay, Merck Sharp & Dohme, and Astra Zeneca (NAFLD) is different from that in the West. Dig Dis Sci.
for this service (see funding below). DRN has advisory board 2007;52:2368–2374.
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