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
Over the last two decades, non-alcoholic fatty liver dis-
ease (NAFLD) has become an increasingly diagnosed
cause of liver disease particularly in Western countries
[1]. Depending on the population studied and the diag-
nostic method used, the estimated overall prevalence of
NAFLD ranges from 6 to 35%, thus representing the com-
monest cause of hepatic disease [2,3] but there are also
studies mentioning NAFLD with a much higher prevalence
(up to 100%) in populations with pre-existing metabolic
conditions characterised by insulin resistance (IR) such as
obesity, metabolic syndrome (MetS) or type 2 diabetes
mellitus (T2DM) [4,5]. NAFLD can result in non-alcoholic
steatohepatitis which may progress over a variable period,
in 25–40% patients to significant fibrosis, liver cirrhosis and
hepatocellular carcinoma [3,6]. Dyslipidaemia associated
with NAFLD has been shown to increase cardiovascular
(CV) risk; the possible mechanisms include oxidative stress,
insulin resistance, inflammation, cytokines and endothelial
abnormalities [4,7]. In 2012, the UK Chief Medical Officer
highlighted the rising tide of serious liver disease in the
UK caused by NAFLD [8].
NAFLD is recognised to be the main hepatic manifesta-
tion of the MetS and the principal risk factors for NAFLD are
obesity, type 2 diabetes mellitus, insulin resistance, hyperg-
lycaemia and hypertriglyceridaemia [2]. NAFLD is also seen
in individuals with normal body mass index (BMI) who do
not necessarily have insulin resistance associated meta-
bolic disorders [9,10]. Age, gender and lifestyle measures
also impact on the prevalence of NAFLD [2,3,6] and a num-
ber of epidemiological studies clearly show an impact of
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
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34   K. NEUKAM ET AL.
Indians are at an increased risk for NAFLD [10–13]. Thus,
liver biopsy and/or ultrasound-based studies on NAFLD
conducted in India have reported a prevalence ranging
from 9 to 32% [9–12] according to regional differences
and social status [10]. These numbers are similar to NAFLD
prevalence reported in other countries [3]. However, some
studies suggest that Indians have higher grade histological
abnormalities and a different clinicopathological profile
compared with Caucasian, Hispanics or African-American
subjects [14,15]. Studies have suggested that Asian immi-
grants are at increased risk of NAFLD as compared with
their western counterparts [16,17].
There is limited data on the prevalence of NAFLD in
those of Indian Asian ethnicity living in the Western coun-
tries, and especially in the UK. The aim of this communi-
ty-based study was to describe the prevalence of NAFLD
among a cohort of first and second generation British
Indians of Gujarati origin residing in North London.
Methods
Design, setting and subjects
This is a retrospective analysis on cross-sectional data rou-
tinely collected as part of a community cardiovascular risk
programme conducted by the Healthy Hearts Team [18].
The cardiovascular screening programme was carried out
in two Hindu temples (BAPS, Shri Swaminarayan Mandir,
Neasden, London NW10 8LD, UK and Shri Swaminarayan
Temple, Willesden, London NW2 5RG, UK), situated in the
borough of Brent in Greater London which has a 64%
ethnic minority population and 18% are of Indian origin
[19]. The congregations of the temples (several thousand)
were mostly Gujaratis. The uptake of screening in our
programme was high and representative of single com-
munity [18]. A detailed description of the cardiovascular
programme and data collection has been previously pub-
lished [18].
Measurement of NAFLD and fibrosis stage
The prevalence of NAFLD was determined by the fatty
liver index (FLI) [20]. The mathematical equation on which
this index is based includes the BMI, plasma gamma-glu-
tamyl transferase (gGT) and triglyceride levels, as well as
waist circumference measurements. FLI score <30 “rules
out” NAFLD, while a score >60 “rules in” NAFLD. Subjects
presenting a score of 30–60 are “unclassified”. In those
subjects in whom NAFLD was diagnosed, the BARD index
(BMI, AST/ALT ratio and Diabetes Mellitus index) was cal-
culated to evaluate the fibrosis stage [21]. A BARD score
from between 0 and 1 is indicative of absence of significant
fibrosis, while a score of 2–4 suggests advanced fibrosis.
A negative predictive value of 96% was determined for
this index [21].
Statistical analysis
Descriptive and inferential statistical analyses were per-
formed using SPSS 19.0 (IBM Corporation, Somers, NY, USA)
and STATA 9.0 (Stata Corp LP, College Station, TX, USA).
Data were checked for normality using histogram and
scatterplots. Categorical variables were evaluated using
chi-square test or Fisher’s exact tests and continuous var-
iables were compared using the Mann–Whitney U-test or
the Student t-test, when applicable. The 95% confidence
intervals (CI) were calculated for the prevalence of NAFLD
and advanced fibrosis. All reported p values are two-sided
and a p < 0.05 was deemed significant.
Results
Study population characteristics
Data from 597 sequentially recruited individuals from
2010 to 2012 were analysed; 306 (51.3%) were female.
Three hundred and eighty-three (64.2%) subjects had a
BMI of ≥25  kg/m2 and 479 (80.2%) a BMI of ≥23  kg/m2.
The aspartate aminotransferase (AST)/alanine aminotrans-
ferase (ALT) ratio was >2 in 29 (4.9%) individuals and <1 in
181 (30.5%) subjects, respectively. The main characteris-
tics of the study population are presented in Table 1. The
presence and absence of DM form a part of the score so
individuals with DM were not excluded.
Only 6.5% (39 individuals) of the above cohort consumed
alcohol. Of the 39 individuals who consumed alcohol, the
majority (36) consumed 7 units or less of alcohol per week.
Of the remaining, 2 had intakes of >21 units/week.
Prevalence of NAFLD and advanced fibrosis
In the overall population, NAFLD was diagnosed in 30.8%
(184/597), with 39.9% (238/597) screening negative. A
further 29.3% (175/597) were unable to be categorised
by applying the FLI. The prevalence of NAFLD according
to the gender is shown in Figure 1. Of those characterised
as having NAFLD, 142 (78.5%; 95% CI: 71.7–84.2%) had a
BARD score >1 suggestive of advanced fibrosis. Evidence
for advanced fibrosis was detected in 61 (92.4%) of the
females and 81 (70.4%) of the male individuals [odds ratio
(95% CI): 5.12 (1.89–13.9); p = 0.001]. The corresponding
figures for the subpopulation with elevated ALT levels
(>19  IU/L for females and >31  IU/L for males) were: 12
(10.4%) for females and 34 (52.3%) for males [odds ratio
9.41; 95% CI: 4.36–20.4); p < 0.001]. The BARD index could
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-
tein cholesterol (HDL-C), triglycerides (TG) and non-HDL-C
(TC–HDL-C) in individuals with and without NAFLD. TC, TG
and non-HDL-C were higher (p < 0.001), whereas HDL-C
was lower (p < 0.001) in the NAFLD group (Table 2). Within
the NAFLD group, the individuals with advanced fibrosis
using BARD scoring had lower levels of TC (p  =  0.008),
HDL-C (p = 0.403), TG (p = 0.160) and non-HDL-C (p = 0.029)
(Table 3).
This study is the first to report the prevalence of NAFLD in
a Gujarati Indian community setting in the UK. The high
prevalence of NAFLD (ie 30.8%) we found among the
Gujarati Indian population of North London is alarming
and indicates a need for detailed characterisation and
assessment for NAFLD in this population. This could allow
intervention on potentially modifiable risk factors associ-
ated with the MetS and NAFLD. It should be noted that
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
Total cholesterol (mmol/l)*
HDL cholesterol (mmol/l)*
Triglycerides (mmol/l)*
Non-HDL cholesterol (mmol/l)*
*
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
Total cholesterol (mmol/l)*
HDL cholesterol (mmol/l)*
Triglycerides (mmol/l)*
Non-HDL cholesterol (mmol/l)*
*
Mean (sd), HDL: high-density lipoprotein; ^Non-alcoholic fatty liver disease.
In this cohort, 15% of the subjects had a 10-year cardi-
ovascular risk >20% [18] and almost all participants (92%)
had at least one risk factor for cardiovascular disease [18]
including obesity, MetS or DM [18]. These factors have been
identified as key risk factors for NAFLD both in Western
populations and those living in India [10–12]. Lifestyle [22]
and dietary factors have also been shown to be important
in subjects living in India with total calorie intake, per cent
of carbohydrate and fat intake of NAFLD cases being sig-
nificantly higher than controls in one study [23]. Increased
income was also associated with a greater prevalence of
NAFLD in another Indian study [10]. However, NAFLD is not
limited to the prosperous sections of Indian society or only
seen in those who are overweight [10,13], although it is rec-
ognised that Asians have an increased body fat compared
with Europeans even at the same BMI [24]. In this context, a
study involving almost 2000 subjects living in a rural region
of East India reported that the only 25% of subjects with
NAFLD had a BMI in the obese range but 39% had abdom-
inal obesity which is associated with NAFLD [10].
The prevalence of NAFLD described in this study is
higher than that reported in previous studies conducted in
populations living in India [10–13]. This may be the result
of a combination of genetic predisposition among Indian
Asians to develop NAFLD and a change in lifestyle associ-
ated with high calorie consumption and reduced physical
activity in the Western world [23,25–28].
Indian heritage comprised approximately 2.5% of the
population in the UK in 2011 [29]. In addition 2.6% are from
Pakistan and Bangladesh, whose cardiovascular risk, risk
for diabetes and MetS are shown to be higher than the
people of Indian origin [29]. Therefore, the future impact
of NAFLD in terms of progressive liver disease is of public
health concern for the UK.
A higher prevalence of NAFLD in men than women was
observed in this study, which is in keeping with previously
published findings [10,13,28,30].
Individuals with NAFLD^ n = 184 p
4.8 (0.9) 5.1 (1.0) <0.001
1.4 (0.3) 1.2 (0.4) <0.001
1.2 (0.5) 2.6 (1.4) <0.001
3.3 (0.9) 3.9 (1.2) <0.001
Individuals with fibrosis p
5.6 (1.2) 5.1 (0.9) 0.008
1.2 (0.7) 1.1 (0.3) 0.403
2.9 (1.6) 2.5 (1.4) 0.160
4.3 (1.4) 3.9 (0.9) 0.029
Nevertheless, this study clearly shows that NAFLD is
present in 30% of this population that are at risk of NAFLD
due to the reported high prevalence of factors associated
with the MetS [18]. Furthermore, advanced fibrosis could
only be excluded in as little as 8% of the female and 30%
of the male population. Thus, more accurate diagnostic
methods such as transient elastography [31] or liver biopsy
may be needed to further assess the prevalence of NAFLD
and liver fibrosis in this population. However, a previous
study found that an AST/ALT ratio <1 is associated with
non-alcoholic steatohepatitis (NASH), while an AST/ALT
ratio >2 is associated with alcoholic steatohepatitis [32].
Approximately one-third of subjects in this study had an
AST/ALT ratio <1 and only 5% showed an AST/ALT ratio >2,
thus making alcohol consumption as a cause for fatty liver
disease in this population unlikely [32]. Furthermore, alco-
hol consumption is absent or minimal in this population
for traditional religious reasons.
In addition to liver disease, patients with NAFLD have
an increased mortality compared with the general pop-
ulation primarily related to CVD or malignancy [33,34].
The pathogenesis of dyslipidaemia in NAFLD is likely
related to imbalance between production/clearance of
the lipoproteins like hepatic FFA (free fatty acid) from
the circulation [34,35]. This results in liver accumulation
of TG predisposing to fatty liver. The FFAs and its deriv-
atives are mainly responsible for lipotoxicity and the
resultant liver injury [35]. In the recent years, a better
understanding of the pathogenesis has resulted in the
discovery of medical therapies targeting various aspects
of TG deposition and hepatocellular injury. Medications
like peroxisome proliferator–activator receptors (PPARs),
volixbat, are targeted to reduce hepatic fat accumulation
and metabolic stress. Agents like vitamin E, pentoxifyl-
line and PXS-4728A are aimed at reducing inflamma-
tion and injury associated with oxidative stress [35].
With regard to lipid lowering agents, statins are safe in

NAFLD (35–37). Statins not only improve dyslipidaemia
but are also associated with a decreased risk of NASH
and advanced fibrosis [36,37]. Rosuvastatin monother-
apy was associated with resolution of NASH, regression
of MetS, reduction in plasma glucose and serum uric acid
levels. These results suggest a decreased risk of vascular
and liver morbidity and mortality-related NAFLD/NASH
[38]. There is an interest in the role of ezetimibe, not only
in reducing cardiovascular risk but also in improvement
of biochemical markers of NAFLD and reduction in
hepatic steatosis [39].
Combination drug therapy could be more effective
in terms of NAFLD/NASH. Combining a potent statin (ie
atorvastatin and rosuvastatin)  with liraglutide has been
suggested to maximise beneficial effects on liver and CVD
morbidity and mortality in T2DM patients with NAFLD/
NASH [40].
Glucagon like peptide 1(GLP1) analogues and Sodium–
glucose co-transporter 2 (SGLT2) inhibitors alone or in
combination might have a beneficial effect on NASH pro-
gression This may improve CVD-related morbidity and
mortality, as well as liver-related morbidity in patients
with NASH [41].
Drugs targeting gut microbial lipopolysaccharide (LPS)
which has been implicated as one of the mechanism of
liver injury for NAFLD are currently being evaluated in
clinical trials [35].
Although risk factors for progressive liver disease in
the context of NAFLD are poorly characterised, there is
no doubt that the MetS contributes to the progression in
liver inflammation [34]. Therefore, some of the measures
above, particularly weight loss and diabetes control may
well have a protective effect in terms of hepatic disease
progression [42,43].
The limitation of this community-based study is that
only non-invasive algorithms, using a combination of blood
biomarkers and anthropometric measures, were available
to evaluate NAFLD and fibrosis staging. This ­limitation may
have over or underestimated the true prevalence. Although
the tests used in this study have been extensively validated
[20,21], approximately one-third of the population could
not be categorised by means of the FLI, suggesting that the
prevalence of NAFLD could be even higher in this popula-
tion. Additionally, while the BARD score reliably excludes
the presence of advanced fibrosis, its positive predictive
value remains suboptimal [21].
Conclusion
Our data suggest a very high prevalence of NAFLD among
the Gujarati Indian community living in North London,
with evidence of significant liver damage. Screening pro-
grammes are urgently needed to fully characterise and
CLINICAL LIPIDOLOGY   37
address this important health issue to prevent future mor-
bidity and mortality, not only from the associated cardio-
vascular disease but also from severe liver disease.
Competing interests
DRN has received grants from Pfizer (Pfizer Foundation
award 2008), Solvay, Merck Sharp & Dohme and Astra
Zeneca for this service (see funding below). DRN has
advisory board membership for Merck Sharp & Dohme,
Sanofi and Amgen. DRN is a speaker for Merck Sharp &
Dohme, Sanofi and Amgen. KN is the recipient of a Miguel
Servet research grant from the Instituto de Salud Carlos
III (grant number CP13/00187) and received lecture fees
from Merck. SB have served on Advisory Boards and been
on the speaker bureau for Merck Sharp & Dohme. AR has
received unrestricted grant from Gilead. AJ, JO and DN,
have no competing interests to disclose.
Ethical approval
Ethics approval was obtained from NHS Health Research
Authority Research Ethics Committee (REC reference: 13/
NW/0070).
Guarantor
DRN
Contributors
DRN developed the proposal for the outreach clinic and is
the lead for the project. KN, SB and AJ planned the analysis,
drafted the paper, SB, AR, JO and DRN edited the paper.
DRN, AJ, DN, were responsible for the implementation of
the study and acquisition of data. All the authors gave their
intellectual input towards the preparation of manuscript
and approved the final version.
Acknowledgements
We thank the staff of BAPS Swaminarayan Mandir, Neasden, for
their support.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
The study was financially supported by the Pfizer Foundation
award 2008, Pfizer UK. We also received unrestricted educa-
tional grants from MSD, Solvay and AstraZeneca. The design
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
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is a speaker for Merck Sharp & Dohme, Sanofi and Amgen. KN is distribution of nonalcoholic fatty liver in persons with
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[18] Rao N, Eastwood SV, Jain A, et al. Cardiovascular risk
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