Diabetes in Asia and the Pacific: Implications for the ...care.diabetesjournals.org/content/diacare/39/3/472.full.pdf · Diabetes in Asia and the Pacific: Implications for the Global

Diabetes in Asia and the Pacific:Implications for the GlobalEpidemicDiabetes Care 2016;39:472–485 | DOI: 10.2337/dc15-1536

The last three decades havewitnessed an epidemic rise in the number of peoplewithdiabetes, especially type 2 diabetes, and particularly in developing countries, wheremore than 80% of the people with diabetes live. The rise of type 2 diabetes in SouthAsia is estimated to be more than 150% between 2000 and 2035. Although aging,urbanization, and associated lifestyle changes are the major determinants for therapid increase, an adverse intrauterine environment and the resulting epigeneticchanges could also contribute in many developing countries. The InternationalDiabetes Federation estimated that there were 382 million people with diabetes in2013, a number surpassing its earlier predictions. More than 60% of the people withdiabetes live in Asia, with almost one-half in China and India combined. TheWesternPacific, the world’s most populous region, has more than 138.2 million people withdiabetes, and the numbermay rise to 201.8million by 2035. The scenario poses hugesocial and economic problems to most nations in the region and could impedenational and, indeed, global development. More action is required to understandthedrivers of the epidemic to provide a rationale for prevention strategies to addressthe rising global public health “tsunami.” Unless drastic steps are taken throughnational prevention programs to curb the escalating trends in all of the countries,the social, economic, and health care challenges are likely to be insurmountable.

Diabetes is now a disease of major concern both globally and regionally and is aleading cause of death in most countries (1). In 2013, the International DiabetesFederation (IDF) estimated that ;382 million people had diabetes worldwide, andby 2035, this was predicted to rise to 592 million. Eighty percent live in low- andmiddle-income countries, and of the total, more than 60% live in Asia, with almostone-third in China (2). Major increases in the prevalence of diabetes have occurredin developing countries due to rapid and ongoing socioeconomic transition and willlikely lead to further rises (2). The prevalence of both type 1 and type 2 diabetes(T2DM) has increased significantly during recent decades. T2DM, being much morecommon (2), has been themain driver for the increase in global diabetes prevalenceand, therefore, will be the focus of this review.It should be noted that with regard to diabetes prevalence, only broad comparisons

can be made among studies on which national and global estimates by the IDF arebased. This is because there are marked differences in age-groups, survey methodol-ogies, diagnostic criteria, and other aspects of these studies in the various countries inAsia and the Pacific. Despite this, almost all developing countries in theWestern Pacificregion (WPR) (3) and also in South Asia (4–6) have shown escalating rates.The WPR is the world’s most populous World Health Organization (WHO) re-

gion, comprising 39 heterogeneous countries and territories, with populations

1India Diabetes Research Foundation, Chennai,India2Department of Medicine & Therapeutics, TheChinese University of Hong Kong, Prince ofWalesHospital, Shatin, Hong Kong3Hong Kong Institute of Diabetes and Obesity,The Chinese University of Hong Kong, Shatin,Hong Kong4Li Ka Shing Institute of Health Sciences, The Chi-nese University of Hong Kong, Shatin, Hong Kong5Saw Swee Hock School of Public Health, Na-tional University of Singapore, Singapore6Baker IDI Heart and Diabetes Institute, Mel-bourne, Australia

Corresponding author: Paul Z. Zimmet, [email protected].

Received 14 July 2015 and accepted 28 Novem-ber 2015.

A.N. and R.C.W.M. contributed equally to thiswork.

© 2016 by the American Diabetes Association.Readersmayuse this article as longas thework isproperly cited, the use is educational and not forprofit, and the work is not altered.

Arun Nanditha,1 Ronald C.W. Ma,2,3,4

Ambady Ramachandran,1

Chamukuttan Snehalatha,1

Juliana C.N. Chan,2,3,4 Kee Seng Chia,5

Jonathan E. Shaw,6 and Paul Z. Zimmet6

472 Diabetes Care Volume 39, March 2016

REV

IEW

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mailto:[email protected]

mailto:[email protected]

ranging from more than 1 billion peo-ple in China to 10,000 in small PacificIsland nations like Tuvalu. The regionhas undergone rapid changes develop-mentally, socioeconomically, politi-cally, and culturally during the lastfew decades (3).The increasing prevalence of diabetes

can be attributed to a multitude of in-terrelated factors, including rapid indus-trialization and urbanization and theensuing changes in lifestyle factors(4,6). The effect of the intrauterine en-vironment and the resulting epigeneticchanges may also convey increased riskof T2DM and other chronic diseases inadult life (1,7). Epigenetic changes canbe transmitted to future generations,thus becoming intergenerational. Therisk factors for T2DM are summarizedin Table 1 and are detailed below. Inter-estingly, the propensity of these risk fac-tors to cause diabetes appears higheramong the populations in South Asiaand in the WPR compared with Westernpopulations, and this is discussed in alater section.T2DM is increasingly present in even

children and adolescents (1,3–5), andthe increase in gestational diabetesmellitus (GDM) poses new challenges

such as higher risk of diabetes amongwomen and long-term consequencesfor the offspring (2,6,8,9). Prediabetesprevalence is also higher than that ofdiabetes in many of the WPR countries(10). T2DM is the focus of this review,which aims to address the major eth-nic, demographic, anthropometric, so-cioeconomic, genetic, and epigeneticfactors that are likely to be responsiblefor the dramatic rise in T2DM. We de-scribe the epidemiological scenario inAsia and in the Pacific. For the purposeof this review, the WPR refers to EastAsia, Southeast Asia, Australia, NewZealand, and the Pacific Islands; SouthAsia refers to Afghanistan, Bangladesh,Bhutan, India, Maldives, Mauritius,Nepal, Pakistan, and Sri Lanka (Fig. 1).Many of the nations in these regionsdo not have national data, so theyhave not been discussed in detail inthis review.

It should be noted that much of thediabetes prevalence data discussed inthis review come from IDF estimates(10). These have significant limitations,in that for countries without availablelocal data, estimates are based on mod-eling using pooled estimates from coun-tries that might be seen to be similar ingeography, ethnicity, and economic de-velopment. Similarly, numerous countrydata are based on WHO STEPwise ap-proach to Surveillance (STEPS) studies(11). These are not necessarily compa-rable with each other owing to method-ological differences. These limitationsmust be considered when examiningthe data.

Impaired fasting glucose and im-paired glucose tolerance (IGT) arehigh-risk conditions for diabetes andcardiovascular disease (12). China andmost of the other countries in WPRhave a high prevalence of IGT (3). Thisis true of many countries in Asia (13).However, many countries use only fast-ing plasma glucose (FPG) in epidemio-logical studies and therefore do nothave data on IGT. The use of FPG under-estimates the true level of diabetes andprediabetes compared with the oral glu-cose tolerance test (OGTT).

LITERATURE SEARCH STRATEGYAND SELECTION CRITERIA

We searched PubMed and Googlesearch using key words “diabetes inWestern Pacific Region,” “diabetes in

South Asia,” diabetes in individual coun-tries of these regions, “risk factors forT2DM in Western Pacific population,”“risk factors for T2DM in South Asians,”“gestational diabetes among Asian pop-ulation,” and “prevention of diabetes.”Published reports by the IDF, theWHO, and the American Diabetes Asso-ciation on the above topics were used.We selected the relevant articles andreviews from peer-reviewed journalsidentified by the search for preparingthe review.

THE DIABETES EPIDEMIC IN THEPACIFIC REGION AND IN ASIA

WPRToday, the nations in theWPR region arehighly heterogeneous in economic pro-file, varying from the high per capitagross domestic product in countriessuch as Singapore to low gross domesticproduct in the poorest nations. Devel-oped countries inWPR, such as Australiaand New Zealand, have a much lowerprevalence of diabetes compared withsome developing countries and alsothe Pacific Islands (14).The IDF esti-mated that in the WPR in 2013, therewere 138 million people with diabetes,36% of the global total (10). The biggestcontribution to this number is China,with 113.9 million adults with diabetesand 493.4 million with prediabetes (15).Some small Pacific Islands, such as Toke-lau, according to the IDF estimates andtheWHO STEPS studies (11), have a veryhigh diabetes prevalence (Table 2). Asmentioned earlier, these are not neces-sarily comparablewith each other owingto methodological differences betweenand within countries. This point is high-lighted in Cambodia by a 2005 report(16) showing that T2DM has emergedat rates similar to those in developednations such as Australia; yet, a subse-quent STEPS modeling study showedthat Cambodia had the lowest preva-lence in the WPR (10).

In the 2013 IDF estimates, China topsthe global list of countries for the totalnumber of people with diabetes, fol-lowed by India (2). The number of peo-ple with diabetes in Japan has increasedsignificantly since 1997, especiallyamong the male population. In 2013, itoccupied the 10th position in the IDF list,with 7.2 million people with diabetes(17). Indonesia has not registered a sig-nificant increase since 1997 (18,19).

Table 1—Plausible etiological factorsresponsible for the increased propen-sity to develop T2DM

Genetic and acquired factorsGenetic factors (familial aggregations)Ethnic susceptibilityAdverse gene–environment interaction

(i.e., epigenetics, metabolicmaladaptations)

Lower threshold for diabetogenic riskfactors (i.e., age, BMI, central adiposity)

Low muscle massIncreased insulin resistanceDecreased b-cell compensationdisproportionate to insulin insensitivity

Presence of metabolic obesityIncreased inflammatory response

Environmental risk factorsUrbanization and modernizationGlobalization and industrializationUnhealthy behavioral habits (sedentary

lifestyle, consumption of energy-dense food, smoking, tobacco chewing,and excessive alcohol consumption)

Sleep disturbancesPsychological stress

Societal factorsCultural and religious taboosPsychosocial factorsLack of universal health coverage

care.diabetesjournals.org Nanditha and Associates 473

http://care.diabetesjournals.org

IDF estimates for diabetes within thePacific vary widely, from the world’s high-est of 47.3% in American Samoa to a com-paratively lower prevalence of 7.3% inFrench Polynesia (3,10). Figure 1 showsthe map of the WPR, and Table 2 reportsthe temporal changes in the prevalence ofdiabetes in these countries. The risingtrend in the developing countries is con-siderably steeper compared with the de-veloped countries (1,12,14,15,17–34). Inrecent decades, apart from the WHOSTEPS studies (11), there have been veryfew national diabetes studies for the Pa-cific Ocean nations (14). Nevertheless,some of the highest estimates of preva-lence globally continue to be seen in thisregion, even though the use of FPG aloneunderestimates the true diabetes preva-lence (35) and the laboratory methodswere not standardized among the studies.Obesity is a major driver of the T2DM

epidemic, and the Pacific Island nationsare among the leaders in the world obe-sity and diabetes charts (14). Accordingto the latest WHO criteria for obesity(11), more than 70% of the people inAmerican Samoa, Nauru, and Tokelauare obese. Other islands also show ahigh prevalence of obesity, includingKiribati (50.6%), the Marshall Islands(45%), the Federated States ofMicronesia

(42.6%), the Solomon Islands (32.8%), andFiji (29.6%) (14).

Since the 1960s, the Pacific region hasbeen recognized as a “hot spot” for di-abetes, with Prior and Davidson (36)first reporting a higher diabetes preva-lence in Polynesians compared withNew Zealanders of European descent.In 1975, on the Central Pacific island ofNauru, the then highest ever nationaldiabetes prevalence of 34.4% was re-ported (37). Income from Nauru’s richphosphate deposits had resulted in itsMicronesian population becoming ex-tremely prosperous and obese. Withthe phosphate deposits now exhausted,and with the consequent contractionof the national economy, a significantfall has occurred in diabetes preva-lence (1). In the 1980s, Zimmet et al.(38) confirmed the higher prevalenceof diabetes in other Pacific Islands usingstandardized protocols. However, be-cause most of these studies were under-taken more than two decades ago, theyare unlikely to reflect current diabetesrates (14).

The paucity of secular data in the Pa-cific presents a difficulty in monitoringtrends. The age-standardized preva-lence of T2DM in Western Samoa in-creased between 1978 and 1991 from

8.1 to 9.5% in men and from 8.2% to13.4% in women in the urban area,and from 2.3% to 7% in men and from4.4% to 7.5% in women in a rural com-munity (39). In Tonga in 2002, Colagiuriet al. (40) reported a dramatic secularincrease (100% in 25 years) in diabetesfrom 7.5% in 1973% to 15.1%, of which80% were undiagnosed cases.

King et al. (16), in 2005, reported ondiabetes in Cambodia, a relatively poorand fairly traditional country, showingprevalence of 5% (rural) and 11% (semi-urban). The prevalence of IGT was 10%(rural) and 15% (semiurban). About two-thirds of all cases of diabetes were un-diagnosed. These figures are muchhigher than those reported by a subse-quent WHO STEPS study (11). Such dif-ferences, which may relate to the firststudy being a dedicated diabetes surveyand using the OGTT and the secondstudy being a general survey of noncom-municable diseases and relying on thefasting glucose alone, need to be keptin mind.

InMalaysia, the reportedprevalence ofdiabetes was 11.6% in 2006 (26), 15.2%(8% undiagnosed) in the 2011 nationalstudy (41), and 22.9% in 2013 (26). Theage distribution of the study groups wassimilar. The higher prevalence seen in the2013 survey may partly be explained bythe use of the OGTT. In Thailand, the Na-tional Health Examination Survey showedthat the diabetes prevalence in peopleaged $15 increased from 2.5% in 1991to 4.6% in 1997 and to 6.8% in 2004(32). In 2009, their National Health Exam-ination Survey (33) found the prevalenceof impaired fasting glucose was 10.6%and diabetes was 7.5% (of which 35.4%were undiagnosed cases) in adults aged$20 years. These prevalences were likelyto be underestimates because diagnosisrelied only on a single FPG, history of phy-sician diagnosis, and information onmedications (33). The age-standardizedprevalence in Singapore has remainedconstant at ;11% during the lasttwo decades. In Singapore, diabeteswas more common in Indians (17.2%)than in Malays (16.6%) or Chinese(9.7%) (31).

The prevalence of diabetes in Korea in-creased from ,1% in 1960 to .10% byearly 2000. TheKoreaNationalHealth andNutrition Examination Survey (KNHANES)2010–2012 also reported a prevalence of10.1% based on FPG (29,30), suggesting a

Figure 1—Map shows the Western Pacific and South Asian regions.

474 Implications of Diabetes in Asia and WPR Diabetes Care Volume 39, March 2016

Tab

le2—Preva

lence

ofdiabetesin

theWPR,withtemporalch

angessh

ownwhereve

rava

ilable*

Country

Year

(Ref)

Samplesize

(n)

Characteristics

Diagn

osticcriteria

Diabetes

(%)

American

Samoa

2004

(14)

2,07

2WHOSTEP

S;stratified

cluster

sampling;

age:

25–64

years

Cap

illaryFPG$6.1mmol/L

47.3

Australia

2011

–20

12(20)†

NR

Age:$18

years

HbA1c$6.5%

($47

.5mmol/mol)

5.4

BruneiDarussalam

2003

(21)†

NR

Population-based

datafrom

integrated

health

screen

ingsystem

frommed

icalcase

records;age:NR

CapillaryFPG$6.1mmol/Lorknowndiabetes

5.4

2010

(21)†

NR

Age:$20

years

CapillaryFPG$6.1mmol/Lorknowndiabetes

12.5

Cam

bodia

2004

(16)

2,24

6Cross-sectional;tw

ocommunities:ruraland

semiurban;age:

$25

years

FPG$7.0mmol/Lor/and2-hPG

$11

.1mmol/L

Rural:5.0

Suburban:11

.020

11(24)†

5,12

3WHOSTEP

S;multistage

cluster

method

(180

clusters);age:

25–65

years


$11

.1mmol/L

Total:2.9(95%

CI2.3–3.4)

Rural:2.3(95%

CI1.7–2.9)

Urban:5.6(95%

CI4.0–7.2)

China

2001

(25)†

15,838

Nationallyrepresentative

stratified

sampling;

age:

35–74

years

FPG$7.0mmol/Lor2-hPG

$11

.1mmol/L

5.5

2010

(15)†

98,658

Complex,multistage,probability

samplingdesign;

age:

$18

years


$11

.1mmol/L

11.6

China,HongKo

ngSA

R19

90(22)

1,51

3Participan

tsfrom

apublic

utilitycompanyanda

regionalhospital;age:

$30

years


$11

.1mmol/L

4.5

2007

–20

10(23)

3,37

6HongKo

ngprofessionaldrivercommunityproject;

age:

18–70

years


$11

.1mmol/L

8.1

CookIslands

1980

(14)

1,10

2Po

pulation-based

study;age:

$20

years


$11

.1mmol/L

6.8

2003

(14)

2,03

6WHOSTEP

S;stratified

samples;age:

NR

CapillaryFPG$6.1mmol/Loronmed

ication

23.6

Federated

States

ofMicronesia

1994

(14)

2,18

8Po

pulation-based

studyin

Kosrae

population;

age:

20–85

years

FPG$7.0mmol/L

12.0

2002

(14)

1,63

8WHOSTEP

S;population-based

cross-sectional

study;age:

25–64

years

FPG$7.0mmol/L

32.1

Fiji

2002

(14)

2,27

7Po

pulation-based

multistage

samplingin30

clusters;

age:

15–64

years


ication;HbA1c

$6.5%($

47.5

mmol/mol)orknownto

havediabetes

16.0

2009

(14)

1,35

3WHOSTEP

S;population-based

study;age:$40

years

44.8

Fren

chPo

lynesia

2010

(14)

3,46

9WHOSTEPS;population-based

multistage

sampling;

age:

18–64

years


ication

7.3

Indonesia

1997

(18)

941

Population-based

studyofgovernmen

tandretired

individuals;age:

NR


$11

.1mmol/L

5.4

2009

(19)

24,417

Samplesfrom

13urban

provinces;age:

$15

years


$11

.1mmol/L

5.7

Japan

1997

(17)

National

Age:$20

years


$11

.1mmol/L

M:F9.9:7.1

2007

(17)

National

Age:$20

years


$11

.1mmol/L

M:F15

.3:7.3

Kiribati

1983

(14)

2,93

8Po

pulation-based

survey;age:

$20

years;South

Tarawaandthefourouterislands;age:15

–64

years


$11

.1mmol/L

Urban

:M:F9.6:8.7

Rural:M:F3.0:3.3

2004

–20

06(14)

1,14

6WHOSTEP

S;population-b

ased

multistage

sampling;

age:

18–64

years

FPG$7.0mmol/L

28.1

Con

tinu

edon

p.47

6



Table

2—Continued

Country

Year

(Ref)

Samplesize

(n)

Characteristics

Diagnosticcriteria

Diabetes

(%)

Malaysia

2006(26)

34,539

Malaysian

NationalHealthMorbiditySurvey

(NHMS)

III;age:

$18

years

FPG$7.1mmol/Lorknownto

havediabetes

11.6

2013(26)

4,34

1Tw

o-stage

stratified

samplingdesign;age:$

18years

HbA

1c$6.5%

,FPG

$7.8mmol/Lor

2-hPG

$11.1mmol/L

22.9

MarshallIslands

2002(14)

994

WHOSTEP

S;population-based

;age:

15–64

years

FPG$7.0mmol/L

19.6

Mongo

lia20

05(27)

3,41

1WHOSTEP

S;population-based

;age:

15–64

years

Cap

illaryFBG$6.1mmol/Loronmed

ication

8.2

2009(27)

5,36

8WHOSTEP

S;population-based

;age:

15–64

years

Cap


ication

6.5

Nauru

1987

(1)

1,20

1Po

pulation-based

data;age:

$20

years


$11

.1mmol/L

24.0

2004(14)

883

System

aticrandom

sampledesign;age:15–

64years

FPG$7.0mmol/Loronmed

ication

16.2

(age

15–24

years)

22.7

(age

25–64

years)

New

Zealand

2002

–20

03(28)

12,929

Stratified

cluster

sampling;

age:

$15

years


$11

.1mmol/L

8.1

2008

–20

09(28)

4,72

1Age:$15

years


$11

.1mmol/L

7.0

Niue

1980

(1)

1,12

8Po

pulation-based

survey;age:

$20

years

FPG$7.8mmol/L

7.2

2012(14)

863

WHOSTEP

S;population-based

;age:

$15

years

Cap


ication

38.4

PapuaNew

Guinea

1991(14)

497

Population-based

cluster;age:

$25

years

Ran

dom

bloodglucose

$8mmol/Lorknowndiabetes

Urban:30

.3Rural:Wan

igela:

11.7

Kalo:1.6

2008(14)

2,94

4WHOSTEP

S;population-based

survey;age:

15–64

years

Cap


ication

14.4

Rep

ublic

ofKo

rea

2005(29)

4,62

8KN

HANES;age:

$30

years

FPG$7.0mmol/Lor/an

dhistory

ofdiabetes

9.1

2007

–20

09(29)

13,512

Age:$30

years

FPG$7.0mmol/L

9.9

2011

–20

12(30)†

14,330

NationalHealthSurvey;age:

$30

years

FPG$7.0mmol/L

10.1

Samoa

1991

(14)†

1,77

6Po

pulation-based

cluster

sampling;age:25

–74

years

FPG$7.8mmol/Lor/an

d2-hPG

$11

.1mmol/L

Apia:M:F9.5:13.4

Poutasi:M:F5.3:5.6

Tuasivi:M:F7.0:7.5

2002(14)

2,81

7WHOSTEP

S;random

samplepopulation-based

study;age:

15–64

years

Cap

illaryFBG$6.1mmol/LorvenousFPG$7.0mmol/L

oronmed

ication

22.1

Singapore

2004

(31)†

NR

Nationalsurvey;age:

18–69

years


$11

.1mmol/L

8.2

2010

(31)†

NR

Nationalsurvey;age:

18–69

years


$11

.1mmol/L

11.3

SolomonIslands

1986(14)

243

Population-based

study;age$18

years

WHOSTEP

S;population-based

;age:

25–64

years

FPG$7.0mmol/Lor/an

d2-hPG

$11

.1mmol/L

2.09

2006(14)

950

Cap


ication

13.5

Thailand

1991

(32)†

National

Age:$30

years

FPG$7.0mmol/L

2.3

2004

(32)†

National

Age:$15

years

FPG$7.0mmol/L

6.8

2009

(33)†

National

Age:$20

years

FPG$7.0mmol/L

7.5

Tokelau

1976(14)

346

Population-based

study;age:

35–74

years

OGTT

(100

g):1-hPG

$13

.9mmol/L

M:F7.0:14.3

2005(14)

573

WHOSTEP

S;population-based

nationalsurvey;

age:

15–64

years

Cap


ication

33.6

Con

tinu

edon

p.47

7


constant prevalence of diabetes duringthe last decade. Diabetes was more prev-alent in individuals in lower socioeco-nomic groups, a finding similar to that indeveloped Western countries.

South AsiaSouth Asia constitutes one-fifth of theworld’s population and includes ninecountries, all ofwhich are undergoing life-style transitions that make their popula-tions more vulnerable to develop T2DM.In the last few decades, the diabetesprevalence in South Asia has also risenconsiderably. Table 3 reports the secularchanges that occurred in these nations(5,42–51). However, true nationally rep-resentative data, which include urban andrural prevalence, are lacking frommost ofthese countries, including India.

South Asian populations also have ahigh prevalence of prediabetes and amore rapid progression to diabetes(13). This is highlighted by a recent studythat reported a diabetes incidence of22.2 per 1,000 person-years and that59% of those with prediabetes con-verted to diabetes after a follow-up of9.1 years (52).

A 2008 report from Southern Indiashowed a marked increase in diabetesprevalence in both urban and rural areascompared with earlier studies (53).Studies from other parts of India havealso shown increases in diabetes preva-lence (13,46).

India is the largest country in the re-gion and has more than 65.1 millionpeople with diabetes, occupying thesecond position next to China in theIDF global list of top 10 countries forpeople with diabetes. Pakistan and Ban-gladesh are in 12th and 13th positions,respectively (10). The IDF estimates thatthe number of people with diabetes inSouth Asia will increase to 120.9 million,10.2% of the adult population, by 2030.The highest increase in diabetes preva-lence is noted in Mauritius (48) (Table3), an Indian Ocean island with a pre-dominantly Asian Indian population. Asurvey conducted in urban and ruralMaldives showed that the prevalenceof diabetes was 10.6% (47). Howeverresults from the STEPS survey con-ducted in Male, the Maldives capitalcity, showed the prevalence of diabeteswas 4.5% in all adults (11). Again, thereason for the difference seen in theSTEPS study is unclear.

Table

2—Continued

Country

Year

(Ref)

Samplesize

(n)

Characteristics

Diagn

osticcriteria

Diabetes

(%)

Tonga

1991

(14)†

1,02

4Nationalsample;age:

$15

years


$11

.1mmol/L

15.1

2004

(14)†

453

WHOSTEP

S;population-based

nationalsurvey;

age:

15–64

years

Cap


ication

16.4

Van

uatu

1991

(14)

1,37

8Anoccupation-based

(civilservants)urban

sample

andarea-based

semiruralandruralsam

ples;age:NR


$11

.1mmol/L

Vila:M:F2.1:12.1

Nguna:M:F2.1:1.1

Tanna:

M:F1.0:0.9

2011

(14)†

4,42

2WHOSTEP

S;population-based

nationalsurvey;

survey

included

allsixprovinces;age:

25–64

years

Cap


ication

21.2

Vietnam

2001

(34)

2,93

2Cross-sectional;age$15

years


$11

.1mmol/L

3.8


$11

.1mmol/L

2011

(12)

2,71

0Cross-sectional;age:

40–64

years


$11

.1mmol/L

3.7

Wallis

andFutuna

1980

(14)†

549

Population-based

study;age:

$20

years


$11

.1mmol/L

2.7

2010

(14)†

487

WHOSTEP

S;population-based

nationalsurvey;

age:

15–64

years


ication

17.5

F,female;FBG,fastingbloodglucose;H

bA1c,glycated

hem

oglobinA1c;M,m

ale;NR,notreported

;PG,plasm

aglucose;SAR,SpecialAdministrativeRegion.*Itneedsto

berecognized

that

onlybroad

comparisons

canbemad

efrom

thesedataowingto

sign

ificantdifferencesin

age-groups,survey

methodologies,diagn

osticcriteria,etc.†Nationalstudies.



Several distinctive features are notedamong the South Asians, such as earlyoccurrence of diabetes at lower BMI lev-els (6), higher rates of insulin resistance,abdominal obesity, and familial aggrega-tionof diabetes than inmanyother ethnicgroups. In recent decades, an increasingdiabetes prevalence has been reported inrural areas in middle-income groups andamong underprivileged people (13,51).Occurrence of T2DM at a young age iscommonly observed among South Asians,with the picture further complicated by thepresence of maturity-onset diabetes of theyoung or latent autoimmune diabetes ofadulthood (13).

Urban-Rural DifferenceIn developing countries in Asia and WPR,the urban-rural difference in diabetesprevalence is narrowing due to the in-creasing reach of Western lifestyles andassociated behavioral changes into ruralsettings. In India, Nepal, Sri Lanka, theSolomon Islands, Samoa, and Thailand,more than 50%of the national populationwith diabetes resides in rural areas (10).Recent studies from India (53) and China(4,6,54) have shown greater rates of in-crease in diabetes prevalence in ruralthan in urban areas. Hwang et al. (55)reported that across multiple surveys,there was evidence of a fivefold rise inthe prevalence of diabetes from 1985 to2010 in rural populations of developingcountries.

Diabetes in the DiasporaPopulation-based studies indicate ahigher prevalence of diabetes amongthe South Asian diaspora comparedwith other ethnic and the local popula-tions in many Western nations, includ-ing the U.S. and the U.K. (13,56–60).Among South Asians, T2DM is usuallydiagnosed at an earlier age and is asso-ciated with increased mortality com-pared with the white population inthese countries.

Risk Factors for Diabetes in Asians andPacific IslandersSimilar risk factors for T2DM have beenidentified in Europids and in Asian popu-lations (5,6,54).Many of these risk factorsare closely linked to economic develop-ment and the increasing urbanizationseen across much of Asia and the Pacific.Some risk factors for T2DM have becomeof great concern among developing coun-tries in Asia and the Pacific. As discussed

Table

3—Preva

lence

ofdiabetesin

South

Asia,withtemporalch

anges

shownwhereve

rava

ilable

Country

Year

(Ref)

Samplesize

(n)

Characteristics

Diagn

osticcriteria

Diabetes

(%)

Afghanistan

2013

(42)

1,16

9Age:.40

years

Cap


ication

13.3

Bangladesh

2005

(5)

6,31

2Cross-sectional;age:

$20

years


$11

.1mmol/L

Urban:8.3

Rural:2.3

2011

(43)*

8,83

5Po

pulation-based

nationalsurvey;age:

$35

years


$11

.1mmol/L

9.7

Bhutan

2008

(44)

2,47

4Stratified

two-stage

sampling;

age:

25–74

years


$11

.1mmol/L

8.2

India

2000

(45)

11,216

Random

sampling,sixmetropolitan

cities;

age:

$20

years


$11

.1mmol/L

12.1

2008

–10

(46)

13,055

Stratified

multistage

sampling(188

urban,1

75rural)

inthreestates

andoneunionterritory;agenotreported

FastingCBG$7mmol/Lor/and2-hCBG$12

.2mmol/L

oronmed

ication

TamilNadu:10

.4Maharashtra:

8.4

Jharkhan

d:5.3

Chan

digarh:13

.6

Maldives

2004

(47)*

1,55

6Cross-sectional;national;age:

25–64

years


$11

.1mmol/L

4.5

Mauritius

1987

(48)

5,08

3Indep

enden

tpopulation-based

survey;age:

20–74

years


$11

.1mmol/L

13.0

2009

(48)

6,37

1Age:20

–74

years


$11

.1mmol/L

21.3

Nep

al20

11(49)

14,425

Populationfrom

EasternNep

al;age:

.20

–10

0years


$11

.1mmol/L

6.3

Pakistan

2000

(50)

1,04

2Age:30

–64

years


$11

.1mmol/L

6.5

2006

(50)

5,43

3Age:30

–64

years


$11

.1mmol/L

Urban:10

.6Rural:7.7

SriLan

ka20

01(5)

6,04

7Cross-sectional;stratified

random

samplesfrom

four

provinces;age:

$30

years


ication

13.8

2006

(51)*

4,53

2Cross-sectional;nationalrepresentative;age:

$20

years


$11

.1mmol/L

10.3

CBG,capillarybloodglucose;FBG,fastingbloodglucose;PG

,plasm

aglucose.*N

ationalstudy.


later, the prevalence of GDM has also in-creasedmarkedly in Asia and thePacific inrecent decades (9,10).Much of the recent increase in diabe-

tes prevalence is related to changes indietary pattern, sedentary behavior, andobesity superimposedona background ofgenetic/epigenetic susceptibility (61).Most Asian countries have witnessed, todifferent degrees, a nutritional transition,with increases in intake of refined carbo-hydrates, animal fats, and meat, and re-duced consumption of dietary fiber andvegetables (61,62). Similar to theU.S., theconsumption of sugar-sweetened bever-ages in China has increased dramaticallyduring the last few decades (62).Several dietary risk factors may be par-

ticularly relevant to Asians. The SouthAsian diet, characterized by high intakeof carbohydrates, trans fats, and saturatedfats (63), appears particularly conduciveto the risk of T2DM.White rice constitutesup to 60% of the glycemic load among theChinese and was found to be associatedwith an increased risk of diabetes in ameta-analysis (64). This association be-tween white rice intake and risk ofT2DM was also noted in India (65). Al-though rice has been a staple food forcenturies, there has been a shift to in-creased intake of polished rice, whichproduces a greater glycemic excursionthan do the more traditional types ofrice. Furthermore, Asians appear to havegreater glycemic excursion to white ricecompared with other populations (66).Physical inactivity is an important risk

factor for T2DM in most populations(4,5). With increasing urbanization, phys-ical activity has declined, particularly inoccupational settings (67), and sedentarybehavior has increased. This highlightsthe importance of encouraging physicalactivity and reducing sedentary behaviorin large-scale community diabetes pre-vention initiatives in Asia and the Pacific.Studies that have examined the asso-

ciation between adiposity and diabetesin multiethnic cohorts noted that Asiansdevelop diabetes at a considerablylower BMI compared with Europids(54,68). This is ascribed to visceral adi-posity in Asian populations (69). As a re-sult, in Asians, lower BMI cutoffs arebeing used to define obesity (70) aswell as lower waist circumference fordefining central obesity (57,70). How-ever, two large observational studieshave shown that the incremental risk

of diabetes associated with increasingadiposity does not differ between Euro-pid and Asian populations (71,72). Thus,the ethnic difference in the adiposity-diabetes relationship is probably bettercharacterized as an increased risk of di-abetes at all levels of BMI (or waist cir-cumference) rather than as diabetesoccurring at lower levels of BMI. It isvery similar to the increased diabetesrisk of Asian populations seen at allages, and both observations point tofactors other than those related to obe-sity or age that increase diabetes sus-ceptibility in Asian populations.

Several novel putative risk factorshave recently emerged as important be-havioral and environmental determi-nants for T2DM. These include sleepdisturbances and environmental expo-sure to organic pollutants and otherchemicals (62). Given the major prob-lems of pollution in many developingcountries, the latter has the potentialto be an important contributor to thediabetes epidemic during adult life oras an in utero exposure.

Developmental Origins of T2DM:Relevance in Asia and PacificCommunitiesThe initial observations on the associationbetween low birth weight and adult riskof diabetes and metabolic disturbanceswere made by Hales and Barker (73). Itis now increasingly appreciated that thein utero environment plays an importantrole in modifying developmental trajec-tory and physiology, thereby altering therisk of obesity, T2DM, and other chronicdiseases in adulthood (7).

Studies in relation to the Dutchwinter(74) and Chinese (75) famines providesupport for the hypothesis that nutri-tional deprivation in utero may predis-pose an individual to T2DM in adult life.In those exposed to severe famine insome parts of China during early life,there is a marked increase in the riskof diabetes as adults compared withthose not exposed to the same severenutritional restriction during in uterodevelopment. This risk of diabetes inmidlife is highest among offspring ex-posed to in utero undernutrition andwho were subsequently exposed to anaffluent diet (75). This phenomenon ofhistorical exposure to undernutrition inearly life followed by exposure to a“metabolically challenging” environment

characterized by an energy-dense dietmay be highly relevant to the currenthigh rates of T2DM in parts of Asia andthe Pacific.

The emergence of T2DM in Cambodiaat rates similar to those in developednations (16) came decades after thepolitical and socioeconomic upheavalcaused severe food shortages in Cambo-dia in 1975. During World War II, theNauruanswere subjected to famine con-ditions on Nauru and on other PacificIslands, such as Truk, where they hadbeen relocated. Some three decadeslater, Nauru had the highest diabetesprevalence in the world (37). These his-torical examples show the potential ofunexpected health outcomes from warsand famine when later followed by rela-tive overnutrition. Furthermore, thestudy by Yajnik (76) in India strongly sug-gest that early development issues andepigenetics may play an important rolein the contemporary burden of diabetesexperienced in India.

In addition to a link between in uteroundernutrition and offspring risk, epi-demiological studies, particularlyamong the Pima Indians, have high-lighted increased risk of obesity andT2DM in offspring exposed to maternaldiabetes or obesity (77–79). This is alsoparticularly relevant in Asia, wherethere is a higher proportion of young-onset diabetes and a higher prevalenceof GDM compared with Europe and theU.S. (9). Thus, intergenerational cyclesmay operate in Asia to increase the riskof diabetes in future generations (76).

GDMWith the epidemiological transitions oc-curring in Asia, leading to a younger ageof diabetes onset, the burden of preg-nancy complicated by hyperglycemia isincreasing (80). Hyperglycemia in preg-nancy includes cases of diabetes predatingpregnancy as well as GDM. On the basisof a systematic literature review of stud-ies reporting the prevalence of GDM indifferent countries, the IDF estimatedthat 16% of pregnancies globally wereaffected by hyperglycemia in 2013,with a crude prevalence of 11.8% in theIDF WPR and 23.1% in the South Asian re-gion (80). TheprevalenceofGDMreportedin Asia has ranged from 1% to more than20%, depending on the period, ethnicity,and population in which the study wasconducted, as well as the screening



strategy and diagnostic criteria being used,which has been extensively reviewed else-where (9). A study from Australia compar-ing women of different ethnicities with adiagnosis of GDMnoted that women fromSoutheast Asia had the lowest BMI andwere more likely to be diagnosed basedon elevated 2-h glucose during OGTT,whereas women from Pacific Islands andAnglo-Europeans had the highest BMI andweremore likely to be diagnosed based onelevated fasting glucose (81).A marked secular increase in preva-

lence of GDM has been reported in sev-eral studies; for example, universalscreening of pregnant women for GDMin Tianjin, China, showed that the prev-alence increased markedly from 2.4 to6.8% from 1999 to 2008 (82). Use of thediagnostic criteria proposed by the In-ternational Association of the Diabetesand Pregnancy Study Groups (IADPSG),recently adopted by the WHO (83), islikely to lead to further increases inGDM prevalence. In a study from Viet-nam, for example, applying the IADPSGcriteria resulted in an increase in preva-lence of GDM from 6.1 to 20.3% (84).The offspring of mothers with GDM

have increased risks of obesity, hyper-tension, diabetes, and other noncom-municable diseases (78,79). Given thehigh risk ofGDMamongAsianpopulationsand the potential transgenerational ef-fects of GDM and maternal nutrition,there is an urgent need to implementpreconception interventions to optimizematernal health (85,86). Also, the highprevalence of GDM and its potentiallong-term effects makes a strong casefor universal screening for GDM in Asianpopulations. This has already been adoptedin some Asian countries (9).

Pattern of Diabetes Complications inAsia and Pacific CommunitiesThere are ethnic differences in the pat-tern of diabetes complications (54). Earlyobservations from the WHO Multi-national Study of Vascular Disease inDiabetes (WHO MSVDD) had suggestedcomparatively high rates of albuminuriain Asian centers (87). In an analysis of65,171 subjects with T2DM evaluatedin primary care in New Zealand between2000 and 2006 (including 3,166 SouthAsians and 1,941 East Asians), the risksof having microalbuminuria, macroalbu-minuria, and advanced proteinuria weresignificantly increased 1.4- to 4-fold in

Pacific Islanders, South Asians, and EastAsians compared with Europeans (88).Moreover, recent studies in multiethnicpopulations that compared diabetic re-nal disease among individuals of differ-ent ethnicities suggest that ethnicminorities in the U.S., including SouthAsians and Chinese, are more likely tosuffer from proteinuric diabetic renaldisease than from nonproteinuric dia-betic renal disease (89).

A meta-analysis of studies on theprevalence of diabetic retinopathynoted that South Asians had the low-est prevalence (90). A lower preva-lence of peripheral sensory neuropathywas also reported in Asian patients inthe Fremantle Diabetes Study (FDS) inAustralia compared with patients ofEuropean descent (91).

The prevalence of diabetes complica-tions in the Pacific region is higher thanthat reported for other regions (e.g.,Asia, Africa, and the Middle East) (14).Consistent with this, Pacific Islanders inthe U.S. have a comparatively high prev-alence of foot complications and ampu-tations (92).

In the WHO MSVDD, the prevalenceof cardiovascular complications washigh in South Asians, but in generalwas low in centers in China, Hong Kong,and Japan (93). More recent studies haveconfirmed these earlier observations. Forexample, other studies in multiethnicpopulations have noted the high preva-lence of cardiovascular complicationsamong South Asian populations, believedto be partly driven by their predispositionto visceral adiposity (6,13). In contrast,patients with T2DM in China appear tohave lower rates of cardiovascular com-plications compared with Europeans (94),and the application to Chinese popula-tions of risk scores developed in Europeanpopulations tends to overestimate therisk of coronary heart disease (95). Stud-ies that have compared the risk of periph-eral vascular disease have noted thatSouth Asians are at lower risk of amputa-tions than Europeans (96).

In addition to ethnic differences inthe risk of diabetes complications, thepattern of diabetes complications inAsia is also notable for the large propor-tion of individuals with young-onsetT2DM. In the Joint Asia Diabetes Evalu-ation (JADE) program, among 41,029patients recruited from across ninecountries/regions in Asia, 18% had

onset of T2DM below the age of 40(97), had longer disease duration, andhad higher rates of retinopathy andend-stage renal disease than those withonset of diabetes after the age of 40 (97).In the Hong Kong Diabetes Registry, pa-tients with young-onset diabetes hadhigher risks of incident cardiovascularand renal complications at any age, drivenby the longer disease duration (98). Giventhe proportion of patients with young-onset T2DM, the potential burden ofdiabetes-related complications is ofgreat concern.

Prevention of DiabetesPrimary prevention of diabetes is a prac-tical and cost-effective method of re-ducing incident diabetes in populationsof varied ethnicity and biological char-acteristics (99). Systematic long-termstudies conducted in Western nations,such as the U.S. (100) and Finland(101), have shown the benefits of usingintensive lifestyle modification (LSM)resulting in significant weight reductionin obese and overweight persons withIGT, leading to a 58% relative risk reduc-tion in diabetes (100). These programsin the Western countries (100) and inChina have also shown the enduringeffect of LSM, with the effects demon-strated to last at least 10–20 years(102,103).

Studies in the Asian populations, suchas the Da Qing studies in China (102,103),the Indian Diabetes Prevention Pro-gramme (IDPP) (104) in India, and theJapanese prevention programs (105,106),have shown that LSM is effective in pre-venting T2DM even in nonobese popula-tions with high levels of insulin resistanceand that this is achieved without sig-nificant weight reduction. Importantly,the 23-year Da Qing IGT and DiabetesStudy follow-up showed a sustained ben-eficial effect of LSM on diabetes incidenceand on cardiovascular and all-cause mor-tality in the Chinese population (102).Pragmatic, cost-effective, and scalableprograms are being tested in developedcountries and in South Asian countries(107). A recent study in India showedthat the cumulative incidence of diabe-tes in 2 years was significantly loweramong the people with prediabeteswho received frequent text messageson mobile phones on healthy lifestyleprinciples (18%) than among the controlgroup on standard care (27%) (108).


Table

4—Randomize

dco

ntro

lledpreve

ntio

nstu

diesin

T2DM

inAsia

npopulatio

nsusin

glife

style

interventio

n

Studypopulatio

ncharacteristics

Mean

duratio

nParticip

antsbytreatm

ent

group

Cumulative

incid

ence

ofdiab

etesRelative

riskred

uctio

nStu

dy(year)

(Ref)

(years)(n)

(%)

(%)

DaQingIGTandDiab

etesStu

dy(1997)

(102)Chinese:

Totaln

=577

Contro

l:67.7

Diet:

31.0BMI:26.0

6Contro

l:133

Diet:

43.8Exercise:

46.0Age:

45.0Diet:

130Exercise:

41.1Diet

+exercise:

42.0Cluster

randomized

byclin

icExercise:

141Diet

+exercise:

46.0Diet

+exercise:

126

DaQingDiab

etesPreven

tion

Study(2008)

(103)Contro

lContro

l:138

Contro

l:93.0

43.0BMI:24.4

20Interven

tion:439

Interven

tion:80.0

Interven

tion

BMI:24.5

DaQingDiab

etesPreven

tion

Study(2014)

(103)Contro

lTo

taln=568

(byinterview

from

med

icalrecords)

Contro

l:89.9

45.0BMI:25.7

23Contro

l:138

Interven

tion:72.6

Interven

tion

Interven

tion:430

CVDmortality

41.0BMI:26.2

Contro

l:19.6

Interven

tion:11.9

All-cau

semortality

29.0Contro

l:38.4

Interven

tion:28.0

IDPP-1

(2006)(104)

BMI:25.8

2.6(m

edian

)To

taln=531

Contro

l:55.0

LSM:28.5

Age:

45.9Contro

l:136

LSM:39.3

Metfo

rmin:26.4

Persisten

tIGT,in

divid

ualran

domizatio

nLSM

:133

Metfo

rmin:40.5

LSM+metfo

rmin:28.2

Metfo

rmin:133

LSM+metfo

rmin:39.5

LSM+metfo

rmin:129

Indian

SMSstu

dy(2013)

(108)BMI:25.8

2Contro

l:266

Contro

l:27.4

Age:

45.9Interven

tion:271

Interven

tion:18.5

36.0Persisten

tIGT,m

en

Japan

esepreven

tionstu

dy(2005)

(105)Jap

anese

men

:4

Contro

l:102

Contro

l:9.3

67.4BMI:23.5

Interven

tion:356

Interven

tion:3.0

Age:

51.5IGT,in

divid

ualran

domizatio

n

Zensharen

StudyforPreven

tionof

LifestyleDiseases

(2011)(106)

Japan

esemen

:3

Contro

l:330

Contro

l:16.6

44.0BMI:27.0

Interven

tion:311

Interven

tion:12.2

Age:

49.0IGT,in

divid

ualran

domizatio

n

Age

givenas

mean

(years)andBMIgiven

asmean

(kg/m2).

CVD,card

iovascu

lardisease.



Table 4 describes the major diabetesprevention studies in Asia using LSM(102–106,108).For any program to be successful at a

population level, major changes are re-quired at relevant personal, cultural, so-cietal, and community levels (109). Anexample of the principles laid out inthe Western Pacific Declaration on Dia-betes (110) being translated in actioncan be found in Singapore’s diabetesprevention efforts discussed below.

Preventing Diabetes in SingaporeAccording to the 2010 Singapore NationalHealth Survey, the crude diabetes preva-lence increased from 8.6% in 1992 to11.3% in 2010 (111). However, the age-standardized prevalence remained con-stant at ;11% during the two decades.Obesity prevalence has been rising in thelast decade from 6 to 11%. The effect ofrising obesity on diabetes prevalence willlikely only be evident in one to two de-cades. It is estimated that Singapore willhave half a million people with diabetesby 2020 and that this will rise to 1 millionby 2050, double an earlier projection thatwas based on aging alone (112). The pub-lic health policy implication is clearly notjust toward increasing the capability ofdealing with diabetes once it has arisen(increased capacity and new models ofcare) but also moving upstream to pri-mary prevention.The traditional approach to preventing

lifestyle-related diseases in Singapore isto provide public education with a strongemphasis on individual responsibility.Singapore’s Healthier Hawker Pro-gram provides a case study of this ap-proach. It is part of The Healthy LivingMaster Plan, a major paradigm shift rec-ognizing the need for multisectoral andintegrated approaches to intervention.Hawker centers are a quintessential

feature of the Singaporean food land-scape and house a variety of cookedfood stalls popular for their conve-nience, competitive prices, and diver-sity. In 2010, ;60% of Singaporeansate at least four times per week athawker centers, food courts, and coffeeshop stalls. Improving the nutritionalquality of foods sold at hawker centersprovides an important opportunity forwidespread dietary modification amongSingaporeans (113).The traditional model of workplace

safety and health in Singapore is focused

on prevention of accidents and occu-pational diseases. However, with theincreasing incidence and earlier onsetof diabetes and delay in the retire-ment age, there will be an increasingnumber of people with diabetes in theworking population. It was estimatedthat there were 180,000 people withdiabetes in Singapore’s working popu-lation in 2010. The cost to the econ-omy was $1 billion, primarily due toproductivity loss. This is ofmajor concernnot only to the government but also in-dividual employers. The Total WorkplaceSafety and Health (TWSH) system waslaunched jointly by the Ministries ofManpower and Health as a nationalprogram to provide a new model ofcare for the safety and health of theworking population (114).

CONCLUSIONS

The scenario presented in this reviewposes huge social and economic prob-lems to most nations in Asia and thePacific and is likely to impede nationaland indeed regional and global devel-opment. More action, particularly re-search, is required to understand thedrivers of the epidemic, particularlythose relating to developmental originsof T2DM, to provide a rationale for pre-vention strategies to address this risingpublic health “tsunami.” Primordialprevention strategies instituted in po-tential mothers, through prevention ofmalnutrition in utero and in childhood,and through healthy diets and adequatephysical activity (“life course approach”)are important additional elements to beincluded in future strategies for T2DMprevention (85). More action is alsoneeded to effectively implement life-style changes on a societal level tostem the tide of the epidemic. Unlessdrastic steps are taken through nationalprevention programs in Asia and the Pa-cific to curb the escalating trends in all ofthe countries, the social, economic, andhealth care challenges will be insur-mountable (1).

Because estimates of the diabetesburden have important implicationsfor future public health planning, it isessential that such estimates providereliable data. This review highlightsthe paucity of these data in a numberof Asian and Pacific nations and theneed for improving the collection of

epidemiological data and its interpreta-tion for public health planning to re-source and direct urgently neededprevention activities. This applies par-ticularly to lower- and middle-incomenations in these regions. India and Chinaalready have a huge burden from dia-betes, and they provide the largest di-aspora communities worldwide. Whatis already happening in Asia and thePacific in terms of the diabetes epi-demic and the complications and so-cioeconomic outcomes provides adaunting lesson for what can happenglobally.

Funding. R.C.W.M. acknowledges supportfrom the Research Grants Council Theme-based Research Scheme (T12-402/13N), theResearch Grants Council General ResearchFund (CU471713), and the European Foun-dation for the Study of Diabetes/ChineseDiabetes Society/Lilly Programme for Collab-orative Research Between China and Europe.J.E.S. is supported by a National Health andMedical Research Council Senior ResearchFellowship.Duality of Interest. No potential conflicts ofinterest relevant to this article were reported.Author Contributions. A.N., R.C.W.M., K.S.C.,J.E.S., and P.Z.Z. researched data, contributed todiscussion, and wrote, reviewed, and edited themanuscript. A.R., C.S., and J.C.N.C. contributedto discussion and reviewed and edited the man-uscript. All authors approved submission of themanuscript for publication.

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