ε Freund Publishing House Ltd..

London Journal of Pediatric Endocrinology & Metabolism, 13, 1 3 9 5 - 1 4 0 2 ( 2 0 0 0 )

Emergence of Type 2 Diabetes Mellitus in Children:

Epidemiological Evidence*
Anne Fagot-Campagna

Division of Diabetes Translation, National Center for Chronic Disease Prevention and Health Promotion,
Centers for Disease Control and Prevention, Atlanta, Georgia, USA

ABSTRACT KEY WORDS

There have been numerous recent reports of adolescents, children, epidemiology, insulin
case series of type 2 diabetes mellitus (DM) in resistance, obesity, public health, type 2 diabetes
American Indian, African-American, Hispanic, mellitus
Asian-American and white children from North
America. A similar phenomenon has also been
INTRODUCTION
described in several other countries. Prevalence
and incidence estimates vary depending on the
Type 1 diabetes mellitus (DM) has been con-
age and ethnicity of the population, but it is
sidered the predominant type of childhood-onset
estimated that type 2 DM represents 8-45% of
DM1. However, since the 1970s, there have been
patients with DM currently diagnosed in large
reports of case series of type 2 DM in adolescents
US pediatric centers; however, this is likely to be
from American Indian and First Nations popu-
an underestimation and incidence is probably
lations, including the Pima Indians from Arizona,
rising. The young patients diagnosed with type 2
USA, in 19792, and the Cree and Ojibway Indians
DM in the USA were generally overweight, had
from Ontario and Manitoba, Canada, in the
a strong family history of type 2 DM and often
1980s3,4. Furthermore, by the 1990s, physicians
had signs of insulin resistance. The majority
began to recognize the presence of type 2 DM in
belonged to ethnic groups at high risk for type 2
North American white, African-American, Asian-
DM. More girls than boys were diagnosed. The
American and Hispanic children5. Also in the
few data on follow-up available suggest a high
1990s, similar reports emerged from other
prevalence of microvascular and macrovascular A7 β
complications among young adults who deve- countries, including Japan · , Hong Kong , Bang-
loped type 2 DM during childhood. Type 2 DM ladesh9, Libya10, Australia" and New Zealand12.
in children has recently been recognized as a This paper describes epidemiological evidence of
potential public health problem in North the appearance of type 2 DM in children from
America. As obesity is currently on the increase several countries and potential secular trends of the
in several industrialized or industrializing disease.
countries, a similar increase in type 2 DM in
children may soon emerge worldwide, and this PREVALENCE AND INCIDENCE
will require preventative measures.
Table 1 summarizes the prevalence and inci-
dence of type 2 DM in children identified through
Reprint address:
different population screening programs6'9,13"8.
Anne Fagot-Campagna
Division of Diabetes Translation
Table 2 summarizes estimates from diabetes regist-
National Center for Chronic Disease Prevention ries or clinics, which include only diagnosed and
and Health Promotion
Centers for Disease Control and Prevention
4770 Buford Highway NE (MS-K68) •Note: The views expressed in this paper are those of the
Atlanta, GA 30341, USA author and do not necessarily represent the official position of
e-mail: adf8@cdc.gov the Centers for Disease Control and Prevention.

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1396 A. FAGOT-CAMPAGNA

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 EMERGENCE OF TYPE 2 D M IN C H I L D R E N 1397

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1398 A. FAGOT-CAMPAGNA
notified cases 4101319 " 22 . In both tables, patients
with type 1 DM were included when they could not
be distinguished from patients with type 2 DM.
Generally, the estimates of diagnosed type 2 DM
(Table 2) are much lower than the estimates from
population screening (Table 1). This difference
suggests that undiagnosed type 2 DM may be
common among children, just as it is among adults
in the USA, where there is one undiagnosed adult
with type 2 DM for every two or three diagnosed
adults 23 .
SECULAR TRENDS IN PREVALENCE AND
INCIDENCE
Several studies suggest evidence of an increas-
ing secular trend in type 2 DM among children. In
15-19 year-old Pima Indians in Arizona, USA, the
prevalence of type 2 DM, ascertained by population
screening, rose from 24 to 38 per 1000 boys (58%
increase) and from 27 to 53 per 1000 girls (96%
increase) between the periods of 1967-1976 and
1987-1996 (ρ < 0.0001) 17 . Data from the US Indian
Health Service clinics show that the prevalence of
diagnosed DM (all types) among 15-19 year-old
American Indians rose from 2.9 per 1000 in 1988 to
4.5 per 1000 in 1996 (p < 0.001), which represents
an increase of 55% . Most of this increase is
probably due to type 2 DM because American
Indians are considerably more likely to develop
type 2 than type l 2 4 . In 10-19 year-old African-
American and white children referred to a major
pediatric center in Cincinnati, Ohio, USA, the
incidence of diagnosed type 2 DM increased 10-
fold, from 0.7 per 100,000 in 1982 to 7.2 per
100,000 in 1994 й .
Between the periods of 1976-1980 and 1991-
1995 in Tokyo, Japan, the annual incidence of type
2 DM (estimated from systematic screening by
urine testing and diagnosed by an oral glucose
tolerance test [OGTT]) increased 10-fold among
primary school children, from 0.2 to 2.0 per
100,000, and almost doubled among junior high
school children, from 7.3 to 13.9 per 100,ООО6.
According to reports from the US registry of
type 1 DM in Allegheny County, Pennsylvania, the
annual incidence of diagnosed DM (based on
insulin treatment started at diagnosis) among 15-
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19 year-old African-Americans increased from 7.6
to 13.8 per 100,000 between the periods of 1980-
1984 and 1985-1989, and to 30.4 per 100,000 in
1990-1994 20 . In the Chicago, Illinois, area during
1985-1994, the annual incidence of diagnosed DM
among 15-19 year-old adolescents was much higher
in African-Americans than in Hispanics (20.5
versus 12.2 per 100,ООО)21. The high incidence
rates in these two diabetes registries may be
partially attributed to an increase in the number of
cases of type 2 DM, which could have been
misclassified as type 1 and treated with insulin at
diagnosis.
Pediatric endocrinologists previously considered
that type 2 DM accounted for about 1% of the cases
of childhood diabetes 1 . However, recent clinical
case series from California, Texas, Ohio, Arkansas,
South Carolina and Illinois in the USA indicate that
type 2 DM now accounts for 8-45% of newly
diagnosed DM among children, which suggests a
secular trend for this disease 5 . Most of the variation
in the percentages reported is probably due to age
and racial/ethnic differences among the populations
studied.
Part of the secular trend for diagnosed type 2
DM (Table 2) may be attributed to increases in the
diagnosis and reporting of patients, but these
increases generally did not occur in the USA until
the end of the 1990s. Better diagnosis and reporting
also cannot explain the trends observed in popu-
lation-based studies.
CHARACTERISTICS AND RISK FACTORS
A detailed review of case series and charac-
teristics of 578 North American children with type
2 DM has been previously published 5 . Most of the
clinical reports provided evidence of the absence of
autoimmunity and any family trait that would
suggest types of DM other than type 2. Children
were usually diagnosed with type 2 DM after the
age of 10 years or after the first signs of puberty.
They were also generally overweight, had a strong
family history of type 2 DM and often had signs of
insulin resistance, including acanthosis nigricans,
hypertension or dyslipidemia. More girls than boys
were diagnosed with type 2 DM. Although patients
were reported from various racial/ethnic groups in
JOURNAL OF PEDIATRIC ENDOCRINOLOGY & METABOLISM
 EMERGENCE OF TYPE 2 DM IN CHILDREN
the USA, the majority of children belonged to
certain ethnic groups at high risk for type 2 DM,
such as American Indians, African-Americans,
Asian-Americans and Hispanics5. A recent report
from the USA describes the characteristics of 42
family members of 11 children with type 2 DM25.
As expected, these families shared common risk
factors, including obesity with central distribution,
high-fat and low-fiber intake, and insufficient
regular physical activity. This study demonstrated
that family and environment play an important role
in determining the risk of type 2 DM.
A report based on 124 patients diagnosed in
Tokyo, Japan, indicated that Japanese children with
type 2 DM generally had the same characteristics as
their North American counterparts, except that as
many as 16% were not overweight7. In addition,
height was reported as taller than average7. In Hong
Kong, a case series of patients with early-onset type
2 DM (including a few pediatric patients) reported
that 71% of young men and 35% of young women
were not obese8. However, some of these young
people may have had types of DM other than type
226
COMPLICATIONS AND FOLLOW-UP
Studies from the USA have found numerous
disparities in access to health care and its delivery
in certain ethnic populations, as well as specific
excess mortality in children with type 1 DM from
these populations . Therefore, excess burden may
exist in children with type 2 DM from certain
racial/ethnic groups.
Available data include few prospective studies,
representing only American Pima Indian28, Japa-
nese7,29'30 and New Zealand Maori12 children.
Among Pima Indian children, cardiovascular risk
factors, including dyslipidemia, hypertension and
microalbuminuria, were often present at the time of
diagnosis of type 2 DM28. Of 37 of these young
Pima Indian patients (mean age 26 years), who
were followed for a mean duration of 10 years,
microalbuminuria was present in 58% and macro-
albuminuria in 16%.
According to a Tokyo study of 1065 Japanese
patients with early-onset type 2 DM (mean age at
diagnosis 23 years), including a few pediatric
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1399
patients, a subgroup of 135 patients developed
proliferative retinopathy before age 35 years, and
32 of these patients became blind at a mean age of
32 years29. Additionally, 14 of these 135 patients
developed cardiovascular disease at a mean age of
36 years, 81 developed nephropathy, 42 developed
renal insufficiency, and 35 developed end-stage
renal disease requiring dialysis at a mean age of 35
years. Another report on a subgroup of 426 of these
study patients observed that 41 developed persistent
proteinuria after a mean follow-up of 6.8 years30.
The corresponding incidence density for nephro-
pathy was as high as 14.1 (range 10.4-19.1) per
1000 person-years, which is similar to that ob-
served in the Diabetes Control and Complications
Trial (DCCT) cohort of type 1 DM patients with
similar characteristics; however, the mean specific
subfraction of glycosylated hemoglobin was lower
in the Japanese patients than in the DCCT patients
(7.5% versus 9.0%)31. In another report of 45
Japanese children with type 2 DM, 25% had
incipient retinopathy, which was detected by fluor-
escent angiography when DM was diagnosed7.
In a New Zealand study, 28 Maori patients with
type 2 DM (age range 11-49 years) were identified
from a large service registry12. They had been
diagnosed between the ages of 5 and 29 years, and
the mean duration of DM was 10 years. Micro-
albuminuria or nephropathy was present in 62% of
these patients, retinopathy in 35% and cardio-
vascular risk factors in 25-50%. In contrast, 18
Maori patients with type 1 DM, who were
identified from the same registry and had a similar
duration of DM but were younger at diagnosis,
were less likely to have microalbuminuria or
nephropathy (18%) and retinopathy (17%).
These few studies demonstrate that a high
prevalence of microvascular and macrovascular
complications is indeed likely among young adults
who develop type 2 DM during childhood. Delayed
diagnosis, poor glucose control during the teenage
years and the long duration of DM may all pre-
dispose to early onset of complications. Charac-
teristics such as a high degree of insulin resistance,
clustering of cardiovascular risk factors, ethnic/
racial susceptibility or environmental exposure
leading to renal disease, lack of access to continu-
ous high-quality care or other socioeconomic
1400 A. F A G O T - C A M P A G N A
disadvantages may also be important determinants
of complications.
SECULAR TRENDS IN MAJOR RISK FACTORS
Just as obesity is a demonstrated major risk
factor for the development of type 2 DM in adults,
the emergence of type 2 DM in children has
paralleled or followed the epidemic of childhood
obesity observed in the USA32 and Japan6.
According to the most recent national survey in the
USA, the prevalence of overweight in children aged
6-17 years was 22% and 11%, based on the age-
and sex-specific 85th and 95th percentiles,
respectively, for body mass index32. Most of the
increase in prevalence occurred between the
periods of 1976-1980 and 1988-1991, before the
recognition of type 2 DM in children in the USA.
In Japan, although the total daily energy intake
per capita did not change between 1955 and 1995,
the intake of total fat and animal fat increased 3-
and 4.6-fold, respectively, but the majority of this
increased intake occurred before 19756. Animal
protein intake also doubled during the same period.
Between 1975 and 1995, the prevalence of obesity
in Tokyo children increased from less than 5% to
more than 8%, while the incidence of type 2 DM
more than tripled.
Although most children with type 2 DM in the
USA are severely overweight, only one prospective
population-based study has examined the relation-
ship between obesity and type 2 DM in children17.
The mean weight of Pima Indian children increased
significantly between the periods of 1967-1976 and
1987-1996 (p < 0.0001), and the prevalence of DM
increased significantly with increasing relative
weight (p < 0.001). In the same study, however,
exposure to DM in utero was also a major
determinant of type 2 DM, possibly perpetuating a
vicious cycle of exposure from a mother to a
daughter who may later become a mother.
CONCLUSIONS
In the 1990s, type 2 DM in children became
recognized as a potentiai public health problem in
North America 5,3 . With the increase in obesity in
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several industrialized or industrializing countries, a
similar increase in type 2 DM in children may soon
emerge worldwide, as it already has in Japan6'7,29,30,
Hong Kong8, Bangladesh9, Libya10, Australia" and
New Zealand12.
During 1999-2000, several agencies and
organizations met in North America to assess
current knowledge of type 2 DM in children and
needs for further research and improving health
care delivery. Awareness of the disease is rising
among health care providers in North America, and
consensus statements have been issued to facilitate
the diagnosis, typology and treatment of type 2 DM
in children, as well as to provide recommendations
for the identification of patients with this dis-
order33. Several important epidemiological and
public health questions related to the magnitude,
secular trends, characteristics, potentially modi-
fiable risk factors, long-term complications, quality
of care and quality of life need to be answered to
improve the understanding of type 2 DM in child-
ren and to assist public health planning.
DM is a disease that is devastating to the
individual and to society. It is associated with loss
in quality of life, numerous complications, pre-
mature death and high economic costs. The
incidence of type 1 DM is increasing worldwide34,
and it is projected that 300 million people in the
world may have DM by the year 20 2 535.
Furthermore, the emergence of type 2 DM in
children is likely to lead to an additional burden,
not only on the young generation, but also on
society in general. As many chronic diseases
become more prevalent around the world and start
to appear in children, the need for preventative
measures becomes increasingly urgent.
ACKNOWLEDGEMENTS
The author would like to thank Drs David S.
Freedman and Heather Dean for communication of
unpublished analyses.
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