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Global epidemiology of type 1 diabetes in young adults and adults: a systematic review

  • Paula A Diaz-Valencia1, 2Email author,
  • Pierre Bougnères1, 3 and
  • Alain-Jacques Valleron1, 2
BMC Public Health201515:255

https://doi.org/10.1186/s12889-015-1591-y

Received: 1 December 2014

Accepted: 27 February 2015

Published: 17 March 2015

Abstract

Background

Although type 1 diabetes (T1D) can affect patients of all ages, most epidemiological studies of T1D focus on disease forms with clinical diagnosis during childhood and adolescence. Clinically, adult T1D is difficult to discriminate from certain forms of Type 2 Diabetes (T2D) and from Latent Autoimmune Diabetes in Adults (LADA).

We searched the information available worldwide on the incidence of T1D among individuals over 15 years of age, and which diagnostic criteria should be used use to qualify T1D in adults. We then studied the variation of T1D incidence with age in adults, and compared it to the incidence in the <15 years-old.

Methods

A systematic review of the literature was performed to retrieve original papers in English, French and Spanish published up to November 6, 2014, reporting the incidence of T1D among individuals aged over 15 years. The study was carried out according to the PRISMA recommendations.

Results

We retrieved information reporting incidence of T1D among individuals aged more than 15 years in 35 countries, and published in 70 articles between 1982 and 2014. Specific anti-beta-cell proteins or C-peptide detection were performed in 14 of 70 articles (20%). The most frequent diagnostic criteria used were clinical symptoms and immediate insulin therapy. Country-to-country variations of incidence in those aged >15 years paralleled those of children in all age groups. T1D incidence was larger in males than in females in 44 of the 54 (81%) studies reporting incidence by sex in people >15 years of age. The overall mean male-to-female ratio in the review was 1.47 (95% CI = 1.33-1.60, SD = 0.49, n = 54, p = <0.0001). Overall, T1D incidence decreased in adulthood, after the age of 14 years.

Conclusions

Few studies on epidemiology of T1D in adults are available worldwide, as compared to those reporting on children with T1D. The geographical variations of T1D incidence in adults parallel those reported in children. As opposed to what is known in children, the incidence is generally larger in males than in females. There is an unmet need to evaluate the incidence of autoimmune T1D in adults, using specific autoantibody detection, and to better analyze epidemiological specificities – if any – of adult T1D.

PROSPERO registration number

CRD42012002369.

Keywords

Type 1 diabetes Systematic review Adults Incidence Epidemiology

Background

The worldwide epidemiology of childhood Type 1 diabetes (T1D) was extensively described in the 6th edition of the International Diabetes Federation (IDF) [1]. Data were retrieved in approximately 45% of the countries [1-4]. In contrast, we are unaware of a similar review on the worldwide epidemiology of adult T1D diabetes, although T1D is known to occur even late in adults [5-7]. A major limitation of the epidemiology of T1D in adults is certainly the difficulty there is to distinguish it from Type 2 diabetes (T2D) requiring insulin treatment or from Latent Autoimmune Diabetes in Adults (LADA), when specific markers of autoimmunity are not searched.

Here, our primary objective was to describe – through a systematic review of the literature – the available published information on adult T1D incidence, and the diagnostic criteria used for case definition. A secondary objective was to study how the variations of T1D incidence in adults mirrored those in children.

Methods

Literature review

A systematic review was conducted according to the PRISMA recommendations to retrieve original papers published in English, French and Spanish up to November 6th, 2014, in peer-reviewed journals reporting the incidence of T1D among individuals aged more than 15 years, in population-based studies (i.e. collected in a defined geographic area [8]) and reporting the diagnostic criteria used to define T1D.

The databases used for the literature search were Medline (PubMed), Google Scholar and Thomson Reuters (Web of Knowledge). The protocol of the search was registered in the International Prospective Register of Systematic Reviews (PROSPERO) and is available on http://www.crd.york.ac.uk/PROSPERO/display_record.asp?ID=CRD42012002369 (Registration number: 2012:CRD42012002369). Figure 1 presents the flow diagram of the bibliographic search, Additional file 1 for the full electronic search strategy, and Additional file 2 for the PRISMA checklist.
Figure 1

PRISMA Flow diagram bibliographic search strategies. * Kumar P, et al. Indian Med Assoc. 2008;106(11):708–711. ** The article: Radosevic B, et al. Pediatr Diabetes. 2013;14(4):273–4 gives information from two countries: 1) Bosnia and Herzegovina: Republic of Srpska and 2) Slovenia, Nationwide.

Data collection

For each study, the following information was extracted:
  • the identification of the study: authors, title, journal, publication year,

  • the period and country of study. The country was categorized by its World Health Organization (WHO) region and economic level: high-income (HIGH) or low- and middle-income (LMIC) [9],

  • the geographic coverage of the study: nationwide (when the study was performed in the entire nation) and local (when it was restricted to a given region, city, or a geographically defined population),

  • the diagnostic criteria used to define T1D in adults: detection of autoantibodies against beta-cells (such as: islet cell antibody (ICA), insulin autoantibody (IAA), islet antigen-2 autoantibody (IA-2), anti-glutamic acid decarboxylase antibodies (GAD)), measurement of the fasting C-peptide level [7], need for permanent insulin therapy, time when the administration of insulin therapy was started, and clinical signals of T1D diabetes such as ketosis, ketonuria and weight loss,

  • the sources of data/registers reporting T1D incidence in the studies, defined according to LaPorte et al. [10] as: primary source of information: a “well-established system of standardized registries for identifying new cases”, for example national or regional registers, secondary source of information: other different sources of cases “that would provide a check on the degree of ascertainment”, for example medical records or hospital discharges, and tertiary source of information: a third approach for identifying cases, for example, through surveillance system or death certificates,

  • the reported percentage of completeness/ascertainment between sources of information reporting incidence [10],

  • the incidence rates reported in the text, tables or graph (expressed as new cases per 100.000 persons/year) by sex and age classes,

  • additional information such as those concerning rural/urban, or ethnic differences.

Data analyses

The country distribution of the T1D incidence information and the analysis of the diagnostic criteria used were performed on the entire set of articles retrieved. For the few papers for which the results were presented by ethnic origin, we estimated the mean value of the incidence for the given period in the countries/regions concerned.

Correlation between adult and children T1D incidences

In the geographical correlation analyses between children and adult incidences, we considered for each country the more recent nationwide study published, or if not available, the last published set of local studies retrieved from a given area in the country; in addition, we included all published papers reporting auto-antibodies against beta-cells or C-peptide. To obtain an estimate of the incidence of T1D in children in the countries for which the adult incidence was available, we used the data provided by the same adult paper, when available. The incidence of T1D in children was not available in 9 of these papers included in the geographical correlation analyses. In this case, it was estimated through a separate systematic review focused on the corresponding countries and periods (see Additional file 3).

Statistics

Data were extracted from graphs using GraphClick [11].

The country-to-country co-variation of children and adult incidences was quantified by the Spearman correlation and a linear regression.

The R software (version 3.0.1) was used for statistical and graphic analyses [12].

Results

Description of the information obtained from the systematic review on adult T1D

Seventy articles reporting incidence of T1D in young adults and adults aged over than 15 years concerned one country, and one article concerning two countries were retrieved in this systematic review, resulting in a total of 71 studies covering 35 countries (Table 1). Twenty-four of the 71 studies were nationwide; 43 papers provided information on the T1D incidence in the age class 15–29 years, 26 in the age class 30–59 years, and 6 in the persons aged >60 years.
Table 1

Systematic review of T1D in adults, diagnostic criteria and sources of information

Study information

T1D diagnosis criteria in adults and young adults

Source of information and validation of ascertainment between sources

Country, area reported in the article

First author, publication year

Ref

Age range

Period

Detect. AA/C-Peptide

Need of insulin therapy

Administration insulin therapy

Clinical impression

Ketosis/ ketonuria

Weight loss

Primary

Secondary

Tertiary

% of ascertainment

African Region, LMIC

Mauritius: NW

Tuomileht J., 1993

[13]

0-19

1986-1990

No

Yes

From diagnosis

Yes

NA

NA

Medical reports

Medical statistics

NA

95.0

United Republic of Tanzania: Dar es Salaam

Swai A. B., 1993

[14]

0-19

1982-1991

No

Yes

From diagnosis

Yes

NA

NA

Medical reports

Hospital records

NA

NA

Eastern Mediterranean Region, LMIC

Iran (Islamic Republic of): Fars

Pishdad G. R., 2005

[15]

0-29

1990-1994

Yes (a)

Yes

From diagnosis

Yes

Yes

Yes

Medical reports from endocrinologists

Medical records

NA

100

Libyan Arab Jamahiriya: Benghazi

Kadiki O. A., 1996

[16]

0-34

1981-1990

No

Yes

From diagnosis

NA

Yes

NA

National Diabetes Program

Hospital registers

NA

95.0

Tunisia: Beja, Monastir, Gafsa

Ben Khalifa F., 1998

[17]

0-19

1990-1994

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

School health centers

NA

96.0

European Region, LMIC

Croatia: Zagreb

Roglic G., 1995

[18]

0- > 55

1988-1992

No

Yes

Within 1 week of diagnosis

Yes

Yes

NA

National Diabetes Program

Death certificates

Diabetes association

96.2

Estonia: NW

Kalits I., 1990

[19]

0- > 50

1988-1988

No

Yes

From diagnosis

Yes

Yes

Yes

NA

NA

NA

NA

Lithuania: NW

Ostrauskas R., 2011

[20]

15-34

1991-2008

No

Yes

Within 2 weeks of diagnosis

Yes

Yes

Yes

National Diabetes Program

Regional endocrinologist

Notes of patient insurance

86.8

Lithuania: NW

Pundziute-Lycka A., 2003

[21]

0-39

1991-2000

No

Yes

Within 2 weeks of diagnosis

Yes

Yes

NA

National Diabetes Program

Pediatrician and endocrinologist reports

Death certificates

91.2

Lithuania: NW

Ostrauskas R., 2000

[22]

15-39

1991-1997

No

Yes

Within 2 weeks of diagnosis

Yes

Yes

NA

National Diabetes Program

Pediatrician and endocrinologist reports

Death certificates

91.2

Poland: Bialystok

Kretowski A., 2001

[23]

0-29

1994-1998

No

Yes

From diagnosis

Yes

Yes

Yes

Pediatric and Internal medicine records

Hospital discharge registers

NA

98.5

Poland: Province of Rzeszow

Sobel-Maruniak A., 2006

[24]

0-29

1980-1999

No

Yes

From diagnosis

Yes

NA

NA

Pediatric and Internal medicine records

Others health care registers

NA

99.0

Poland: Province of Rzeszow

Grzywa M. A., 1995

[25]

0-29

1980-1992

No

Yes

From diagnosis

Yes

NA

NA

Pediatric and Internal medicine records

Others health care registers

NA

99.0

Poland: Warsaw

Wysock M. J., 1992

[26]

0-29

1983-1988

No

Yes

From diagnosis

Yes

NA

NA

Medical records from diabetic clinics

General practitioners and diabetologist registers

Death certificates

NA

Romania: Bucharest

Ionescu-Tirgoviste C., 1994

[27]

0- ≥ 85

1981-1991

No

Yes

From diagnosis

Yes

Yes

NA

Bucharest Diabetes Registry

NA

NA

NA

Slovakia: NW

Kyvik K O, 2004

[28]

15-29

1996-1997

No

Yes

From diagnosis

Yes

NA

NA

Pediatrician and endocrinologist reports

Other health care registers

NA

80.0

European Region, HIGH

Austria: Upper

Rami B., 2001

[29]

0-29

1994-1996

No

Yes

From diagnosis

Yes

NA

NA

Pediatricians and endocrinologists reports

Austrian Diabetes Association

NA

87.0

Belgium: Antwerp

Weets I., 2007

[30]

0-39

1989-2003

Yes

Yes

From diagnosis

Yes

NA

NA

Pediatricians and endocrinologists reports

General practitioners and diabetes nurses reports

Diabetes associations and self-reporting

97.0

Belgium: Antwerp

Weets I., 2002

[31]

0-39

1989-2000

Yes

Yes

From diagnosis

NA

NA

NA

Pediatrician and endocrinologist reports

General practitioner and diabetes nurse reports

Diabetes associations and self-reporting

93

Belgium: Antwerp

Vandewalle C., 1997

[32]

0-39

1989-1995

Yes

Yes

From diagnosis

Yes

Yes

Yes

Pediatrician and endocrinologist reports

General practitioner and diabetes nurse reports

Diabetes associations and self-reporting

85

Bosnia and Herzegovina: Republic of Srpska

Radosevic B., 2013

[33]

0-18

1998-2010

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

Insulin prescription registers

NA

100

Denmark: Copenhagen and Frederiksborg

Molbak A. G., 1994

[34]

30-95

1973-1977

Yes (b)

Yes

From diagnosis

Yes

Yes

Yes

Hospital discharges

General practitioners and diabetologist registers and death certificates

Missing coding of T1D diagnosis in hospital admissions

99.0

Finland: NW

Lammi N., 2007

[35]

15-39

1992-1996

Yes

Yes

From diagnosis

Yes

NA

NA

National Diabetes Program

Hospital discharge registers

Drug reimbursement registers

88.0

France: Aquitaine, Lorraine, Basse Normandie, Haute Normandie

Charkaluk M. L, 2002

[36]

0-19

1988-1997

No

Yes

None declared

NA

NA

NA

Prospective registers

French Social Security registers

NA

96.0

France: Aquitaine, Lorraine, Basse Normandie, Haute Normandie

Levy-Marchal, C., 1998

[37]

0-19

1988-1995

No

Yes

None declared

NA

NA

NA

Prospective registers

French Social Security registers

NA

96.0

Israel: NW

Blumenfeld O., 2014

[38]

0-17

1997-2010

No

Yes

From diagnosis

Yes

NA

NA

Israel juvenile diabetes register

Israel Center for Disease Control

NA

NA

Israel: NW

Sella T., 2011

[39]

0-17

2000-2008

No

Yes

None declared

Yes

NA

NA

Israel juvenile diabetes register

Israel Center for Disease Control

NA

NA

Israel: NW

Koton S., 2007

[40]

0-17

1997-2003

No

Yes

From diagnosis

Yes

NA

NA

Israel juvenile diabetes register

NA

NA

NA

Italy: Lombardie

Garancini, P., 1991†

[41]

0-34

1981-1982

No

Yes

None declared

NA

NA

NA

Hospital discharge records

Hospital admission records

NA

85.7

Italy: Pavia

Tenconi M. T., 1995

[42]

0-29

1988-1992

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

Drug registers

NA

100

Italy: Sardinia

Muntoni S, 1992

[43]

0-29

1989-1990

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

Diabetes association

NA

92.8

Italy: Sardinia (Oristano)

Frongia O., 1997

[44]

0-29

1993-1996

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

Drug registers

NA

100

Italy: Turin

Bruno G., 2009

[45]

15-29

2000-2004

Yes

Yes

Within 6 months of diagnosis

NA

NA

NA

Hospital records

Drug registers

NA

NA

Italy: Turin

Bruno G., 2005

[46]

30-49

1999-2001

Yes

Yes

Within 6 months of diagnosis

NA

Yes

NA

Diabetes clinics

Drug registers

NA

99.0

Italy: Turin

Bruno G., 1993

[47]

0-29

1984-1988

No

Yes

From diagnosis

NA

Yes

NA

Diabetic clinics records

Hospital discharge records

NA

97.0

Luxembourg: NW

De Beaufort C. E., 1988

[48]

0-19

1977-1986

No

Yes

None declared

NA

NA

NA

Pediatric and Internal medicine records

Dutch Diabetes Association

NA

100

Malta: NW

Schranz A. G., 1989

[49]

0-24

1980-1987

No

Yes

Within 3 moths of diagnosis

Yes

Yes

Yes

Medical reports

Diabetic clinic records

NA

NA

Netherlands: NW

Ruwaard D., 1994

[50]

0-19

1988-1990

No

Yes

None declared

NA

NA

NA

Pediatric and Internal medicine records

NA

NA

81.0

Norway: NW

Joner G., 1991

[51]

15-29

1978-1982

No

Yes

From diagnosis

NA

NA

NA

Pediatricians and endocrinologists reports

Hospital records

NA

90.0

Slovenia: NW

Radosevic B., 2013

[33]

0-18

1998-2010

No

Yes

From diagnosis

Yes

NA

NA

Slovenian National Registry of Childhood diabetes

Insulin prescription registers

NA

100

Spain: Badajoz

Morales-Perez F. M., 2000

[52]

0-29

1992-1996

No

Yes

From diagnosis

Yes

Yes

NA

Pediatricians and endocrinologists reports

Diabetic clinic records

NA

95.0

Spain: Canarias Islands

Carrillo Dominguez, A., 2000

[53]

0-30

1995-1996

No

Yes

None declared

Yes

NA

Yes

Hospital records and Endocrinologist reports

Diabetes association reports and sales on blood glucose monitors

NA

90.1

Spain: Catalonia

Abellana R., 2009

[54]

0-29

1989-1998

Yes (c)

Yes

From diagnosis

Yes

Yes

NA

Catalan Registry of Type 1 Diabetes

Summer camps, associations, and prescription data

NA

90.0

Spain: Catalonia

Goday A., 1992

[55]

0-29

1987-1990

No

Yes

From diagnosis

Yes

NA

NA

Catalan Registry of Type 1 Diabetes

Summer camps, patient associations, and prescription data

NA

90.1

Spain: Navarra

Forga L., 2014

[56]

0- > 45

2009-2012

Yes

Yes

Within 6 months of diagnosis

Yes

Yes

NA

Hospital records

Electronic medical records, diabetes associations

NA

98.4

Spain: Navarra

Forga L., 2013

[57]

0-79

2009-2011

Yes

Yes

Within 6 months of diagnosis

Yes

Yes

NA

Hospital records

Electronic medical records, diabetes associations

NA

98.4

Sweden: NW

Dahlquist G. G., 2011

[58]

0-34

1983-2007

No

Yes

From diagnosis

Yes

Yes

Yes

National Diabetes Program

Pediatricians and endocrinologist reports

NA

96.0

Sweden: NW

Östman J., 2008

[59]

15-34

1983-2002

No

Yes

From diagnosis

Yes

NA

NA

National Diabetes Program

Pediatrician and endocrinologist reports

Computer-based patient administrative register

82

Sweden: NW

Pundziute-Lycka A., 2002

[60]

0-34

1983-1998

No

Yes

From diagnosis

Yes

Yes

Yes

National Diabetes Program

Pediatrician and endocrinologist reports

Computer-based patient administrative register

91.2

Sweden: NW

Nyström L., 1992

[61]

0-34

1983-1987

No

Yes

None declared

NA

NA

NA

National Diabetes Program

Hospital admission and discharge registers

NA

89

Sweden: NW

Blohme G., 1992

[62]

15-34

1983-1987

No

Yes

From diagnosis

Yes

Yes

Yes

National Diabetes Program

Hospital admission and discharge registers

NA

NA

Sweden: Kronoberg

Thunander M., 2008

[63]

0-100

1998-2001

Yes

Yes

Within 4 weeks of diagnosis

Yes

Yes

NA

Opportunistic screening of all adult patients in contact with the medical care system

Departments of ophthalmology

NA

98.0

United Kingdom: NW

Imkampe A. K., 2011

[64]

0-34

1991-2008

No

Yes

Within 3 moths of diagnosis

Yes

NA

NA

National Diabetes Program

Pediatricians and endocrinologist reports

NA

NA

United Kingdom: Oxford region

Bingley P. J., 1989

[65]

0-21

1985-1986

No

Yes

From diagnosis

Yes

NA

NA

Medical reports from general practioners and pediatricians

Regional hospital records

NA

95.0

Region of the Americas, LMIC

Barbados: NW

Jordan O. W., 1994

[66]

0-29

1982-1991

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

Others health care registers

NA

94.0

Region of the Americas, HIGH

Canada: Quebec

Legault L., 2006

[67]

0-18

2000

No

Yes

None declared

NA

NA

NA

Departmental program: Régie des Rentes du Québec program

NA

NA

NA

United States of America: Alabama (Jefferson County)

Wagenknecht L. E., 1991

[68]

0-19

1979-1988

No

Yes

None declared

NA

NA

NA

Hospital records

Summer camps, patient associations, and prescription data

NA

NA

United States of America: Alabama (Jefferson County)

Wagenknecht L. E.,1989

[69]

0-19

1979-1985

No

Yes

From diagnosis

Yes

NA

NA

Hospital records

Association registers

NA

95.0

United States of America: Colorado

Vehik K., 2007

[70]

0-17

2000-2004

No

Yes

Within 2 weeks of diagnosis

Yes

NA

NA

Pediatricians and endocrinologists reports

Other health care registers

The SEARCH Study

96.5

United States of America: Colorado

Kostraba J. N., 1992

[71]

0-17

1978-1988

No

Yes

Within 2 weeks of diagnosis

Yes

NA

NA

Pediatricians and endocrinologists reports

Hospital registers

NA

93.3

United States of America: Pennsylvania (Allegheny)

Libman I. M., 1998

[72]

0-19

1990-1994

No

Yes

From diagnosis

Yes

NA

NA

Medical reports

General practitioners and diabetes nurses reports

NA

97.7

United States of America: Rhode Island

Fishbein H. A., 1982

[73]

0-29

1979-1980

No

Yes

None declared

NA

NA

NA

Medical reports

Insulin prescription registers

NA

NA

United States of America: five areas §

Bell R., 2009

[74]

0-19

2002-2005

Yes

Yes

From diagnosis

Yes

NA

NA

Medical reports

Other health care registers

The SEARCH Study

NA

United States of America: Wisconsin

Allen C., 1986

[75]

0-29

1970-1979

No

Yes

From diagnosis

Yes

NA

NA

Hospital discharges

Pediatricians and endocrinologist reports

NA

90.0

United States of America: The United States Navy

Gorham C., 1993

[76]

17-34

1974-1988

No

NA*

None declared

Yes

NA

NA

Hospital discharges

NA

NA

NA

Western Pacific Region, HIGH

Australia: New South Wales

Tran F., 2014

[77]

10-18

2001-2008

No

Yes

NA

Yes

NA

Yes

Endocrine group diabetes register

National diabetes register

NA

96.0

Australia: Sydney (Southern Metropolitan Health Region)

Sutton L., 1989

[78]

0-19

1984-1987

No

Yes

From diagnosis

Yes

NA

NA

Medical reports from general practioners and pediatricians

Schools in the area

Syringe register

NA

Japan: Osaka

Sasaki A., 1992

[79]

0-18

1978-1988

No

Yes

None declared

Yes

Yes

NA

Medical benefits system

NA

NA

NA

New Zealand: Canterbury

Scott, R. S., 1991

[80]

0- ≥ 80

1981-1986

No

Yes

Within 1 year of diagnosis

Yes

NA

Yes

Community-based surveys administrated in pharmacies where diabetic patients acquired their insulin supplies

Hospital admission and discharge registers and diabetologist

NA

95.0

Other Regions currently non WHO

Taiwan: NW

Lin W.-H., 2013

[81]

0- ≥ 60

1999-2010

Yes

Yes

None declared

Yes

Yes

NA

National Health Insure register and Illness certificates

Random sample of a database used to reimbursements

NA

98.3

US Virgin Islands: NW

Washington R. E., 2013

[82]

0-19

2001-2010

No

Yes

From diagnosis

Yes

Yes

Yes

Medical reports

Medical providers

NA

98.7

WHO Member States are divided into high-income (HIGH) or low- and middle-income (LMIC) states [30]. AA: autoantibodies, NW: Nation-wide study, NA: Unavailable data. (a) When there were diagnostic doubts, (b) Only for patients aged over 40 years at onset, (c) Not performed in all cases; the author of this study was contacted to confirm the proportion of these cases, but by the time of submission of this paper no answer was available. T1D: Type 1 Diabetes. Highlighted: reports of the systematic review using the autoantibodies/C-peptide as diagnosis criteria. () Studies used in the statistical analyses. (*) Data were not available but researchers assumed that patients have had T1D based on their average of age. (§) Ohio (8 counties), Washington State (5 counties), South Carolina, Colorado, California.

A primary source of information was reported in 99% (70 of 71) of the studies: among these reported sources, 60% (42 of 70) were from medical/hospital records, 36% (25 of 70) from national or regional registers, and 4% (3 of 70) from other sources, such as community-based surveys; a secondary source of information was reported in 90% (64 of 71) of the studies: among these reported sources, 58% (37 of 64) were from medical/hospital records, 16% (10 of 64) from associations of patients, 14% (9 of 64) from drug or supplies prescription registers, 8% (5 of 64) from national or regional registers, and 5% (3 of 64) from death certificates and schools registers; finally, a tertiary source of information was reported in 21% (15 of 71) of the studies: among these reported sources, 27% (4 of 15) were from national or regional registers, 27% (4 of 15) from associations of patients, 20% (3 of 15) from death certificates, 20% (3 of 15) from drug or supplies prescription registers, and 7% (1 of 15) from medical registers; see details in Table 1. Percentage of ascertainment (completeness) between sources of information was evaluated in 53 of 71 (75%) studies. The mean percentage of ascertainment of these 53 studies was 94% (Table 1).

In the group of young adults (15–19), the lowest incidence of T1D was reported in Mauritius, (1.1/100.000 persons/year) [13], and the highest in Estonia (39.9/100.000 persons/year) [19]. In the 70–79 year age group, the lowest incidence was reported in Navarra, Spain (0.8/100.000 persons/year) [57] and the highest in Kronoberg, Sweden (55/100.000 persons /year) [63]. The details of all retrieved incidence by study and age classes are in Additional file 4: Table S1.

Diagnostic criteria used to define T1D in adults reported in 71 epidemiological studies

Autoantibodies against beta-cell antigens or the C-peptide were included in the T1D diagnostic criteria in 14 studies [15,30-32,34,35,45,46,54,56,57,63,74,81], detection of ICAs was reported in 9 studies [15,30-32,34,45,46,54,63], IAA in 4 studies [30-32,54], IA2 in 5 studies [30-32,56,57], and GAD in 11 studies [30-32,35,45,46,56,57,63,74,81]. The C-peptide was measured in 7 studies. In one paper difference of auto-antibodies by age group (0–19) was explored but no significant differences were detected [74]. The other reported diagnostic criteria for T1D were the need for insulin therapy (reported in 70 of 71 studies), clinical symptoms of diabetes (reported in 56 of 71 studies), low or normal body weight (14 of 71 studies), and ketosis or ketonuria (26 of 71 studies). The details are shown in Table 1.

Comparison of adult and children T1D incidences

The variations of incidence of T1D in adults with country and age were studied in each area for which we retrieved information on a geographically defined population. This concerned 35 countries.

Variation of T1D incidence with age in adults

In 23 out of 35 (66%) countries (55 of 71 studies), the incidence of T1D was higher in the age range of 0–14 compared with 15–19 years. When restricted to the 14 reports for which the criteria of diagnosis of T1D were auto-antibodies against beta-cells or C-peptide detection, the variation of adult incidence with age showed a consistent decrease after the age of 14 years (Figure 2 and Additional file 4: Table S1).
Figure 2

Age variation of incidence from childhood to adult age. On this figure, the adult estimates of incidence were taken from the 14 reports of the systematic review using the autoantibodies/C-peptide as diagnostic criteria. Full lines correspond to articles from which both child as well as adult information could be retrieved. The dotted lines are those for which the child information was searched in the same country as in the adult paper, but was from a different paper (see Additional file 3 for details on this literature search). The corresponding countries are shown as: BE1: Belgium (2007) [30]; BE2: Belgium (2002) [31]; BE3: Belgium (1997) [32]; DK: Denmark [34]; ES1: Spain, Catalonia [54]; ES2: Spain, Navarra (2014) [56]; ES3: Spain, Navarra (2013) [57]; FI: Finland [35]; IR: Iran (Islamic Republic of) [15]; IT: Italy [45,46]; SE: Sweden [63], TW: Taiwan [81]; US: United States of America [74].

Geographical correlation of adult and child T1D incidence

A significant geographical correlation, as measured by the Spearman correlation coefficient, was found between adult T1D incidence and 0–14 incidence in the age classes 15–19 years, 20–24 years, 25–29 years, 30–34 years and overall in the entire 15–60 group (r = 0.75, p-value: 5.7 × 10−10). The correlation was not significant in the oldest class where sparse data were available, but the relation was similar (Figure 3).
Figure 3

Geographical correlation of T1D incidence between individuals aged 0–14 years and adults. Studies using autoantibodies/C-Peptide for T1D case definition are identified by Red diamonds. The corresponding countries are shown as: BE1: Belgium (2007) [30]; BE2: Belgium (2002) [31]; BE3: Belgium (1997) [32]; DK: Denmark [34]; ES1: Spain, Catalonia [54]; ES2: Spain, Navarra (2014) [56]; ES3: Spain, Navarra (2013) [57]; FI: Finland [35]; IR: Iran (Islamic Republic of) [15]; IT: Italy [45,46]; SE: Sweden [63], TW: Taiwan [81]; US: United States of America [74]. Sp. Cor: Spearman correlation.

Comparison of male and female T1D adult incidences

T1D incidence was larger in males aged 15 to 39 years than in females in 44 (81%) of the 54 studies reporting incidence by sex (Additional file 5: Table S2). The mean male-to-female ratio in our review was 1.47 (95% CI for mean 1.33-1.60, SD = 0.49, n = 54, p = < 0.0001).

Discussion

A first result of this systematic review is the paucity of data available on adult incidence of T1D as compared to those concerning children. The 71 studies retrieved provided information on adult T1D in only 35 countries, 40% of the 88 countries with primary childhood T1D incidence information in the 6th IDF atlas [1].

A second result is that only a small proportion (n = 14) of the 71 studies used detection of specific autoantibodies and/or dosage of C-peptide [83] as diagnostic criteria of adult T1D.

A third result was that in a majority of the retrieved studies, adult T1D incidence was greater in men than in women, which contrasts with incidence of T1D in children where sex ratio is around one [2,84]. Using comparative data, Karvonen et al. also described a male excess among young adults in the 15–39 years of age [85]. Sex differences in exposure to possible environmental triggers of T1D, in hormonal/genetic susceptibility, in lifestyle have been proposed as possible explanations for this difference [62].

A last striking observation of the current analysis is the strong geographical correlation of the incidences in adults and children. This correlation may be explained by the fact that adults with T1D share the gene alleles known to be associated to incidence of T1D in children, [86,87], and/or some predisposing environmental causes [4]. For example, in a previous study on incidence of T1D in children, a significant positive correlation was detected between the percentage of urban population and the incidence of T1D in children (r = 0.41 p-value: < 0.0001) [4]; in this review a significantly higher urban proportion of T1D incidence among adults was found in 4 of the 7 studies reporting differences between rural vs urban areas [15,21,42,75].

There was an overall decrease of incidence with age in adults and young adults after the age of 14. A second peak of T1D around the age of 50, as described by Krolewski et al. [88], was only reported in 7% (4 of 58) of the studies [18,63,80,89].

The paucity of data made it impossible to document an increase in adult T1D incidence that would parallel the dramatic increase observed in children [2,3,90]. Indeed, successive studies in the same region over different periods reporting incidence in people aged >30 years of age were only found for Belgium [30-32], Lithuania [20-22] and Sweden [58-62]. Similarly, this review did not dispose of sufficient data to document differences in the clinical presentation of T1D of adults and children as suggested elsewhere [32,40]; indeed only two of the 71 studies describe differences in clinical presentation of T1D between adults and children [89,91].

Improving the quantity and quality of information on adult T1D is not only useful to better understand the epidemiology and natural history of T1D, but can have practical consequences, as delay of T1D diagnosis may mean retardation in insulin treatment, lost opportunities for potential prevention of acute and chronic complications, and even death [92]: in Croatia [18], 14% of the incident cases were identified solely through death certificates, and high mortality was found in the newly-diagnosed T1D aged over 50.

Conclusions

Overall, the results of this systematic review should encourage the launching of epidemiological studies of adult T1D with specific diagnostic criteria.

Availability of supporting data

All the supporting data are included as additional files.

Declarations

Acknowledgements

We thank Anne-Lise Haenni of the Institut Jacques Monod, CNRS - Paris-Diderot University, for critically reading and reviewing the English of this manuscript.

Funding

This study was supported by grants from the Programme Hospitalier de Recherche Clinique, and from Colciencias, the Administrative Department of Science, Technology and Innovation for Colombia. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Authors’ Affiliations

(1)
Institut National de la Santé et de la Recherche Médicale, Inserm U-1169
(2)
Pierre et Marie Curie University
(3)
Paris-Sud University

References

  1. Patterson C, Guariguata L, Dahlquist G, Soltesz G, Ogle G, Silink M. Diabetes in the young - a global view and worldwide estimates of numbers of children with type 1 diabetes. Diabetes Res Clin Pract. 2013;103(2):161–75.View ArticlePubMedGoogle Scholar
  2. The DIAMOND Project Group. Incidence and trends of childhood Type 1 diabetes worldwide 1990–1999. The DIAMOND project Group. Diabet Med. 2006;23(8):857–66.View ArticleGoogle Scholar
  3. Patterson CC, Gyurus E, Rosenbauer J, Cinek O, Neu A, Schober E, et al. Trends in childhood type 1 diabetes incidence in Europe during 1989–2008: evidence of non-uniformity over time in rates of increase. Diabetologia. 2012;55(8):2142–7.View ArticlePubMedGoogle Scholar
  4. Diaz-Valencia PA, Bougneres P, Valleron AJ. Covariation of the incidence of type 1 diabetes with country characteristics available in public databases. PloS one. 2015;10(2):e0118298.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Borg H, Arnqvist HJ, Bjork E, Bolinder J, Eriksson JW, Nystrom L, et al. Evaluation of the new ADA and WHO criteria for classification of diabetes mellitus in young adult people (15–34 yrs) in the Diabetes Incidence Study in Sweden (DISS). Diabetologia. 2003;46(2):173–81.View ArticlePubMedGoogle Scholar
  6. Tuomi T, Groop LC, Zimmet PZ, Rowley MJ, Knowles W, Mackay IR. Antibodies to glutamic acid decarboxylase reveal latent autoimmune diabetes mellitus in adults with a non-insulin-dependent onset of disease. Diabetes. 1993;42(2):359–62.View ArticlePubMedGoogle Scholar
  7. Zimmet PZ. Diabetes epidemiology as a tool to trigger diabetes research and care. Diabetologia. 1999;42(5):499–518.View ArticlePubMedGoogle Scholar
  8. LaPorte RE, Tajima N, Akerblom HK, Berlin N, Brosseau J, Christy M, et al. Geographic differences in the risk of insulin-dependent diabetes mellitus: the importance of registries. Diabetes Care. 1985;8 Suppl 1:101–7.View ArticlePubMedGoogle Scholar
  9. Health Statistics and health information systems. [http://www.who.int/healthinfo/global_burden_disease/definition_regions/en/]
  10. LaPorte RE, McCarty D, Bruno G, Tajima N, Baba S. Counting diabetes in the next millennium. Application of capture-recapture technology. Diabetes Care. 1993;16(2):528–34.View ArticlePubMedGoogle Scholar
  11. GraphClick. In., 3.0 edn: Arizona Software; 2008. Available in the website: http://www.arizona-software.ch/graphclick/ [last accesed: 12 January, 2012].
  12. R Development Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing. In., R version 3.0.1 (2013-05-16). http://www.R-project.org/. Vienna, Austria, 2013.
  13. Tuomilehto J, Dabee J, Karvonen M, Dowse GK, Gareeboo H, Virtala E, et al. Incidence of IDDM in Mauritian children and adolescents from 1986 to 1990. Diabetes Care. 1993;16(12):1588–91.View ArticlePubMedGoogle Scholar
  14. Swai AB, Lutale JL, McLarty DG. Prospective study of incidence of juvenile diabetes mellitus over 10 years in Dar es Salaam, Tanzania. BMJ. 1993;306(6892):1570–2.View ArticlePubMedPubMed CentralGoogle Scholar
  15. Pishdad GR. Low incidence of type 1 diabetes in Iran. Diabetes Care. 2005;28(4):927–8.View ArticlePubMedGoogle Scholar
  16. Kadiki OA, Reddy MR, Marzouk AA. Incidence of insulin-dependent diabetes (IDDM) and non-insulin-dependent diabetes (NIDDM) (0-34 years at onset) in Benghazi, Libya. Diabetes Res Clin Pract. 1996;32(3):165–73.View ArticlePubMedGoogle Scholar
  17. Ben Khalifa F, Mekaouar A, Taktak S, Hamhoum M, Jebara H, Kodia A, et al. A five-year study of the incidence of insulin-dependent diabetes mellitus in young Tunisians (preliminary results). Diabetes Metab. 1997;23(5):395–401.PubMedGoogle Scholar
  18. Roglic G, Pavlic-Renar I, Sestan-Crnek S, Prasek M, Kadrnka-Lovrencic M, Radica A, et al. Incidence of IDDM during 1988-1992 in Zagreb, Croatia. Diabetologia. 1995;38(5):550–4.View ArticlePubMedGoogle Scholar
  19. Kalits I, Podar T. Incidence and prevalence of type 1 (insulin-dependent) diabetes in Estonia in 1988. Diabetologia. 1990;33(6):346–9.View ArticlePubMedGoogle Scholar
  20. Ostrauskas R, Zalinkevicius R, Jurgeviciene N, Radzeviciene L, Lasaite L. The incidence of type 1 diabetes mellitus among 15-34 years aged Lithuanian population: 18-year incidence study based on prospective databases. BMC Public Health. 2011;11:813.View ArticlePubMedPubMed CentralGoogle Scholar
  21. Pundziute-Lycka A, Urbonaite B, Ostrauskas R, Zalinkevicius R, Dahlquist GG. Incidence of type 1 diabetes in Lithuanians aged 0-39 years varies by the urban-rural setting, and the time change differs for men and women during 1991-2000. Diabetes Care. 2003;26(3):671–6.View ArticlePubMedGoogle Scholar
  22. Ostrauskas R, Zalinkevicius R. Incidence in young adulthood-onset Type 1 diabetes mellitus in Lithuania during 1991-1997. Lithuanian Epidemiology Diabetes Study Group. Diabetes Nutr Metab. 2000;13(2):68–74.PubMedGoogle Scholar
  23. Kretowski A, Kowalska I, Peczynska J, Urban M, Green A, Kinalska I. The large increase in incidence of Type I diabetes mellitus in Poland. Diabetologia. 2001;44 Suppl 3:B48–50.View ArticlePubMedGoogle Scholar
  24. Sobel-Maruniak A, Grzywa M, Orlowska-Florek R, Staniszewski A. The rising incidence of type 1 diabetes in south-eastern Poland. A study of the 0-29 year-old age group, 1980–1999. Endokrynol Pol. 2006;57(2):127–30.PubMedGoogle Scholar
  25. Grzywa MA, Sobel AK. Incidence of IDDM in the province of Rzeszow, Poland, 0- to 29-year-old age-group, 1980-1992. Diabetes Care. 1995;18(4):542–4.View ArticlePubMedGoogle Scholar
  26. Wysocki MJ, Chanska M, Bak M, Czyzyk AS. Incidence of insulin-dependent diabetes mellitus in Warsaw, Poland, in children and young adults, 1983-1988. World Health Stat Q. 1992;45(4):315–20.PubMedGoogle Scholar
  27. Ionescu-Tirgoviste C, Paterache E, Cheta D, Farcasiu E, Serafinceanu C, Mincu I. Epidemiology of diabetes in Bucharest. Diabet Med. 1994;11(4):413–7.View ArticlePubMedGoogle Scholar
  28. Kyvik KO, Nystrom L, Gorus F, Songini M, Oestman J, Castell C, et al. The epidemiology of Type 1 diabetes mellitus is not the same in young adults as in children. Diabetologia. 2004;47(3):377–84.View ArticlePubMedGoogle Scholar
  29. Rami B, Waldhor T, Schober E. Incidence of Type I diabetes mellitus in children and young adults in the province of Upper Austria, 1994-1996. Diabetologia. 2001;44 Suppl 3:B45–7.View ArticlePubMedGoogle Scholar
  30. Weets I, Rooman R, Coeckelberghs M, De Block C, Van Gaal L, Kaufman JM, et al. The age at diagnosis of type 1 diabetes continues to decrease in Belgian boys but not in girls: a 15-year survey. Diabetes Metab Res Rev. 2007;23(8):637–43.View ArticlePubMedGoogle Scholar
  31. Weets I, De Leeuw IH, Du Caju MV, Rooman R, Keymeulen B, Mathieu C, et al. The incidence of type 1 diabetes in the age group 0-39 years has not increased in Antwerp (Belgium) between 1989 and 2000: evidence for earlier disease manifestation. Diabetes Care. 2002;25(5):840–6.View ArticlePubMedGoogle Scholar
  32. Vandewalle CL, Coeckelberghs MI, De Leeuw IH, Du Caju MV, Schuit FC, Pipeleers DG, et al. Epidemiology, clinical aspects, and biology of IDDM patients under age 40 years. Comparison of data from Antwerp with complete ascertainment with data from Belgium with 40% ascertainment. The Belgian Diabetes Registry. Diabetes Care. 1997;20(10):1556–61.View ArticlePubMedGoogle Scholar
  33. Radosevic B, Bukara-Radujkovic G, Miljkovic V, Pejicic S, Bratina N, Battelino T. The incidence of type 1 diabetes in Republic of Srpska (Bosnia and Herzegovina) and Slovenia in the period 1998-2010. Pediatr Diabetes. 2013;14(4):273–9.View ArticlePubMedGoogle Scholar
  34. Molbak AG, Christau B, Marner B, Borch-Johnsen K, Nerup J. Incidence of insulin-dependent diabetes mellitus in age groups over 30 years in Denmark. Diabet Med. 1994;11(7):650–5.View ArticlePubMedGoogle Scholar
  35. Lammi N, Taskinen O, Moltchanova E, Notkola IL, Eriksson JG, Tuomilehto J, et al. A high incidence of type 1 diabetes and an alarming increase in the incidence of type 2 diabetes among young adults in Finland between 1992 and 1996. Diabetologia. 2007;50(7):1393–400.View ArticlePubMedGoogle Scholar
  36. Charkaluk ML, Czernichow P, Levy-Marchal C. Incidence data of childhood-onset type I diabetes in France during 1988-1997: the case for a shift toward younger age at onset. Pediatr Res. 2002;52(6):859–62.PubMedGoogle Scholar
  37. Levy-Marchal C. Evolution of the incidence of IDDM in childhood in France. Rev Epidemiol Sante Publique. 1998;46(3):157–63.PubMedGoogle Scholar
  38. Blumenfeld O, Dichtiar R, Shohat T, Israel IRSG. Trends in the incidence of type 1 diabetes among Jews and Arabs in Israel. Pediatr Diabetes. 2014;15(6):422–7.View ArticlePubMedGoogle Scholar
  39. Sella T, Shoshan A, Goren I, Shalev V, Blumenfeld O, Laron Z, et al. A retrospective study of the incidence of diagnosed Type 1 diabetes among children and adolescents in a large health organization in Israel, 2000-2008. Diabet Med. 2011;28(1):48–53.View ArticlePubMedGoogle Scholar
  40. Koton S. Incidence of type 1 diabetes mellitus in the 0- to 17-yr-old Israel population, 1997-2003. Pediatr Diabetes. 2007;8(2):60–6.View ArticlePubMedGoogle Scholar
  41. Garancini P, Gallus G, Calori G, Formigaro F, Micossi P. Incidence and prevalence rates of diabetes mellitus in Italy from routine data: a methodological assessment. Eur J Epidemiol. 1991;7(1):55–63.View ArticlePubMedGoogle Scholar
  42. Tenconi MT, Devoti G, Albani I, Lorini R, Martinetti M, Fratino P, et al. IDDM in the province of Pavia, Italy, from a population-based registry. A descriptive study. Diabetes Care. 1995;18(7):1017–9.View ArticlePubMedGoogle Scholar
  43. Muntoni S, Songini M. High incidence rate of IDDM in Sardinia. Sardinian Collaborative Group for Epidemiology of IDDM. Diabetes Care. 1992;15(10):1317–22.View ArticlePubMedGoogle Scholar
  44. Frongia O, Mastinu F, Sechi GM. Prevalence and 4-year incidence of insulin-dependent diabetes mellitus in the province of Oristano (Sardinia, Italy). Acta Diabetol. 1997;34(3):199–205.View ArticlePubMedGoogle Scholar
  45. Bruno G, Novelli G, Panero F, Perotto M, Monasterolo F, Bona G, et al. The incidence of type 1 diabetes is increasing in both children and young adults in Northern Italy: 1984–2004 temporal trends. Diabetologia. 2009;52(12):2531–5.View ArticlePubMedGoogle Scholar
  46. Bruno G, Runzo C, Cavallo-Perin P, Merletti F, Rivetti M, Pinach S, et al. Incidence of type 1 and type 2 diabetes in adults aged 30-49 years: the population-based registry in the province of Turin, Italy. Diabetes Care. 2005;28(11):2613–9.View ArticlePubMedGoogle Scholar
  47. Bruno G, Merletti F, Vuolo A, Pisu E, Giorio M, Pagano G. Sex differences in incidence of IDDM in age-group 15-29 yr. Higher risk in males in Province of Turin, Italy. Diabetes Care. 1993;16(1):133–6.View ArticlePubMedGoogle Scholar
  48. de Beaufort CE, Michel G, Glaesener G. The incidence of type 1 (insulin-dependent) diabetes mellitus in subjects aged 0-19 years in Luxembourg: a retrospective study from 1977 to 1986. Diabetologia. 1988;31(10):758–61.View ArticlePubMedGoogle Scholar
  49. Schranz AG, Prikatsky V. Type 1 diabetes in the Maltese Islands. Diabet Med. 1989;6(3):228–31.View ArticlePubMedGoogle Scholar
  50. Ruwaard D, Hirasing RA, Reeser HM, van Buuren S, Bakker K, Heine RJ, et al. Increasing incidence of type I diabetes in The Netherlands. The second nationwide study among children under 20 years of age. Diabetes Care. 1994;17(6):599–601.View ArticlePubMedGoogle Scholar
  51. Joner G, Sovik O. The incidence of type 1 (insulin-dependent) diabetes mellitus 15-29 years in Norway 1978-1982. Diabetologia. 1991;34(4):271–4.View ArticlePubMedGoogle Scholar
  52. Morales-Perez FM, Barquero-Romero J, Perez-Miranda M. Incidence of type I diabetes among children and young adults (0-29 years) in the province of Badajoz, Spain during 1992 to 1996. Acta Paediatr. 2000;89(1):101–4.View ArticlePubMedGoogle Scholar
  53. Carrillo Dominguez A. Incidence of type 1 diabetes mellitus in the Canary Islands (1995-1996). Epidemiologic Group of the Canary Society of Endocrinology and Nutrition. Rev Clin Esp. 2000;200(5):257–60.View ArticlePubMedGoogle Scholar
  54. Abellana R, Ascaso C, Carrasco JL, Castell C, Tresserras R. Geographical variability of the incidence of Type 1 diabetes in subjects younger than 30 years in Catalonia, Spain. Med Clin (Barc). 2009;132(12):454–8.View ArticleGoogle Scholar
  55. Goday A, Castell C, Tresserras R, Canela J, Taberner JL, Lloveras G. Incidence of type 1 (insulin-dependent) diabetes mellitus in Catalonia, Spain. The Catalan Epidemiology Diabetes Study Group. Diabetologia. 1992;35(3):267–71.View ArticlePubMedGoogle Scholar
  56. Forga L, Goni MJ, Ibanez B, Cambra K, Mozas D, Chueca M. Incidence of type 1 diabetes in Navarre, 2009-2012. An Sist Sanit Navar. 2014;37(2):241–7.View ArticlePubMedGoogle Scholar
  57. Forga L, Goni MJ, Cambra K, Ibanez B, Mozas D, Chueca M. En Representacion del Grupo de Estudio de Diabetes tipo 1 de N: [Differences by age and gender in the incidence of type 1 diabetes in Navarre, Spain (2009-2011)]. Gac Sanit/SESPAS. 2013;27(6):537–40.View ArticleGoogle Scholar
  58. Dahlquist GG, Nystrom L, Patterson CC. Incidence of type 1 diabetes in Sweden among individuals aged 0-34 years, 1983-2007: an analysis of time trends. Diabetes Care. 2011;34(8):1754–9.View ArticlePubMedPubMed CentralGoogle Scholar
  59. Ostman J, Lonnberg G, Arnqvist HJ, Blohme G, Bolinder J, Ekbom Schnell A, et al. Gender differences and temporal variation in the incidence of type 1 diabetes: results of 8012 cases in the nationwide Diabetes Incidence Study in Sweden 1983-2002. J Intern Med. 2008;263(4):386–94.View ArticlePubMedGoogle Scholar
  60. Pundziute-Lycka A, Dahlquist G, Nystrom L, Arnqvist H, Bjork E, Blohme G, et al. The incidence of Type I diabetes has not increased but shifted to a younger age at diagnosis in the 0-34 years group in Sweden 1983-1998. Diabetologia. 2002;45(6):783–91.View ArticlePubMedGoogle Scholar
  61. Nystrom L, Dahlquist G, Ostman J, Wall S, Arnqvist H, Blohme G, et al. Risk of developing insulin-dependent diabetes mellitus (IDDM) before 35 years of age: indications of climatological determinants for age at onset. Int J Epidemiol. 1992;21(2):352–8.View ArticlePubMedGoogle Scholar
  62. Blohme G, Nystrom L, Arnqvist HJ, Lithner F, Littorin B, Olsson PO, et al. Male predominance of type 1 (insulin-dependent) diabetes mellitus in young adults: results from a 5-year prospective nationwide study of the 15-34-year age group in Sweden. Diabetologia. 1992;35(1):56–62.View ArticlePubMedGoogle Scholar
  63. Thunander M, Petersson C, Jonzon K, Fornander J, Ossiansson B, Torn C, et al. Incidence of type 1 and type 2 diabetes in adults and children in Kronoberg, Sweden. Diabetes Res Clin Pract. 2008;82(2):247–55.View ArticlePubMedGoogle Scholar
  64. Imkampe AK, Gulliford MC. Trends in Type 1 diabetes incidence in the UK in 0- to 14-year-olds and in 15- to 34-year-olds, 1991-2008. Diabet Med. 2011;28(7):811–4.View ArticlePubMedGoogle Scholar
  65. Bingley PJ, Gale EA. Incidence of insulin dependent diabetes in England: a study in the Oxford region, 1985-6. BMJ. 1989;298(6673):558–60.View ArticlePubMedPubMed CentralGoogle Scholar
  66. Jordan OW, Lipton RB, Stupnicka E, Cruickshank JK, Fraser HS. Incidence of type I diabetes in people under 30 years of age in Barbados, West Indies, 1982-1991. Diabetes Care. 1994;17(5):428–31.View ArticlePubMedGoogle Scholar
  67. Legault L, Polychronakos C. Annual incidence of type 1 diabetes in Quebec between 1989-2000 in children. Clin Invest Med. 2006;29(1):10–3.PubMedGoogle Scholar
  68. Wagenknecht LE, Roseman JM, Herman WH. Increased incidence of insulin-dependent diabetes mellitus following an epidemic of Coxsackievirus B5. Am J Epidemiol. 1991;133(10):1024–31.PubMedGoogle Scholar
  69. Wagenknecht LE, Roseman JM, Alexander WJ. Epidemiology of IDDM in black and white children in Jefferson County, Alabama, 1979-1985. Diabetes. 1989;38(5):629–33.View ArticlePubMedGoogle Scholar
  70. Vehik K, Hamman RF, Lezotte D, Norris JM, Klingensmith G, Bloch C, et al. Increasing Incidence of Type 1 Diabetes in 0- to 17-Year-Old Colorado Youth. Diabetes Care. 2007;30(3):503–9.View ArticlePubMedGoogle Scholar
  71. Kostraba JN, Gay EC, Cai Y, Cruickshanks KJ, Rewers MJ, Klingensmith GJ, et al. Incidence of insulin-dependent diabetes mellitus in Colorado. Epidemiology. 1992;3(3):232–8.View ArticlePubMedGoogle Scholar
  72. Libman IM, LaPorte RE, Becker D, Dorman JS, Drash AL, Kuller L. Was there an epidemic of diabetes in nonwhite adolescents in Allegheny County, Pennsylvania? Diabetes Care. 1998;21(8):1278–81.View ArticlePubMedGoogle Scholar
  73. Fishbein HA, Faich GA, Ellis SE. Incidence and hospitalization patterns of insulin-dependent diabetes mellitus. Diabetes Care. 1982;5(6):630–3.View ArticlePubMedGoogle Scholar
  74. Bell RA, Mayer-Davis EJ, Beyer JW, D'Agostino Jr RB, Lawrence JM, Linder B, et al. Diabetes in non-Hispanic white youth: prevalence, incidence, and clinical characteristics: the SEARCH for Diabetes in Youth Study. Diabetes Care. 2009;32 Suppl 2:S102–11.View ArticlePubMedPubMed CentralGoogle Scholar
  75. Allen C, Palta M, D'Alessio DJ. Incidence and differences in urban-rural seasonal variation of type 1 (insulin-dependent) diabetes in Wisconsin. Diabetologia. 1986;29(9):629–33.View ArticlePubMedGoogle Scholar
  76. Gorham ED, Garland FC, Barrett-Connor E, Garland CF, Wingard DL, Pugh WM. Incidence of insulin-dependent diabetes mellitus in young adults: experience of 1,587,630 US Navy enlisted personnel. Am J Epidemiol. 1993;138(11):984–7.PubMedGoogle Scholar
  77. Tran F, Stone M, Huang CY, Lloyd M, Woodhead HJ, Elliott KD, et al. Population-based incidence of diabetes in Australian youth aged 10-18 yr: increase in type 1 diabetes but not type 2 diabetes. Pediatr Diabetes. 2014;15(8):585–90.View ArticlePubMedGoogle Scholar
  78. Sutton DL, Lyle DM, Pierce JP. Incidence and prevalence of insulin-dependent diabetes mellitus in the zero- to 19-years' age-group in Sydney. Med J Aust. 1989;151(3):140–1. 144-146.PubMedGoogle Scholar
  79. Sasaki A, Okamoto N. Epidemiology of childhood diabetes in Osaka District, Japan, using the documents from the medical benefits system specific for childhood diabetes. Diabetes Res Clin Pract. 1992;18(3):191–6.View ArticlePubMedGoogle Scholar
  80. Scott RS, Brown LJ. Prevalence and incidence of insulin-treated diabetes mellitus in adults in Canterbury, New Zealand. Diabet Med. 1991;8(5):443–7.View ArticlePubMedGoogle Scholar
  81. Lin WH, Wang MC, Wang WM, Yang DC, Lam CF, Roan JN, et al. Incidence of and mortality from Type I diabetes in Taiwan from 1999 through 2010: a nationwide cohort study. PloS one. 2014;9(1):e86172.View ArticlePubMedPubMed CentralGoogle Scholar
  82. Washington RE, Orchard TJ, Arena VC, Laporte RE, Tull ES. Incidence of type 1 and type 2 diabetes in youth in the U.S. Virgin Islands, 2001-2010. Pediatr Diabetes. 2013;14(4):280–7.View ArticlePubMedGoogle Scholar
  83. Bingley PJ, Bonifacio E, Ziegler AG, Schatz DA, Atkinson MA, Eisenbarth GS. Proposed guidelines on screening for risk of type 1 diabetes. Diabetes Care. 2001;24(2):398.View ArticlePubMedGoogle Scholar
  84. Soltesz G, Patterson CC, Dahlquist G. Worldwide childhood type 1 diabetes incidence–what can we learn from epidemiology? Pediatr Diabetes. 2007;8 Suppl 6:6–14.View ArticlePubMedGoogle Scholar
  85. Karvonen M, Pitkaniemi M, Pitkaniemi J, Kohtamaki K, Tajima N, Tuomilehto J. Sex difference in the incidence of insulin-dependent diabetes mellitus: an analysis of the recent epidemiological data. World Health Organization DIAMOND Project Group. Diabetes Metab Rev. 1997;13(4):275–91.View ArticlePubMedGoogle Scholar
  86. Todd JA. Etiology of type 1 diabetes. Immunity. 2010;32(4):457–67.View ArticlePubMedGoogle Scholar
  87. Caillat-Zucman S, Garchon HJ, Timsit J, Assan R, Boitard C, Djilali-Saiah I, et al. Age-dependent HLA genetic heterogeneity of type 1 insulin-dependent diabetes mellitus. J Clin Invest. 1992;90(6):2242–50.View ArticlePubMedPubMed CentralGoogle Scholar
  88. Krolewski AS, Warram JH, Rand LI, Kahn CR. Epidemiologic approach to the etiology of type I diabetes mellitus and its complications. N Engl J Med. 1987;317(22):1390–8.View ArticlePubMedGoogle Scholar
  89. Karjalainen J, Salmela P, Ilonen J, Surcel HM, Knip M. A comparison of childhood and adult type I diabetes mellitus. N Engl J Med. 1989;320(14):881–6.View ArticlePubMedGoogle Scholar
  90. Patterson CC, Dahlquist GG, Gyurus E, Green A, Soltesz G. Incidence trends for childhood type 1 diabetes in Europe during 1989-2003 and predicted new cases 2005-20: a multicentre prospective registration study. Lancet. 2009;373(9680):2027–33.View ArticlePubMedGoogle Scholar
  91. Sabbah E, Savola K, Ebeling T, Kulmala P, Vahasalo P, Ilonen J, et al. Genetic, autoimmune, and clinical characteristics of childhood- and adult-onset type 1 diabetes. Diabetes Care. 2000;23(9):1326–32.View ArticlePubMedGoogle Scholar
  92. Atkinson MA, Eisenbarth GS. Type 1 diabetes: new perspectives on disease pathogenesis and treatment. Lancet. 2001;358(9277):221–9.View ArticlePubMedGoogle Scholar

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