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. 2017 Oct 9;7:12810. doi: 10.1038/s41598-017-12954-8

Climates on incidence of childhood type 1 diabetes mellitus in 72 countries

Yin-ling Chen 1,3, Yong-cheng Huang 1, Yong-chao Qiao 2, Wei Ling 1, Yan-hong Pan 1,3, Li-jun Geng 1,3, Jian-long Xiao 1,3, Xiao-xi Zhang 1,3,✉, Hai-lu Zhao 1,2,3,✉
PMCID: PMC5634499  PMID: 28993655

Abstract

We are aimed to systematically assess the worldwide trend in incidence of childhood type 1 diabetes mellitus (CT1DM) from 1965 to 2012 and to discuss whether climate affect incidence of CT1DM. We searched the relevant literatures in detail to judge the effect of different climates on incidence of CT1DM. The climates included Mediterranean, monsoon, oceanic, continental, savanna, and rainforest. According to different climates, we further researched relevant factor such as sunshine durations and latitudes. The overall incidence of CT1DM in 72 countries was 11.43 (95% CI 10.31–12.55) per 100,000 children/yr. The incidence of CT1DM in Oceanic climate [10.56 (8.69–12.42)] is highest compared with other climates; the incidence in 40°–66°34′N/S [14.71 (12.30–17.29)] is higher than other latitude groups; the incidence in sunshine durations with 3–4 hours per day [15.17 (11.14–19.20)] is highest compared with other two groups; the incidence of CT1DM from 2000 to 2012 [19.58 (14.55–24.60)] is higher than other periods; all p < 0.01. Incidence of CT1DM was increasing from 1965 to 2012, but incidence in Oceanic climate is higher than other climates. Furthermore, it is higher in centers with higher latitude and lower sunshine durations. The climates might play a key role in inducing CT1DM.

Introduction

The worldwide variation in the incidence of type 1 diabetes mellitus (TIDM) among children has been confirmed to be increased over the past 50 years1–3, especially among children of 10–14 years of age4. Childhood type 1 diabetes mellitus (CTIDM) is a syndrome caused by β-cell destruction that results in progressive or acute insulin deficiency5,6.

While we know that children with diabetes aged less than 7 years are at high risk of cognitive dysfunction, and poor glycaemic control might induce hypoglycaemia that could influence the developing nervous system7,8. Furthermore, immunosuppressive drugs for CT1DM treatment have kidney toxicity and other side effects9.

No clear evidence of a correlation between the CT1DM and climates had emerged from human or animal studies. Previous studies indicated the milk consumption10,11, dietary habit12,13, socioeconomic14, latitude15, familial predisposition16, drinking water17 or radiation18 might be important factor for CT1DM.

It is vital therefore to conduct this study to confirm the various climates in relation to the incidence of CT1DM.

Methods

Data collection

This study is supported by the Guilin Medical University Ethnic Committee Board. Articles published between Jan 1, 1965 and Jan 31, 2017 that were systematically searched in the databases: the PubMed, the Chinese National Knowledge Infrastructure (CNKI), Library of Congress, and Web of Science. All potentially relevant articles in reference lists of included articles were screened as full-text. For missing information or ambiguous, the corresponding author of this study was contacted with authors of relevant articles by email. For duplicated duplications, we only included the latest articles in our analysis. More than 3,600 publications reporting the incidence of CT1DM were identified.

Eligibility Criteria

Relevant studies for incidence of CT1DM in various countries were included in final analysis if the following strict criteria were met: (1) patients younger than 19 years old diagnosed with T1DM; (2) the number of cases was three or more; (3) the study period was more than a year; (4) T1DM was diagnosed according to World Health Organization definition. Studies met the following criteria were excluded: duplication (the same articles in different database); case reports, and comments; the studies not meeting criteria of inclusion. Eligibility assessment was independently conducted by 2 authors, with all inconsistent questions solved by discussion with other authors.

Description of the data

Incidence data were extracted either from the text or from the tables in the publications. There was no incidence rate of the original articles were presented in the figures. Altogether 87 studies from 72 countries met the inclusion criteria and were finally included in this study (Table 1). In 78 studies the children aged from 0 to 14 years and in 9 studies from 0 to 12, 15, 17, 19 years. The time period of the researches ranged from 1 to 30 years. The degree of case-ascertainment ranged from 85 to 100%. The researches included in this study were from the period 1965 to 2012.

Table 1.

The characteristics of worldwide incidence (per 100,000 children/yr) of childhood type 1 diabetes mellitus.

Regions and Centers Study periods Age-group (years old) Main climate type Boy* Girl* Total References
case (n) Incidence case (n) Incidence case (n) Incidence
Africa
Algeria
Oran 1980–1989 0–14 ① 505 8.1 44
1990 0–14 9 4.4 14 7 23 5.7 (3.62–5.82) 4
1979–1988 0–14 4.7 45
1990–1999 0–14 7.7 9.6 8.6 (7.6–9.8) 46
Libya
Benghazi 1981–1990 0–19 ② 121 8.3 (6.9–10.0) 130 9.2 (7.7–11.0) 251 8.8 (7.8–10.0) 47
1991–1999 0–14 7.8 10.3 9 (8.0–10.2) 46
Mauritius 1986–1990 0–14 ③ 1.8 2.4 2.1 48
1990–1994 0–14 10 1.3 11 1.5 21 1.4 (0.83–2.07) 4
Sudan 1991–1995 0–14 ② 534 10.1 (9.0–12.8) 49
Khartoum ② 196 31.8 (28.4–35.2) 50
Gezira 1990 0–14 ② 17 5.6 12 4.4 29 5(3.74–6.54) 4
 Sultanate of Oman 1993 0–14 ② 3.23 1.99 2.45 51
1994 0–14 2.91 1.95 2.62 51
Tunisia
Beja 1990–1994 0–14 ② 22 9 16 6.5 38 7.8 (5.47–10.68) 4
1990–1999 0–14 8.4 6.9 7.7 (6.1–9.6) 46
Gafsa 1990–1994 0–14 ② 31 10 22 7.5 53 8.8 (6.59–11.51) 4
1990–1999 0–14 9.5 7.5 8.5 (6.9–10.3) 46
Kairoan 1991–1993 0–14 ② 7.3 7.8 7.6 (5.6–10.0) 46
Monastir 1990–1994 0–14 ② 15 4.7 16 5.2 31 4.9 (3.35–6.96) 4
1990–1999 0–14 6.6 5.1 5.8 (4.6–7.3) 46
Tanzania
Dar es Salaam 1982–1991 0–14 ④ 0.8 0.9 86 0.8 52
Asia
China
Beijing 1990–1994 0–14 ⑤ 38 0.7 52 1.1 90 0.9 (0.72–1.09) 4
1995–2000 0–14 0.93 (0.65–1.22) 1.60 (1.42–1.78) 1.25 (1.07–1.43) 53
2001–2005 0–14 1.37 (1.26–1.48) 2.07 (1.62–2.51) 1.70 (1.48–1.91) 53
2006–2010 0–14 2.05 (1.45–2.63) 2.48 (1.81–3.15 2.25 (1.64–2.85) 53
Chang Chun 1990–1994 0–14 ⑤ 7 0.6 11 1.1 18 0.8 (0.49–1.30) 46
Changsha 1990–1994 0–14 ⑤ 10 0.6 7 0.2 17 0.2 (0.2–0.4) 46
Dalian 1990–1994 0–14 ⑤ 10 1.1 11 1.2 21 1.1 (0.7–1.7) 46
Guilin 1991–1994 0–14 ⑤ 2 0.6 3 1 5 0.8 (0.2–2.0) 46
Hainan 1990–1994 0–14 ⑤ 6 0.1 11 0.2 17 0.2 (0.1–0.2) 46
Harbin 1990–1996 0–14 ⑤ 18 0.6 17 0.6 35 0.6 (0.4–0.8) 46
Hong-Kong 1986–1990 0–14 ⑤ 1.5 2.4 22 2 54
1990–1994 0–14 4 0.6 13 2.1 17 1.3 (0.77–2.17) 4
1990–1995 0–14 0.6 1.9 1.3 (0.8–1.9) 46
1997 0–14 218 1.4 55
Huhehot 1990–1994 0–14 ⑥ 10 1.1 6 0.7 16 0.9 (0.5–1.5) 46
Jilin 1990–1994 0–14 ⑥ 8 0.4 14 0.8 22 0.6 (0.4–0.9) 46
Jinan 1990–1995 0–14 ⑤ 12 0.5 11 0.4 23 0.4 (0.3–0.6) 46
Lanzhou 1991–1994 0–14 ⑥ 5 0.4 3 0.2 8 0.3 (0.1–0.5) 46
Nanjing 1990–1994 0–14 ⑤ 7 0.3 13 0.7 20 0.5 (0.3–0.8) 46
Nanning 1990–1994 0–14 ⑤ 4 0.7 10 0.7 14 0.7 (0.5–0.9) 46
Shanghai 1980–1991 0–14 ⑤ 35 0.55 (0.38–0.76) 40 0.67 (0.45–0.91) 75 0.61 (0.48–0.77) 56
1989–1993 0–14 28 0.78 (0.52–1.12) 30 0.88 (0.59–1.25) 58 0.83 (0.61–1.04) 57
1990–1994 0–14 24 0.4 23 0.5 47 0.5 (0.3–0.7) 46
1997–2011 0–14 306 3.1 (2.8–3.4) 316 3.2 (2.8–3.5) 622 3.1 (2.9–3.3) 39
Sichuan 1990–1994 0–14 ⑤ 9 1.8 13 2.7 22 2.3 (1.4–3.3) 46
Tie Ling 1990–1994 0–14 ⑤ 5 0.2 3 0.1 8 0.2 (0.1–0.3) 46
Wuhan 1990–1994 0–14 ⑤ 13 5.2 9 3.8 22 4.5 (2.8–7.0) 46
Wulumuqi 1990–1994 0–14 ⑥ 5 0.9 4 0.8 9 0.8 (0.3–1.7) 46
Zhengzhou 1991–1994 0–14 ⑤ 2 0.2 8 1 10 0.6 (0.3–1.1) 46
Zunyi 1990–1995 0–14 ⑤ 1 0 2 0.1 3 0.1 (0.0–0.2) 46
India
Karnataka 0–15 ⑤ 3.7 4 58
Israel 1975–1980 0–14 ① 4.4 6.7 296 5.5 59
1989–1990 0–14 64 4.4 (3.4–5.6) 92 6.7 (5.4–8.2) 156 5.5 (4.7–6.5) 59
1990–1993 0–14 5.5 6.6 6 (5.4–6.7) 46
1990–1993 0–17 201 7.0 (6.1–8.0) 206 7.6 (6.6–8.7) 407 7.3 (6.6–8.0) 60
1990–1994 0–14 167 5.5 194 6.6 361 6.0 (5.42–6.67) 4
Japan 1986–1990 0–14 ⑤ 522 1.2 (1.1–1.3) 738 1.8 (1.7–1.9) 1260 1.5 (1.4–1.6) 61
Chiba 1990–1993 0–14 ⑤ 27 1.2 34 1.6 61 1.4 (1.1–1.8) 46
Hokkaido 1974–1986 0–14 ⑤ 1.3 2.1 283 1.7 62
1990–1993 0–14 45 2.2 44 2.1 89 2.2 (1.7–2.6) 46
Okinawa 1990–1993 0–14 ③ 6 1 11 1.8 17 1.4 (0.8–2.2) 46
Kuwait 1992–1993 0–14 ② 47 16.58 (12.2–22.1) 39 14.11(10.0–19.3) 86 15.36 (12.4–19.1) 63
1992–1994 0–14 82 19.2 71 17.3 153 18.3 (15.5–21.4) 4
1992–1999 0–14 21.7 22.9 22.3 (20.5–24.2) 46
Pakistan
Karachi 1990 0–14 ② 9 0.5 16 0.9 25 0.7 (0.44–0.99) 4
1990–1999 0–14 0.4 0.5 0.5 (0.3–0.5) 46
Republic of Korea
Seoul 1985–1988 0–14 ⑤ 0.6 0.8 71 0.7 64
1990–1991 0–14 ⑤ 1.1 1.2 1.1 (0.9–10.4) 46
Russia
Novosibirsk 1983–1989 0–14 ⑥ 4.6 4.9 4.7 65
1990–1994 0–14 90 5.7 101 6.4 191 6.0 (5.18–6.94) 4
1990–1999 0–14 6.8 7.1 6.9 (6.3–7.6) 46
Saudi Arabia 1986–1997 0–14 ② 19 9.9 (5.4–17.7) 27 14.8 (8.9–23.9) 46 12.3 (8.4–17.9) 66
Al-Madinah 2004–2009 0–12 ② 170 22.2 (19.1–25.7) 249 33.0 (29.1–37.3) 419 27.6 (25.0–37.3) 67
Eastern 1990–2007 0–14 ② 195 243 438 27.52 (26.7–28.3) 68
Europe
Austria 1979–1993 0–14 ③ 7.8 45
1989–1990 0–14 107 7.9 (6.5–9.3) 98 7.5 (6.1–9.2) 205 7.7 (6.7–8.8) 59
1990–1994 0–14 348 9.8 312 9.3 660 9.6 (8.84–10.31) 4
1990–1999 0–14 10.3 9.5 9.9 (9.4–10.4) 46
2000–2005 0–14 610 14.8 (13.6–16.0) 561 14.3 (13.2–15.5) 1171 14.6 (13.7–15.4) 69
Belgium
Antwerpen 1989–1990 0–14 ③ 15 9.2 (5.2–15.3) 16 10.4 (5.9–16.9) 31 9.8 (6.7–13.9) 59
1990–1994 0–14 44 10.5 51 12.8 95 11.6 (9.40–14.41) 4
1990–1999 0–14 10.7 12.8 11.7 (10.2–13.5) 46
Belarus
Gomel 1976–1999 0–14 ⑥ 433 4.6 (4.4–4.8) 70
Bosnia and Herzegovina
Tuzla 1990–1998 0–14 ⑥ 22 3.39 (1.8–4.9) 21 3.37 (1.7–5.0) 43 3.38 (2.3–4.5) 71
Bulgaria
Sofia 1987–1991 0–14 ⑥ 6.7 72
East 1974–1995 0–14 ⑥ 6.3 45
Varna 1990–1994 0–14 ① 82 5.9 100 7.6 182 6.8 (5.80–7.83) 4
1990–1999 0–14 7.9 8.3 8.1 (7.4–9.0) 46
West-Bulgaria 1990–1994 0–14 ③ 131 9.9 125 10 256 9.9 (8.71–11.21) 4
1990–1999 0–14 11.6 9.8 10.7 (9.8–11.6) 46
Croatia 1995–2003 0–14 ① 369 9.26 (8.30–10.21) 323 8.47 (7.54–9.41) 692 9.05 (8.38–9.72) 25
Zagreb 1988–1992 0–14 ⑥ 7.7 6.7 72 7.2 73
Czech Republic 1990–1997 0–14 ③ 814 10.0 (9.4–10.7) 790 10.2 (9.5–11.0) 1604 10.1 (9.6–10.6) 74
1995–1999 0–14 12.6 12.7 12.7 (11.9–13.5) 46
1990–2001 0–14 2644 11.4 (11.0–11.9) 75
Denmark
3 countries 1989–1994 0–14 ③ 34 21.5 (14.9–30.1) 32 21.4 (14.7–30.3) 66 21.5 (16.6–27.3) 59
Four countries 1990–1994 0–14 ③ 96 16.4 81 14.5 177 15.5 (13.3–17.9) 4
1990–1999 0–14 17.1 16.2 16.6 (14.9–18.4) 46
Estonia 1983–1990 0–14 ③ 149 6.3(5.3–7.4) 142 6.3 (5.3–7.5) 291 10.1 (8.9–11.4) 76
1991–1998 0–14 153 6.7 (5.7–7.9) 157 7.2 (6.1–8.4) 210 12.3 (11.0–13.8) 76
1990–1994 0–14 85 9.9 93 11.2 178 10.5 (9.05–12.20) 4
1990–1999 0–14 12.6 10.9 11.7 (10.6–13.0) 46
Finland 1987–1992 0–14 ③ 1113 37.6 (35.5–39.9) 949 33.5 (31.5–35.8) 2062 35.7 (34.1–37.2) 77
1983–1990 0–14 1447 35.9 (34.1–37.8) 1198 31.2 (29.5–33.0) 2645 34.6 (33.3–36.0) 76
1987–1991 0–14 1728 35.4 (33.9–37.4) 78
1991–1998 0–14 1654 1497 3151 40.8 (39.4–42.2) 76
1990–1994 0–14 915 37 853 36 1768 36.5 (34.8–38.3) 4
1990–1999 0–14 41.9 39.9 40.9 (39.6–42.2) 46
2 regions 1989–1990 0–14 ③ 84 47.0 (37.5–58.1) 67 38.8 (30.5–50.0) 151 42.9 (36.6–50.6) 59
France 1988 0–19 ③ 96 7.86 (6.63–9.09) 79 6.96 (5.76–8.16) 175 7.41 (6.55–8.27) 79
1997 0–19 117 10.48 (6.13–11.83) 93 8.68 (7.39–9.97) 210 9.58 (8.64–10.52) 79
Four regions 1989–1990 0–14 ③ 134 7.8 (6.6–9.3) 127 7.8 (6.5–9.2) 261 7.8 (6.9–8.8) 59
1990–1994 0–14 372 8.7 337 8.3 709 8.5 (7.9–9.1) 46
FYR Macedonia 1995–1999 0–14 ⑥ 4.9 3.5 4.2 (3.4–5.2) 46
Germany 1999–2003 0–14 ③ 19.9 (19.0–20.7) 18.9 (18.1–19.8) 12335 19.4 (18.7–20.1) 80
2004–2008 0–14 23.5 (22.5–24.5) 22.4 (21.4–23.3) 13299 22.9 (24.6–28.0) 80
Düsseldorf 1995–1999 0–14 ③ 14.8 16.1 15.4 (13.8–17.2) 46
Baden-Württemberg 1990–1994 0–14 ③ 463 11 440 10.9 903 11.0 (10.3–11.7) 4
1990–1999 0–14 12.7 12.6 12.6 (12.1–13.2) 46
1987–2003 0–14 14.1 (13.7–14.6) 81
1999–2003 0–14 17.4(16.6–18.1) 16.5 (15.9–17.2) 1492 17.0 (16.4–17.6) 80
2004–2008 0–14 22.7 (21.9–23.6) 21.7 (20.8–22.5) 1832 25.4 (24.1–26.8) 80
North Rhine-Westphalia 1999–2003 0–14 ③ 21.8 (21.1–22.5) 20.8 (20.0–21.5) 3112 21.3 (20.7–21.9) 80
2004–2008 0–14 25.0 (24.1–25.8) 23.8 (23.0–24.6) 3295 24.4 (23.8–25.0) 80
Saxony 1999–2003 0–14 ③ 15.8 (14.7–16.9) 15.0 (14.0–16.1) 411 17.7 (15.9–19.6) 80
2004–2008 0–14 20.8 (19.4–22.2) 19.8 (18.5–21.1) 445 20.3 (19.1–25.5) 80
Greece 1992 0–14 ① 6.7 6.5 137 6.6 82
Attica 1990–1994 0–14 ① 149 10.2 124 9.1 273 9.7 (8.55–10.92) 4
1990–1999 0–14 11 9 10 (9.2–10.9) 46
Athens region 1989–1990 0–14 ① 72 10.9 (8.5–13.7) 50 7.7 (5.7–10.2) 122 9.3 (7.7–11.1) 59
Northen 5 regions 1989–1990 0–14 ① 9 5.3 (2.4–10.1) 6 3.8 (1.4–8.2) 15 4.6 (2.6–7.5) 59
Hungary 1978–1987 0–14 ⑥ 1060 6.1 (4.7–7.3) 83
Eighteen countries 1989–1990 0–14 ⑥ 132 7.7 (6.4–9.1) 124 7.5 (6.3–9.0) 256 7.6 (6.7–8.6) 59
1990–1994 0–14 337 8.7 360 9.6 697 9.1 (8.43–9.81) 4
1990–1999 0–14 9.6 9.8 9.7 (9.2–10.2) 46
Italy 1990–2003 0–14 ① 2840 13.13 (12.66–13.62) 2340 11.35 (10.90–11.82) 5180 12.26 (11.93–12.60) 84
Lazio 1989–1990 0–14 ① 66 7.2 (5.5–9.2) 51 5.8 (4.4–7.7) 117 6.5 (5.4–7.8) 59
1990–1994 0–14 164 8 162 8.3 326 8.1 (7.28–9.07) 4
1990–1999 0–14 8.9 8.6 8.8 (8.1–9.4) 46
Lombardia 1989–1990 0–14 ① 110 7.6 (6.3–9.2) 83 5.9 (4.7–7.3) 193 6.8 (5.8–7.8) 59
1990–1994 0–14 239 7.6 204 6.8 443 7.2 (6.55–7.92) 4
1990–1995 0–14 7.2 6.5 6.9 (6.3–7.5) 46
Marche 1990–1994 0–14 ① 55 10.5 44 8.9 99 9.7 (7.90–11.84) 4
1990–1999 0–14 10.5 9.7 10.1 (8.8–11.6) 46
Pavia 1990–1994 0–14 ① 17 11.6 17 11.9 34 11.7 (8.08–16.44) 4
1990–1999 0–14 12.3 12.5 12.4 (9.7–15.6) 46
Sardinia 1989–1990 0–14 ① 126 33.5 (27.9–39.9) 95 26.9 (21.7–32.9) 221 30.2 (26.4–34.4) 59
1990–1994 0–14 337 43.6 211 29.5 548 36.8 (33.72–39.98) 4
1990–1998 0–14 45 30.6 37.8 (35.5–40.3) 46
Eastern Sicily 1989–1990 0–14 ① 29 11.2 (7.5–16.1) 23 9.0 (5.7–13.5) 52 10.1 (7.5–13.2) 59
1990–1994 0–14 75 13.4 53 9.9 128 11.7 (9.8–13.9) 46
Turin 1984–1991 0–14 ① 116 8.42 (6.99–10.10) 111 8.42 (6.95–10.19) 227 8.42 (7.37–9.62) 85
1990–1994 0–14 86 11.9 69 10.1 155 11.0 (9.32–11.15) 4
1990–1999 0–14 11.7 10.3 11 (9.8–12.3) 46
Roman and Lazio region 1989–1993 0–14 ① 7.9(6.8–9.2) 7.8(6.7–9.1) 7.9 (7.1–8.8) 86
Liguria 1989–1998 0–14 ① 126 14.15 (11.9–16.9) 93 10.88 (8.9–13.3) 219 12.56 (11.0–14.3) 87
Iceland 1970–1979 0–14 ③ 31 9.3 (6.3–13.2) 21 6.6 (4.1–10.1) 52 8.0 (8.4–13.8) 88
1980–1989 0–14 34 10.5 (7.3–14.7) 34 11.1 (7.6–15.5) 68 10.8 (8.4–13.8) 88
Latvia 1983–1990 0–14 ③ 229 6.6 (5.8–7.5) 227 6.7 (5.8–7.6) 456 6.6 (5.8–7.3) 76
1991–1998 0–14 242 6.9 (6.0–7.8) 263 7.7 (6.8–8.7) 505 7.4 (6.6–8.2) 76
1990–1992 0–14 59 7 47 5.7 106 5.9 (5.06–6.98) 4
1990–1999 0–14 7.8 7 7.4 (6.6–8.3) 46
Lithuania 1983–1990 0–14 ③ 143 9.7 (8.2–11.4) 132 9.5 (7.9–11.3) 275 6.8 (6.2–7.5) 76
1991–1998 0–14 162 12.5 (10.7–14.6) 139 10.9 (9.1–12.8) 301 7.8 (7.1–8.5) 76
1990–1994 0–14 162 7.7 145 7.1 307 7.4 (6.57–8.25) 4
1990–1999 0–14 7.6 8.2 7.9 (7.3–8.5) 46
1983–2000 0–14 543 7.3 (6.7–7.9) 557 7.8 (7.1–8.4) 1100 7.5 (7.1–8.0) 89
Luxemburg 1977–1986 0–14 ③ 12.1 12.6 16 12.4 59
1989–1990 0–14 8 12.1 (5.2–23.9) 8 12.6 (5.4–24.8) 16 12.4 (7.1–20.1) 59
1990–1994 0–14 22 12.6 17 10.2 39 11.4 (8.14–15.59) 4
1990–1999 0–14 10.3 12.2 11.3 (9.0–13.9) 46
The Netherlands
Five regions 1989–1990 0–14 ③ 30 11.2 (7.6–16.0) 28 10.8 (7.2–15.7) 58 11.0 (8.4–14.3) 59
1990–1994 0–14 178 12.9 175 13.2 353 13 (11.7–14.4) 46
Macedonia 1985–1991 0–14 2.4 2.5 112 2.5 90
Malta 1980–1987 0–14 ⑥ 43 12.7 (9.6–15.8) 47 14.6 (11.3–17.9) 90 13.6 (11.0–16.2) 91
2006–2010 0–14 41 40 81 24.68 (21.98–27.43) 92
Montenegro 1997–2006 0–14 ③ 90 12.6 (10.1–15.5) 94 14.3 (11.5–17.5) 184 13.4 (11.5–15.5) 93
Norway 1973–1982 0–14 ③ 1914 20.5 94
2004–2012 0–14 33.9 (32.2–35.7) 31.4 (29.7–33.2) 32.7 (31.5–34.0) 95
Eight countries 1989–1990 0–14 87 22.3 (17.9–27.6) 71 19.3 (15.1–24.3) 158 20.8 (17.7–24.3) 59
1990–1994 0–14 222 22.4 187 19.9 409 21.2 (19.18–23.29) 4
1990–1999 0–14 21.6 19.9 20.8 (19.4–22.1) 46
Poland
 9 western provinces 1989–1990 0–14 ⑥ 80 5.3 (4.6–6.5) 84 5.8 (4.6–7.2) 164 5.5 (4.7–6.4) 59
 3 cities 1989–1990 0–14 ⑥ 51 5.7 (4.2–7.5) 51 6.0 (4.5–7.9) 102 5.8 (4.8–7.1) 59
 Cracow 1990–1999 0–14 ⑥ 7.5 7.6 7.6 (7.0–8.2) 46
 Upper Silesia 1995–1999 0–14 ⑥ 8 9.5 8.8 (7.9–9.7) 46
 Wielkopolska 1990 0–14 ⑥ 28 4.1 40 6 68 5 (3.88–6.36) 4
Portugal
3 regions combined 1989–1990 0–14 ① 17 10.1 (5.9–16.1) 8 4.9 (2.1–9.6) 25 7.5 (4.8–11.0) 59
Algarve 1990–1994 0–14 ① 26 16.3 19 12.9 45 14.6 (10.62–19.64) 4
Coimbra 1990–1994 0–14 ① 19 9.4 19 9.9 38 9.7 (6.76–13.36) 4
1990–1999 0–14 10.1 9.1 9.6 (7.6–12.2) 46
Madeira Island 1990–1994 0–14 ③ 10 6.9 11 7.5 21 7.2 (4.46–11.05) 4
1990–1999 0–14 7.1 6.8 6.9 (5.0–9.4) 46
Portalegre 1990–1994 0–14 ① 9 15.9 14 26.7 23 21.3 (13.29–31.89) 4
Romania
Bucharest 1989–1990 0–14 ⑥ 22 4.6 (2.9–6.9) 25 5.7 (3.7–8.4) 47 5.1 (3.8–6.8) 59
1990–1994 0–14 52 4.2 65 5.9 117 5.0 (4.14–6.05) 4
1990–1999 0–14 4.7 5.9 5.3 (4.7–6.1) 46
Silesian 1989–2005 0–14 ⑥ 720 10.01 (8.58–11.45) 665 9.72 (8.32–11.31) 1385 9.87 (8.45–11.47) 96
Slovakia 1990–1994 0–14 ⑥ 261 7.9 289 9.1 550 8.5 (7.81–9.25) 4
1990–1999 0–14 9.7 9.7 9.7 (9.2–10.3) 46
2000 0–14 81 15.04 66 12.83 147 13.96 (11.35–15.72) 97
Slovenia 1989–1990 0–14 ① 23 5.2 (3.3–10.4) 33 7.7 (5.3–10.9) 56 6.5 (4.9–8.4) 59
1990–1994 0–14 70 6.8 88 9 158 7.9 (6.68–9.23) 4
1990–1998 0–14 142 8.28 (6.9–9.6) 157 9.63 (8.1–11.1) 299 8.94 (7.9–9.9) 71
1990–1999 0–14 8.3 9.5 8.9 (8.0–9.9) 46
Spain
Catalonia 1989–1990 0–14 ① 151 10.5 (8.8–12.3) 146 10.6 (9.0–12.5) 297 10.6 (9.4–11.9) 59
1990–1994 0–14 358 12.5 338 12.6 696 12.5 (11.55–13.50) 4
1990–1999 0–14 12.6 12.3 12.4 (11.7–13.1) 46
 Biscay 1990–2013 0–14 ③ 199 10.4 (8.9–11.8) 200 11.5 (9.5–12.6) 399 10.7 (9.6–11.7) 98
 Extremadura 2003–2007 0–14 ① 104 24.9 (20.1–29.7) 104 26.2 (21.2–31.6) 208 25.5 (22.1–29.0) 99
 Madrid 1985–1988 0–14 ⑥ 11.3 10.5 501 10.9 100
 Cordoba 1991–1992 0–14 ① 21 6.2 26 7.9 47 7 (5.20–9.26) 4
Sweden 1978–1987 0–14 ③ 2012 25 1824 23.8 3838 24.4 101
1990–1994 0–14 1135 28.1 1031 26.9 2166 27.5 (26.36–28.67) 4
1990–1999 0–14 30.5 29.4 30 (29.1–30.8) 46
1983–2000 0–14 4171 29.2 (28.3–30.1) 3860 28.5 (27.6–29.4) 8031 28.9 (28.2–29.5) 89
2002–2004 0–14 42.9 (38.7–47.7) 42.1 (37.6–46.7) 2046 42.5 (39.3–45.7) 102
2005–2007 0–14 46.7 (41.6–51.5) 41.2 (36.0–45.6) 2029 43.9 (40.7–47.3) 102
Serbia
Belgrade 1982–1992 0–14 ⑥ 126 7.6 (6.4–9.1) 133 8.6 (7.2–10.2) 289 8.1 (7.1–9.2) 103
1982–2005 0–14 372 10.6 (9.5–11.8) 330 10.5 (9.4–11.7) 702 10.6 (9.8–11.4) 104
 Switzerland 1995–1999 0–14 ① 13.3 10.7 12 (11.2–12.9) 46
Turkey
 Diyarbakir 2010–2011 0–14 ⑥ 24 8.7 17 5.7 41 7.2 105
UK
Scotland 1976–1983 0–14 ③ 20 19.4 1856 19.7 62
1990 0–14 16 32.5 7 15 23 24.0 (15.22–36.01) 4
1990–1999 0–14 26.8 25.9 26.4 (25.4–27.4) 46
Leicestershire 1971–1980 0–14 10.6 (5.1–17.1) 106
1990–1994 0–14 ③ 70 15.4 66 15.3 136 15.3 (12.85–18.07) 4
Northern Ireland 1989–1990 0–14 ③ 71 17.8 (13.9–22.5) 59 15.4 (11.7–19.8) 130 16.6 (13.9–19.7) 59
1990–1994 0–14 202 20.1 185 19.3 387 19.7 (17.81–21.79) 4
1990–1999 0–14 21.5 21.2 21.3 (19.9–22.8) 46
Oxford 1985–1995 0–14 ③ 572 19.9 (18.3–21.5) 465 17.2 (15.6–18.7) 1037 18.6 (17.4–19.8) 107
1989–1990 0–14 90 17.8 (14.3–21.9) 71 14.9 (11.7–18.8) 161 16.4 (13.9–19.1) 59
1990–1994 0–14 266 20.1 191 15.3 457 17.8 (16.18–19.46) 4
Plymouth 1990–1994 0–14 ③ 63 16.5 65 18.1 128 17.3 (14.41–20.53) 4
1990–1999 0–14 17.1 20.8 19 (16.8–21.2) 46
Yorkshire 1978–2007 0–14 ③ 2662 18.1 (17.6–18.7) 108
1990–1999 0–14 18.9 18.1 18.5 (17.5–19.5) 46
 Tayside 1980–1983 0–14 ③ 19.7 22.1 64 20 62
 Bradford 1978–1998 0–14 ③ 142 12.4 (10.4–14.4) 147 13.6 (11.4–15.8) 289 13.0 (11.5–14.5) 109
 Far the south-west England 1975–1996 0–14 ③ 228 13.63 (12.00–15.47) 260 16.29 (14.49–18.38) 488 14.93 (13.58–16.16) 110
North America
Canada
 Newfoundland and Labrador 1995–2002 0–19 ⑥ 400 77.3 (69.9–85.3) 494 100.2 (91.6–109.4) 894 88.6 (74.0–105.4) 111
 Edmonton 1990–1996 0–14 ⑥ 23 23.6 23.3 (20.5–26.4) 46
 Calgary 1990–1999 0–14 ⑥ 20.3 20.9 20.6 (18.5–22.7) 46
Prince Edward Island 1975–1986 0–14 ⑥ 27 20.8 92 23.9 62
1990–1993 0–14 17 28 12 20.8 29 24.5 (16.38–35.16) 4
 The Avalon Peninsula 1987–2002 0–14 ⑥ 140 36.15 134 35.69 274 35.93 112
Montreal 1971–1985 0–14 ⑥ 9.6 10 919 9.8 62
1971–1983 0–14 9 9.1 9.0 (7.7–10.6) 113
 Alberta 1990–1994 0–14 ⑥ 87 23.4 88 24.7 175 24.0 (20.62–27.82) 4
 Manitoba 1991–1993 0–14 ⑥ 21.4 20.7 21.1 (17.1–25.9) 4
USA
 Allegheny, PA 1990–1994 0–14 ⑥ 112 19.1 94 16.4 206 17.8 (15.45–20.33) 4
 Chicago, IL 190–1994 0–14 ⑥ 131 10.2 169 13.3 300 11.7 (10.47–13.12) 4
1994–2003 0–17 617 16.0 (14.6–17.6) 749 20.1 (18.3–22.1) 1366 18.1 (16.9–19.3) 114
 Jefferson, AL 1990–1994 0–14 ⑥ 50 14.6 51 15.4 101 15.0 (12.21–18.22) 4
1990–1995 0–14 14.1 15.1 14.6 (12.2–18.2) 46
 Colorado ⑥
 non-Hispanics 1978–1988 0–17 654 16.4 (15.1–17.7) 544 14.5 (13.3–15.7) 115
 Hispanics 1978–1988 0–17 56 7.1 (5.4–9.3) 79 10.5 (8.4–13.1) 115
 North Dakota 1980–1986 0–14 ⑥ 21.6 16.2 204 18.9 116
 Wisconsin (part) 1970–1979 0–14 ⑥ 20.2 16.2 166 18.2 62
 Rochester 1965–1979 0–14 ⑥ 15.8 18.4 38 17.1 62
 Philadelphia 1985–1989 0–14 ⑥ 11.3 14.8 215 13.4 117
 San Diego 1978–1981 0–14 ① 9.6 9.1 48 9.4 62
South America
 Argentina
Avellaneda 1985–1990 0–14 ④ 30 6.7 118
1990–1994 0–14 11 5.6 15 7.5 26 6.5 (4.31–9.51) 4
1990–1996 0–14 5.3 7.2 6.3 (5.7–11.1) 46
Corrientes 1992–1994 0–14 ④ 4 2.9 8 5.7 12 4.3 (2.21–7.51) 4
1992–1999 0–14 4.7 8.5 6.6 (5.0–8.7) 46
Tierra del Fuego 1993–1994 0–14 ③ 4 20.2 0 4 8.0 (2.18–17.60) 4
1993–1996 0–14 14.2 6.3 10.3 (5.5–18.5) 46
Brazil
Sao Paulo 1987–1991 0–14 ⑤ 5.8 9.5 52 7.6 119
1990–1992 0–14 15 6.9 19 9.1 34 8 (5.53–1.14) 4
 Passo Fundo 1996–1999 0–14 ⑤ 5.4 8.7 7 (4.1–11.9) 46
Chile 1990–1991 0–14 ② 2.2 2.8 52 2.5 120
Santiago 1990–1992 0–14 ① 66 1.7 56 1.5 122 1.6 (1.28–2.04) 4
1990–1999 0–14 3.6 3.9 3.7 (3.4–4.0) 46
 Colombia 1990 0–14 ⑦ 4.7 2.9 3.8 (2.9–4.9) 4
 Cali 1995–1999 0–14 ⑦ 0.4 0.5 0.5 (0.3–0.7) 46
 Bogota 1990 0–14 ⑦ 35 4.7 21 2.9 56 3.8 (2.88–4.93) 4
 Paraguay 1990–1994 0–14 ④ 45 1 34 0.8 79 0.9 (0.71–1.11) 4
1990–1999 0–14 1 0.8 0.9 (0.8–1.0) 46
Peru
Lima 1990–1991 0–14 ② 0.2 0.6 0.4 (0.22–0.61) 4
1990–1994 0–14 0.4 0.6 0.5 (0.4–0.64) 46
Uruguay
 Montevideo 1992 0–14 ⑤ 13 8.3 13 8.3 26 8.3 (5.38–12.10) 4
Venezuela
 Caracas 1992 0–14 ④ 18 0.1 25 0.2 43 0.1 (0.09–0.18) 4
Central America and West Indies
 Antigua 1989–1993 0–19 ③ 3.5 (0.9–8.8) 121
Barbados 1982–1991 0–14 ③ 37 5 122
1989–1993 0–19 2.6 (1.3–4.6) 121
1990–1993 0–14 3 2.4 2 1.6 5 2.0 (0.32–6.36) 4
Cuba 1978–1990 0–14 ⑦ 2.5 2.8 267 2.7 62
1990–1994 0–14 152 2.5 197 3.4 349 2.9 (2.63–3.24) 4
1990–1999 0–14 2.1 2.5 2.3 (2.2–2.5) 46
Dominican Republic 1990–1993 0–14 ③ 3 6.6 2 4.9 5 5.7 (1.53–14.65) 4
1995–1999 0–14 0.7 0.3 0.5 (0.4–0.7) 46
 Mexico
 Mexico city 1984–1986 0–14 ⑥ 0.4 0.7 100 0.6 62
 Veracruz 1990–1993 0–14 ④ 3 6 9 1.5 (0.70–2.94) 4
Puerto Rico (USA) 1985–1994 0–14 ⑦ 18.0 (17.6–18.3) 123
1990–1994 0–14 398 16.2 445 18.7 843 17.4 (16.25–18.63) 4
1990–1999 0–14 15.8 17.8 16.8 (16.0–17.6) 46
Virgin Islands (USA) 1990–1994 0–14 ③ 9 14.7 7 11.5 16 13.1 (7.64–21.01) 4
1990–1996 0–14 14 12.8 (8.1–18.8) 46
Oceania
 Australia 2000–2011 0–14 ② 6049 24.2 (23.6–24.8) 5526 23.0 (22.4–23.7) 11575 23.6 (23.2–24.0) 124
West 1985–1992 0–14 ④ 14.9 45
1985–2002 0–14 560 15.6 (13.7–17.5) 584 17.3 (15.3–19.4) 1144 16.5 (14.7–18.2) 24
1985–2010 0–14 17.7 (16.9–19.3) 18.5 (17.4–19.8) 18.1 (17.5–19.2) 125
New South Wales 1990–1993 0–14 ① 335 13.1 387 15.9 722 14.5 (13.42–15.55) 4
1990–1996 0–14 17.0 (14.1–20.6) 18.6 (15.4–22.3) 17.8 (15.6–20.3) 26
New Zealand
Auckland 1978–1985 0–14 ③ 9 10.5 233 9.8 62
1990–1994 0–14 65 12.3 70 13.6 135 12.9 (10.87–15.28) 4
1990–1996 0–14 12.9 14.6 13.7 (12.0–15.7) 46
Canterbury 1981–1986 0–14 ③ 10.2 12.9 39 11.6 62
1990–1994 0–14 43 23.9 35 19.8 78 21.9 (17.33–27.32) 4
1990–1999 0–14 23.8 20.8 22.3 (19.1–25.9) 46
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Data showed as mean (95% CI); *represented boy vs. girl, p > 0.05, p derived from t-test; ①, Mediterranean climate; ②, Desert Climate; ③, Oceanic climate; ④, Savanna climate; ⑤, Monsoon climate; ⑥, Continental climate; ⑦, Rainforest climate.

Quality assessment

All abstracts ascertained initial search were screened and the researches in violation of inclusion criteria were excluded by two authors. Full-texts were posteriorly accessed by another two authors, in case of disagreement, a third professor was invited to evaluate such studies and the consensus was achieved via discussion. If original data was missing, the corresponding author of this study was contacted with alone tailored application forms by email.

Climate Style, latitude, and sunshine durations

Mediterranean climate, monsoon climate, oceanic climate, continental climate, savanna climate and rainforest climate were included in this study. Climate style met the announcement of national climate center, and the missing information was searched in the climate of the countries of the world19. Latitude of every center was identified by Google Earth’s high-resolution satellite image20, and if the countries didn’t have centers records, we would extract the latitude of the capital. Sunshine durations of the capital in each country was ascertained by average sunshine durations timetable around the world21. Mediterranean climate is the climate typical of the lands around the Mediterranean Sea from the largest areas, but it is also found in sections of Asia, in most coastal California, and in parts of Southern and West of Australia. Monsoon is currently defined as a seasonal changing in atmospheric precipitation and circulation associated with the asymmetric heating of land and sea. Oceanic climate is the typical of west coasts in higher middle latitudes of regions, with few extremes of temperature and a relatively narrow annual temperature range, and generally features cool summers and winters. Continental climate is referred to climates with significantly annual variation in temperature, which tended to occur in the middles of continents, mostly occur in the mainland China and the eastern U.S.22.

Statistical methods

The incidence of CT1DM for our study was obtained from the individual studies as it was researched in these publications. The incidence rates were calculated per 100, 000 people a year. Age standardization of the incidence rates was calculated using 5-years intervals with age groups 0–4 years, 5–9 years, and 10–14 years as the standard. The latitude groups 0°–23°26′N/S, 23°26′–40°N/S, and 40°–66°34′N/S as the study standard according to the tropic of Cancer/Capricorn, the Arctic/Antarctic circle, and westerlies, which based on geographic meteorology.

Statistical analysis was performed using SPSS version 20.0 (SPSS Inc., Chicago, IL, USA). Continuous data that accord with a normal distribution were presented as mean [95% confidence interval (CI)], with least significant difference in parameters between two groups were analyzed by t-test, and the one-way ANOVA was used to assess the multiple groups for continuous variables in normal distribution. A p < 0.05 is considered to be statistically significant difference.

Results

Description of the included studies

After initial screening and removal of duplicates, we reviewed 3602 articles in full, of which 87 eligible studies on the incidence of CT1DM in various countries were included in this study (Table 1). Included studies on incidence of CT1DM entailed 118 records for centers in 72 countries. The numbers of records were available for North America (n = 17), South America (n = 10), Asia (n = 30), Europe (n = 47), Oceania (n = 3), Central America and West Indies (n = 2), and Africa (n = 9). The numbers of records were obtainable for Mediterranean climate (n = 22), Monsoon climate (n = 22), Oceanic climate (n = 22), Continental climate (n = 34), Desert climate (n = 11), Savanna climate (n = 5), and Rainforest climate (n = 2). The specific characteristics of included articles are displayed in Tables 1 and 2.

Table 2.

The characteristics of incidence of childhood type 1 diabetes mellitus (per 100,000 children/yr) in different age-groups.

Countries and centers Search periods 0–4 years old* 5–9 years old** 10–14 years old
Case (n) Incidence Case (n) Incidence Case (n) Incidence
Australia 2000–2011 2402 14.9 (14.3–15.5) 4007 24.7 (23.9–25.4) 5166 31.0 (30.2–31.9)
West 1985–2002 249 11.0 (9.2–12.8) 437 18.8 (16.3–21.3) 458 19.6 (17.6–21.6)
1985–2010 11.0 (10.3–12.6) 21.1 (19.5–22.6) 25.5 (20.8–23.9)
New South Wales 1990–1996 10.8 (7.9–14.4) 17.8 (14.1–22.4) 25.0 (20.4–30.5)
Belarus 1976–1999 2.7 5.2 9.3
Canada
 Newfoundland and Labrador 1995–2002 59 29.6 (22.6–38.3) 213 90.5 (78.9–103.6) 348 127.4 (114.4–141.5)
 The Avalon Peninsula 1987–2002 58 24.95 95 37.01 121 43.62
China
 Shanghai 1980–1991 16 0.26 (0.15–0.42) 41 1.25 (0.89–1.70) 18 0.62 (0.37–0.98)
1989–1993 15 0.56 (0.32–0.93) 28 1.02 (0.68–1.47) 15 0.94 (0.52–1.55)
 Hong Kong 1997 43 0.9 84 1.5 91 1.7
 Beijing 1995–2000 0.41 (0.20–0.61) 1.47 (1.07–1.90) 1.49 (1.21–1.73)
2001–2005 0.79 (0.65–0.93) 1.79 (1.43–2.15) 2.22 (1.91–2.53)
2006–2010 0.92 (1.81–3.15) 2.83 (1.68–3.85) 2.99 (1.93–4.04)
Croatia 1995–2003 134 5.77 (4.79–6.74) 255 9.80 (8.60–11.01) 303 11.13 (9.88–12.38)
Czech 1990–1997 5.9 (5.3–6.7) 10.5 (9.7–11.5) 13.1 (12.2–14.1)
Germany
1999–2003 14.5 (14.0–15.1) 21.5 (20.1–22.9) 22.2 (20.8–23.7)
2004–2008 17.1 (16.5–17.8) 25.4 (23.8–27.1) 26.3 (24.6–28.0)
 Baden-Württemberg 1987–2003 5.8 (2.5–9.3) 3.4 (0.8–6.0) 2.7 (0.3–5.1)
1999–2003 12.7 (11.9–13.5) 18.8 (17.7–19.9) 19.4 (18.3–20.6)
2004–2008 16.6 (15.6–17.6) 24.6 (23.3–25.9) 25.4 (24.1–26.8)
 North Rhine-Westphalia 1999–2003 15.9 (15.1–16.8) 23.5 (22.5–24.6) 24.4 (23.3–25.5)
2004–2008 18.2 (17.3–19.2) 27.0 (25.8–28.2) 28.0 (26.8–29.2)
 Saxony 1999–2003 11.5 (10.3–12.8) 17.0 (15.3–18.9) 17.7 (15.9–19.6)
2004–2008 15.2 (13.7–16.8) 22.4 (20.3–24.8) 23.2 (21.0–25.7)
Italy
 Rome and Lazio Region 1989–1993 78 0.3 (5.0–7.9) 130 9.8 (8.3–11.6) 122 7.5 (6.2–9.0)
 Turin 1984–1991 40 5.49 (3.92–7.47) 62 7.30 (5.69–9.49) 125 11.17 (9.49–13.49)
 Liguria 1989–1998 50 9.01 (6.7–11.9) 72 13.03 (10.2–16.4) 97 15.01 (12.2–18.3)
 Apulia 2009–2013 149 20.1 (16.8–23.3) 1–4years 296 29.7 (26.3–33.1) 299 28.2 (25.0–31.4)
Jordanian 19992–1996 39 1.3 90 3.2 146 5.5
Kuwait 1992–1993 27 12.83 (8.46–18.74) 30 15.71 (10.60–22.46) 29 18.29 (12.25–26.34)
Libya
 Benghazi 1981–1990 21 2.2 (1.4–3.4) 54 7.2 (5.3–9.5) 90 14.8 (12.0–18.4)
Lithuania 1983–2000 185 4.0 (3.5–4.6) 395 8.0 (7.2–8.8) 520 10.5 (9.6–11.5)
Saudi Arabia 1986–1997 8 7.1 (3.6–13.2) 13 7.1 (3.7–13.2) 25 24.1 (15.9–35.7)
 Ai-Madinah 2004–2009 115 17.1 (14.2–20.5) 178 30.9 (26.6–35.7) 126 46.5 (38.9–55.2)
Serbia
Belgrade 1982–1992 40 3.9 (2.8–5.3) 98 8.9 (7.3–10.9) 121 11.2 (9.3–13.4)
1982–2005 108 5.5 (4.5–6.7) 256 11.9 (10.5–13.5) 346 15.4 (13.8–17.1)
Silesian 1989–2005 5.33 (4.31–6.55) 9.86 (8.45–11.45) 13.20 (11.53–15.05)
Slovenia 1990–1998 59 6.17 (4.5–7.7) 103 9.20 (7.4–10.9) 137 10.79 (9.0–12.6)
Bosnia and Herzegovina
Tuzla 1990–1998 3 0.80 (0–1.7) 18 4.68 (2.5–6.8) 22 5.16 (2.8–7.5)
Slovakia 2000 10.5 12.57 17.97
Spain
Extremadure 2003–2007 48 18.5 (10.1–30.3) 66 25.2 (20.1–29.4) 94 31.8 (25.8–34.1)
Biscay 1990–2013 57 5.1 (3.8–6.5) 168 14.6 (12.4–16.8) 174 13.2 (11.3–15.2)
Sultanate of Oman 1993 1.54 2.32 3.69
1994 0.97 2.79 4.22
Sweden 1978–1987 759 15.7 1345 25.8 1734 30.6
1983–2000 1816 19.5 (18.6–20.4) 2961 31.7 (30.6–32.8) 3254 35.4 (34.2–36.6)
2002–2004 408 28.7 (23.9–33.5) 765 50.9 (44.5–57.0) 873 46.7 (41.5–52.2)
2005–2007 387 25.2 (20.8–29.6) 676 47.9 (41.6–54.1) 966 56.5 (50.5–62.9)
Turkey
Diyarbakir 2010–2011 8 4.3 17 9.1 16 8.4
UK
Leicestershire 1971–1980 6.3 (1.3–8.9) 10.9 (1.6–19.5) 15.1 (5.9–23.7)
Yorkshire 1978–2007 807 11.7 (10.9–12.5) 1330 18.6 (17.6–19.6) 1774 23.7 (22.6–24.8)
Bradford 1978–1998 70 9.3 (7.1–11.5) 88 12.1 (9.6–14.7) 131 17.9 (14.9–21.0)
Far the south-west 1975–1996 96 9.35 (7.57–11.42) 170 15.81 (13.52–18.37) 222 19.02 (16.44–21.51)
USA
Chicago 1994–2003 178 8.1 (7.0–9.5) 340 15.3 (13.7–17.2) 560 28.1 (25.5–30.9)
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Data showed as mean (95% CI); *represented 0–4 years old vs. 5–9 years old, p > 0.05; 0–4 years old vs. 10–14 years old, p < 0.01; **represented 5–9 years old vs. 10–14 years old, p > 0.05, p derived from one-way ANOVA.

Incidence of CT1DM

The average incidence of CT1DM in 70 countries showed in Fig. 1.

Figure 1.

Figure 1

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Incidence of childhood type 1 diabetes mellitus in 72 countries (the first author independently created map by software-Adobe Illustrator CS5 and Adobe Photoshop CS5, and the copyright of map belongs to first author).

Overall incidence of CT1DM

Overall incidence of CT1DM was 11.43 (10.31–12.55) per 100,000 children/yr, in addition, boy, 11.42 (10.23–12.61) per 100,000 children/yr; girl, 11.11 (9.94–12.27) per 100,000 children/yr. There no significant difference existed between two groups of gender (p > 0.05) (Table 1).

Incidence of CT1DM in different regions

Overall incidence in different regions was indicated as following: Europe, 13.93 (12.59–15.27) per 100,000 children/yr; Asia, 4.31 (2.37–6.26) per 100,000 children/yr; North America, 21.75 (13.79–29.70) per 100,000 children/yr; South America, 4.47 (3.06–5.88) per 100,000 children/yr; Africa, 7.38 (4.37–10.39) per 100,000 children/yr; Central America and West Indies, 6.71 (3.27–10.16) per 100,000 children/yr; and Oceanic, 16.47 (13.67–19.27) per 100,000 children/yr; North America vs. other regions showed p < 0.01 excluded Oceania (Fig. 2A).

Figure 2.

Figure 2

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Incidence of childhood type 1 diabetes mellitus in different regions, age-groups, climates, and sunshine durations. (A, Incidence of childhood type 1 diabetes mellitus in different regions: #indicated North America vs. other regions excluded Oceania, all p < 0.01; B, Incidence of childhood type 1 diabetes mellitus in three age-groups: #represented 0–4 years old vs. 10–14 years old, p < 0.01; C, Incidence of childhood type 1 diabetes mellitus in seven kinds of climates: *represented Monsoon climate vs. other climates excluded Savanna climate and Rainforest climate, all p < 0.01; D, Incidence of childhood type 1 diabetes mellitus in three sections of sunshine durations: #showed 3–4 hours/day vs. other two sections, both p < 0.01; all p derived from one-way ANOVA).

Incidence of CT1DM in different age-groups

Incidence of CT1DM in different age-groups as following: 0–4 years old, 9.70 (7.60–11.81) per 100,000 children/yr; 5–9 years old, 16.68 (12.51–20.86) per 100,000 children/yr; 10–14 years old, 20.27 (14.94–25.60) per 100,000 children/yr; 0–4 years old vs. 5–9 years old, p > 0.05; 5–9 years old vs. 10–14 years old, p > 0.05; 0–4 years old vs. 10–14 years old, p < 0.001 (Table 2, Fig. 2B).

Incidence of CT1DM in different climates type

Different gender for CT1DM incidence of different climates was displayed as follow: Monsoon climate: boy, 1.56 (0.95–2.16) per 100,000 children/yr; girl, 2.10 (1.28–2.92) per 100,000 children/yr; Oceanic climate: boy, 16.31 (14.29–18.33) per 100,000 children/yr; girl, 15.32 (13.51–17.12) per 100,000 children/yr; and the incidence of CT1DM of different genders in other climates showed in Table 3, all p > 0.05. Furthermore, overall incidence of different climates was presented as following: Mediterranean climate, 10.56 (5.69–12.42) per 100,000 children/yr; Monsoon climate, 2.12 (1.29–2.94) per 100,000 children/yr; Oceanic climate, 15.73 (13.93–17.54) per 100,000 children/yr; Continental climate, 12.30 (13.93–17.54) per 100,000 children/yr; Desert climate, 11.04 (7.06–15.02) per 100,000 children/yr; Savanna climate, 6.47 (2.68–10.26) per 100,000 children/yr; Rainforest climate, 7.58 (1.86–13.29) per 100,000 children/yr; pairwise comparison, Monsoon climate vs. other climates that excluding Savanna climate and Rainforest climate, all p < 0.01 (Fig. 2C).

Table 3.

The incidence of childhood type 1 diabetes mellitus (per 100,000 children/yr) with different gender in different climate.

Incidence P*
Boy Girl Total
Mediterranean Climate 11.46 (9.11–13.81) 10.58 (8.81–12.35) 10.56 (8.69–12.42) >0.05
Desert Climate 9.03 (5.76–12.29) 9.18 (5.39–12.98) 11.04 (7.06–15.02)
Oceanic Climate 16.31 (14.29–18.33) 15.32 (13.51–17.12) 15.73 (13.93–17.54)
Monsoon Climate 1.56 (0.95–2.16) 2.10 (1.28–2.92) 2.12 (1.29–2.94
Continental Climate 12.34 (8.98–15.69) 12.75 (8.77–16.73) 12.30 (13.93–17.54)
Savanna Climate 5.47 (1.01–9.93) 6.74 (1.96–11.52) 6.47 (2.68–10.26)
Rainforest Climate 6.11 (0.88–11.35) 6.44 (0.30–12.58) 7.58 (1.86–13.29)
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Data showed as Mean (95% CI); *represented boy vs. girl, all p > 0.05, p derived from the t-test.

Incidence of CT1DM in countries with different sunshine durations

Incidence of CT1DM in countries with different sunshine durations as following: 3–4 hours/day, 15.17 (11.14–19.20) per 100,000 children/yr; 4–5 hours/day, 8.77 (5.71–11.84) per 100,000 children/yr; above 5 hours/day, 6.96 (4.07–9.85) per 100,000 children/yr; 3–4 hours/day vs. other sunshine durations, p < 0.01; 4–5 hours/day vs. above 5 hours/day, p > 0.05 (Fig. 2D).

Incidence of CT1DM in centers with different latitude

Incidence of CT1DM in centers with different latitude as following: 0°–23°26′N/S: 4.98 (2.14–8.83) per 100,000 children/yr; 23°26′–40° N/S: 7.83 (6.01–9.84) per 100,000 children/yr; 40°–66°34′N/S: 14.71 (12.30–17.29) per 100,000 children/yr; 40°–66°34′N/S vs. other latitude, both p < 0.01; 0°–23°26′N/S vs. 23°26′–40° N/S, p > 0.05 (Fig. 3).

Figure 3.

Figure 3

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Incidence of childhood type 1 diabetes mellitus in three latitude sections (*expressed 40°–66°34′N/S vs. other two latitude sections, both p < 0.01, p derived from the one-way ANOVA).

Incidence of CT1DM during different periods

Incidence of CT1DM during different periods as following: 1965 to 1979, 9.44 (8.22–10.66) per 100,000 children/yr; 1980 to 1989, 10.79 (8.33–13.26) per 100,000 children/yr; 1990 to 1999, 11.50 (10.04–12.95) per 100,000 children/yr; 2000 to 2012, 19.58 (14.55–24.60) per 100, 000 children/yr; 2000 to 2012 vs. other two groups, p < 0.01; 1965 to 1990 vs. 1990 to 1999, p > 0.05 (Fig. 4).

Figure 4.

Figure 4

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Incidence of childhood type 1 diabetes mellitus among four stages (*revealed 2000 to 2012 vs. other two stages, all p < 0.01, p derived from the one-way ANOVA).

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Discussion

This study performed firstly systematic estimates of CT1DM incidence among various climates, regions, genders, age-groups, latitude, and sunshine durations. The total countries based on this research consisted of 32% of the all countries in the world.

The worldwide incidence of CT1DM was increasing between 1965 and 2012 according to this study. Interestingly, the results of this study suggested there no significant difference was found in CT1DM incidence trended in boys compared with girls in this study. There are consistent results on the difference in incidence of diabetes by gender. Haynes et al. and Stipancic et al.23,24 displayed a significant increase incidence of T1DM in both boys and girls, and no significant difference was found in boys versus girls. However, others found a higher incidence in girls25–27. Adverse to our findings, Casu et al.28 expressed that a higher incidence of T1DM in boys. These divergences might depend on difference in sample size and statistical analysis.

In addition, our study illustrated a significantly increased incidence of T1DM in North America. Most countries in North America are developed countries with a higher per capita GDPs. Muntoni et al.29 showed that countries with a higher per capita GDPs tended to have higher T1DM incidence. Populations in wealthier countries typically drank more milk or eat more cheese than in poorer countries30,31. A high frequency of intake of milk or foods rich in protein may induce the occurrence and development of diabetes in humans10–12,32. Furthermore, these foods and dinks contain higher proportion of carbohydrate. Studies manifested that dietary carbohydrate could exacerbate postprandial glucose responses, which may be play a key role in blood glucose control33,34. Therefore, the higher proportion of carbohydrate may be also a major factor in development of diabetes in these regions.

Furthermore, the incidence of CT1DM of Asia has been increasing in recent years, although lower compared with Europe and America. Especially, the result of this study indicated the CT1DM incidence was higher in inland regions with continental climates compared with monsoon climates in China. The study stated the incidence of Huhehot is about 11 times in Hainan4. The higher incidence existed in inland region with high latitude that plays an important role in reducing childhood insulin-dependent diabetes mellitus (IDDM)35. Recent years, the per capita milk consumption and protein intake are increasing, especially in Xinjiang36 or Nnner Mongolia37. However, the overall incidence is low in China may based on individual’s diet habit and environmental factors38, which may resulted in a lack of public awareness, so could lead to a low quality of life of children in China.

As well, the incidence of CT1DM in regions with higher latitude and lower sunshine durations was higher than low latitude with high sunshine durations. In this study, the average incidence of CT1DM in Finland was 38.11 from 1965 to 1999, in which, latitude was 60°10′ N and the average amount of sunshine durations was only 3.18 hours a day. Eurodiab ACE Study Group39 had reported a 3-fold incidence increase of childhood IDDM was observed with the increasing latitude in Europe, and a similar result was reported within China40. In December, the northern Finland only has 2 hours of sunshine durations every day. Although there exists 23 hours of daylight per day in June, the most of the year exposure to daylight, Vitamin D production in the skin, is low by contrast with southern areas. Vitamin D supplementation is, thus, possibly more significant in this populations than others41. In this research, children lacked of adequate Vitamin D, who lived in higher latitude with low sunshine durations. Vitamin D is an immunosuppressive agent42, and the study believed the adequate Vitamin D supplementation for children might inhibit autoimmune reaction via damaging the β cells of pancreas and reduce the increasing trend in T1DM41. On the contrary, Vitamin D deficiency might induce CT1DM.

Last but not least, the incidence of CT1DM in centers or countries with oceanic climate was higher than other climates. The oceanic climate generally features long, but relatively mild winters and cool and short summers, which have a mean temperature below 22 °C in the warmest month43. In coastal areas of the higher middle latitudes (45–60° latitude), the prevailing onshore flow creates the basic structure of most oceanic climates. The previous studies reported the incidence rates of T1DM were associated with geographic variables such as average annual temperature35. Muntoni et al.29 indicated that countries or centers with lower annual temperatures tended to induce high incidence rate of CT1DM.

Nevertheless, this study just researched the incidence of CT1DM in 0–14 years old. Incidence data in older age groups exist from a few individuals. Furthermore, the incidence of childhood is unavailable after 2012 in this study. As well, the incidence of gender missing from Table 1 revealed the populations where development of the new register strategy was desired. Therefore, the continuous community-based registries are needed to access the T1DM incidence in the world, and further research is needed to find out the primary factor to identify prevention measures to stop the increased incidence of CT1DM.

Conclusions

In this study, the worldwide incidence of CT1DM was increasing, especially in countries with oceanic climates. Compared with previous researches, other than milk consumption, per capita GDPs, and genders, we found the climates included latitude and sunshine durations might play a key role in inducing CT1DM, which affected the lifestyle and dietary habit of individuals.

Acknowledgements

This work was supported by the National Natural Science Foundation of China [grant number 81471054], Guangxi Natural Science Foundation [grant number 2015GXNSFBA139169] and the Innovation Project of Guangxi Graduate Education [grant number JGY2015128].

Author Contributions

Yin-ling Chen collected and analyzed data, wrote the first daft, and created the map. Yong-cheng Huang and Yong-chao Qiao designed the study and directed statistical analyses of the data. Wei Ling, Yan-hong Pan, Li-jun Geng, and Jian-long Xiao analyzed and interpreted the data. Xiao-Xi Zhang and Hai-Lu Zhao designed the study, and revised the submission. All authors contributed to the discussion, and approved the final manuscript.

Competing Interests

The authors declare that they have no competing interests.

Footnotes

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Xiao-xi Zhang, Email: mike_527@163.com.

Hai-lu Zhao, Email: zhaohailu9@126.com.

References

  • 1.Gillespie KM, Bain SC, Barnett AH, et al. The rising incidence of childhood type 1 diabetes and reduced contribution of high-risk HLA haplotypes. Lancet. 2004;364:1699–700. doi: 10.1016/S0140-6736(04)17357-1. [DOI] [PubMed] [Google Scholar]
  • 2.Gale EA. The rise of childhood type 1 diabetes in the 20th century. Diabetes. 2002;51:3353–61. doi: 10.2337/diabetes.51.12.3353. [DOI] [PubMed] [Google Scholar]
  • 3.Agardh CD, Cilio CM, Lethagen A, et al. Clinical evidence for the safety of GAD65 immunomodulation in adult-onset autoimmune diabetes. J. Diabetes Complicat. 2005;19:238–46. doi: 10.1016/j.jdiacomp.2004.12.003. [DOI] [PubMed] [Google Scholar]
  • 4.Karvonen M, et al. Incidence of childhood type 1 diabetes worldwide. Diabetes Mondiale (DiaMond) Project Group. Diabetes care. 2000;23:1516–26. doi: 10.2337/diacare.23.10.1516. [DOI] [PubMed] [Google Scholar]
  • 5.American Diabetes A. Hyperglycemic crises in patients with diabetes mellitus. Diabetes care. 2001;24:1988–96. doi: 10.2337/diacare.24.11.1988. [DOI] [PubMed] [Google Scholar]
  • 6.Gale EA. The discovery of type 1 diabetes. Diabetes. 2001;50:217–26. doi: 10.2337/diabetes.50.2.217. [DOI] [PubMed] [Google Scholar]
  • 7.Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J. Clin. Invest. 2005;115:1111–9. doi: 10.1172/JCI25102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Wills, T. Pharniaceutrie Rationalis or the Exercitation of the Operation of Medicines in Humane Bodies: The Works of Thomas Willis. London: Dring, Harper and Leigh (1679).
  • 9.Bluestone JA, Herold K, Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature. 2010;464:1293–300. doi: 10.1038/nature08933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Virtanen SM, Laara E, Hypponen E, et al. Cow’s milk consumption, HLA-DQB1 genotype, and type 1 diabetes: a nested case-control study of siblings of children with diabetes. Childhood diabetes in Finland study group. Diabetes. 2000;49:912–7. doi: 10.2337/diabetes.49.6.912. [DOI] [PubMed] [Google Scholar]
  • 11.Verge CF, et al. Environmental factors in childhood IDDM. A population-based, case-control study. Diabetes care. 1994;17:1381–9. doi: 10.2337/diacare.17.12.1381. [DOI] [PubMed] [Google Scholar]
  • 12.Dahlquist GG, Blom LG, Persson LA, Sandstrom AI, Wall SG. Dietary factors and the risk of developing insulin dependent diabetes in childhood. BMJ. 1990;300:1302–6. doi: 10.1136/bmj.300.6735.1302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Pundziute-Lycka A, Persson LA, Cedermark G, et al. Diet, growth, and the risk for type 1 diabetes in childhood: a matched case-referent study. Diabetes care. 2004;27:2784–9. doi: 10.2337/diacare.27.12.2784. [DOI] [PubMed] [Google Scholar]
  • 14.West R, et al. Epidemiologic survey of juvenile-onset diabetes in Montreal. Diabetes. 1979;28:690–3. doi: 10.2337/diab.28.7.690. [DOI] [PubMed] [Google Scholar]
  • 15.Cantorna MT. Vitamin D and autoimmunity: is vitamin D status an environmental factor affecting autoimmune disease prevalence? Proc. Soc. Exp. Biol. Med. 2000;223:230–3. doi: 10.1046/j.1525-1373.2000.22333.x. [DOI] [PubMed] [Google Scholar]
  • 16.Ito T, Nakamura K, Umeda E, et al. Familial predisposition of type 1 diabetes mellitus in Japan, a country with low incidence. Japan Diabetes Society Data Committee for ChildhoodDiabetes. JPEM. 2001;14(Suppl 1):589–95. doi: 10.1515/jpem.2001.14.s1.589. [DOI] [PubMed] [Google Scholar]
  • 17.Parslow RC, et al. Incidence of childhood diabetes mellitus in Yorkshire, northern England, is associated with nitrate in drinking water: an ecological analysis. Diabetologia. 1997;40:550–6. doi: 10.1007/s001250050714. [DOI] [PubMed] [Google Scholar]
  • 18.Duthie MS, Kimber I, Norval M. The effects of ultraviolet radiation on the human immune system. Brit. J. Dermatol. 1999;140:995–1009. doi: 10.1046/j.1365-2133.1999.02898.x. [DOI] [PubMed] [Google Scholar]
  • 19.Library of Congress Country Studies. Climate of the countries of the world. https://geographic.org/climate/climate_of_countries.html (2004).
  • 20.Navinfo Data. Tencent-GS. http://www.gpsspg.com/maps.htm (2016).
  • 21.Min, D. H. Sunshine durations in cities around the world. http://www.doc88.com/p-9991671143207.html (2013).
  • 22.The free encyclopedia-Wikipedia. Continental Climate. https://en.wikipedia.org/wiki/Continental_climate (2009).
  • 23.Haynes A, Bower C, Bulsara MK, Jones TW, Davis EA. Continued increase in the incidence of childhood Type 1 diabetes in a population-based Australian sample (1985–2002) Diabetologia. 2004;47:866–70. doi: 10.1007/s00125-004-1385-8. [DOI] [PubMed] [Google Scholar]
  • 24.Stipancic G, et al. Incidence and trends of childhood Type 1 diabetes in Croatia from 1995 to 2003. Diabetes Res. Clin. Pr. 2008;80:122–7. doi: 10.1016/j.diabres.2007.10.019. [DOI] [PubMed] [Google Scholar]
  • 25.Craig ME, Howard NJ, Silink M, Chan A. The rising incidence of childhood type 1 diabetes in New South Wales, Australia. JPEM. 2000;13:363–72. doi: 10.1515/JPEM.2000.13.4.363. [DOI] [PubMed] [Google Scholar]
  • 26.Ionescu-Tirgoviste C, Guja C, Calin A, Mota M. An increasing trend in the incidence of type 1 diabetes mellitus in children aged 0–14 years in Romania–ten years (1988–1997) EURODIAB study experience. JPEM. 2004;17:983–91. doi: 10.1515/JPEM.2004.17.7.983. [DOI] [PubMed] [Google Scholar]
  • 27.Crow YJ, Alberti KG, Parkin JM. Insulin dependent diabetes in childhood and material deprivation in northern England, 1977–86. BMJ. 1991;303:158–60. doi: 10.1136/bmj.303.6795.158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Casu A, Pascutto C, Bernardinelli L, Songini M. Type 1 diabetes among sardinian children is increasing: the Sardinian diabetes register for children aged 0–14 years (1989–1999) Diabetes care. 2004;27:1623–9. doi: 10.2337/diacare.27.7.1623. [DOI] [PubMed] [Google Scholar]
  • 29.Muntoni S, Cocco P, Aru G, Cucca F. Nutritional factors and worldwide incidence of childhood type 1 diabetes. Am. J. Clin. Nutr. 2000;71:1525–9. doi: 10.1093/ajcn/71.6.1525. [DOI] [PubMed] [Google Scholar]
  • 30.Singh GM, Micha R, Khatibzadeh S, et al. Global, Regional, and National Consumption of Sugar-Sweetened Beverages, Fruit Juices, and Milk: A Systematic Assessment of Beverage Intake in 187 Countries. PloS one. 2015;10:e0124845. doi: 10.1371/journal.pone.0124845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Sanchez-Villegas A, Martinez JA, Prattala R, et al. A systematic review of socioeconomic differences in food habits in Europe: consumption of cheese and milk. Eur. J. Clin. Nutr. 2003;57:917–29. doi: 10.1038/sj.ejcn.1601626. [DOI] [PubMed] [Google Scholar]
  • 32.Elliott RB, Martin JM. Dietary protein: a trigger of insulin-dependent diabetes in the BB rat? Diabetologia. 1984;26:297–9. doi: 10.1007/BF00283653. [DOI] [PubMed] [Google Scholar]
  • 33.Accurso A, Bernstein RK, Dahlqvist A, et al. Dietary carbohydrate restriction in type 2 diabetes mellitus and metabolic syndrome: time for a critical appraisal. Nutr. & Metab. 2008;5:9. doi: 10.1186/1743-7075-5-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Sheard NF, Clark NG, Brand-Miller JC, et al. Dietary carbohydrate (amount and type) in the prevention and management of diabetes: a statement by the american diabetes association. Diabetes care. 2004;27:2266–71. doi: 10.2337/diacare.27.9.2266. [DOI] [PubMed] [Google Scholar]
  • 35.Geographic patterns of childhood insulin-dependent diabetes mellitus Diabetes Epidemiology Research International Group. Diabetes. 1988;37:1113–9. doi: 10.2337/diab.37.8.1113. [DOI] [PubMed] [Google Scholar]
  • 36.Zhao GS, Yuan XY, Gong BQ, Wang SZ, Cheng ZH. Nutrition, metabolism, and hypertension. A comparative survey between dietary variables and blood pressure among three nationalities in China. J. Clin. Hypertens. 1986;2:124–31. [PubMed] [Google Scholar]
  • 37.Ohno Y, Hirai K, Sowa S, Oka S, Murai Y. Food and nutrient intakes among nomads living in three different areas of Inner Mongolia, China. Asia Pac. J. Clin. Nutr. 2005;14:7–18. [PubMed] [Google Scholar]
  • 38.Zhao Z, Sun C, Wang C, et al. Rapidly rising incidence of childhood type 1 diabetes in Chinese population: epidemiology in Shanghai during 1997–2011. Acta diabetologica. 2014;51:947–53. doi: 10.1007/s00592-014-0590-2. [DOI] [PubMed] [Google Scholar]
  • 39.Variation and trends in incidence of childhood diabetes in Europe EURODIAB ACE Study Group. Lancet. 2000;355:873–6. doi: 10.1016/S0140-6736(99)07125-1. [DOI] [PubMed] [Google Scholar]
  • 40.Yang Z, Wang K, Li T, et al. Childhood diabetes in China. Enormous variation by place and ethnic group. Diabetes care. 1998;21:525–9. doi: 10.2337/diacare.21.4.525. [DOI] [PubMed] [Google Scholar]
  • 41.Hypponen E, Laara E, Reunanen A, Jarvelin MR, Virtanen SM. Intake of vitamin D and risk of type 1 diabetes: a birth-cohort study. Lancet. 2001;358:1500–3. doi: 10.1016/S0140-6736(01)06580-1. [DOI] [PubMed] [Google Scholar]
  • 42.Lemire J. 1,25-Dihydroxyvitamin D3–a hormone with immunomodulatory properties. Z. Rheumatol. 2000;59(Suppl 1):24–7. doi: 10.1007/s003930070034. [DOI] [PubMed] [Google Scholar]
  • 43.“Whittier, Alaska, United States climate summary”. Weatherbase. Retrieved 9 March (2017).
  • 44.Bessaoud K, et al. Epidemiology of juvenile insulin dependent diabetes mellitus in Algeria (Department of Oran). Rev. Epidem. Sante. Publ. 1990;38:91–99. [PubMed] [Google Scholar]
  • 45.Onkamo P, Vaananen S, Karvonen M, Tuomilehto J. Worldwide increase in incidence of Type I diabetes–the analysis of the data on published incidence trends. Diabetologia. 1999;42:1395–403. doi: 10.1007/s001250051309. [DOI] [PubMed] [Google Scholar]
  • 46.Group DP. Incidence and trends of childhood Type 1 diabetes worldwide 1990–1999. Diabet. Med. 2006;23:857–66. doi: 10.1111/j.1464-5491.2006.01925.x. [DOI] [PubMed] [Google Scholar]
  • 47.Kadiki OA, Moawad SE. Incidence and prevalence of type 1 diabetes in children and adolescents in Benghazi, Libya. Diabet. Med. 1993;10:866–9. doi: 10.1111/j.1464-5491.1993.tb00182.x. [DOI] [PubMed] [Google Scholar]
  • 48.Tuomilehto J, et al. Incidence of IDDM in Mauritian children and adolescents from 1986 to 1990. Diabetes Care. 1993;16:1588–91. doi: 10.2337/diacare.16.12.1588. [DOI] [PubMed] [Google Scholar]
  • 49.Elamin A, Ghalib M, Eltayeb B, Tuvemo T. High incidence of type 1 diabetes mellitus in Sudanese children, 1991–1995. Ann. Saudi. Med. 1997;17:478–80. doi: 10.5144/0256-4947.1997.478. [DOI] [PubMed] [Google Scholar]
  • 50.Elamin A, Omer MI, Zein K, Tuvemo T. Epidemiology of childhood type I diabetes in Sudan, 1987–1990. Diabetes Care. 1992;15:1556–9. doi: 10.2337/diacare.15.11.1556. [DOI] [PubMed] [Google Scholar]
  • 51.Soliman AT, al-Salmi IS, Asfour MG. Epidemiology of childhood insulin-dependent diabetes mellitus in the Sultanate of Oman. Diabet. Med. 1996;13:582–6. doi: 10.1002/(SICI)1096-9136(199606)13:6&#x0003c;582::AID-DIA114&#x0003e;3.0.CO;2-E. [DOI] [PubMed] [Google Scholar]
  • 52.Tuomilehto-Wolf E, Tuomilehto J. HLA antigens in insulin-dependent diabetes mellitus. Ann. Med. 1991;23:481–8. doi: 10.3109/07853899109150507. [DOI] [PubMed] [Google Scholar]
  • 53.Gong C, et al. Trends in childhood type 1 diabetes mellitus incidence in Beijing from 1995 to 2010: a retrospective multicenter study based on hospitalization data. Diabetes Technol. Ther. 2015;17:159–65. doi: 10.1089/dia.2014.0205. [DOI] [PubMed] [Google Scholar]
  • 54.Wong GW, Leung SS, Oppenheimer SJ. Epidemiology of IDDM in southern Chinese children in Hong Kong. Diabetes Care. 1993;16:926–8. doi: 10.2337/diacare.16.6.926. [DOI] [PubMed] [Google Scholar]
  • 55.Huen KF, et al. Epidemiology of diabetes mellitus in children in Hong Kong: the Hong Kong childhood diabetes register. J. Pediatr. Endocrinol. Metab. 2000;13:297–302. doi: 10.1515/JPEM.2000.13.3.297. [DOI] [PubMed] [Google Scholar]
  • 56.Fu H, et al. Shanghai, China, has the lowest confirmed incidence of childhood diabetes in the world. Diabetes Care. 1994;17:1206–8. doi: 10.2337/diacare.17.10.1206. [DOI] [PubMed] [Google Scholar]
  • 57.Shen SX, et al. The incidence of insulin-dependent diabetes mellitus in urban districts of Shanghai (1989–1993) J. Pediatr. Endocrinol. Metab. 1996;9:469–73. doi: 10.1515/jpem.1996.9.4.469. [DOI] [PubMed] [Google Scholar]
  • 58.Kumar KM. Incidence trends for childhood type 1 diabetes in India. Indian J. Endocrinol. Metab. 2015;19:S34–5. doi: 10.4103/2230-8210.155378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Green A, Gale EA, Patterson CC. Incidence of childhood-onset insulin-dependent diabetes mellitus: the EURODIAB ACE Study. Lancet. 1992;339:905–9. doi: 10.1016/0140-6736(92)90938-Y. [DOI] [PubMed] [Google Scholar]
  • 60.Shamis I, Gordon O, Albag Y, Goldsand G, Laron Z. Ethnic differences in the incidence of childhood IDDM in Israel (1965–1993). Marked increase since 1985, especially in Yemenite Jews. Diabetes Care. 1997;20:504–8. doi: 10.2337/diacare.20.4.504. [DOI] [PubMed] [Google Scholar]
  • 61.Kida K, et al. Incidence of Type 1 diabetes mellitus in children aged 0-14 in Japan, 1986–1990, including an analysis for seasonality of onset and month of birth: JDS study. The Data Committee for Childhood Diabetes of the Japan Diabetes Society (JDS) Diabet. Med. 2000;17:59–63. doi: 10.1046/j.1464-5491.2000.00205.x. [DOI] [PubMed] [Google Scholar]
  • 62.Rewers M, LaPorte RE, King H, Tuomilehto J. The Diabetes Epidemiology Research International Study Group—DERI: Trends in the prevalance and incidence of diabetes: insulin-dependent diabetes mellitus in childhood. World Health Stat. 1988;41:179. [PubMed] [Google Scholar]
  • 63.Shaltout AA, et al. High incidence of childhood-onset IDDM in Kuwait. Kuwait Study Group of Diabetes in Childhood. Diabetes Care. 1995;18:923–7. doi: 10.2337/diacare.18.7.923. [DOI] [PubMed] [Google Scholar]
  • 64.Ko KW, Yang SW, Cho NH. The incidence of IDDM in Seoul from 1985 to 1988. Diabetes Care. 1994;17:1473–5. doi: 10.2337/diacare.17.12.1473. [DOI] [PubMed] [Google Scholar]
  • 65.Podar T, Laporte RE, Tuomilehto J, Shubnikov E. Risk of childhood type 1 diabetes for Russians in Estonia and Siberia. Int. J. Epidemiol. 1993;22:262–7. doi: 10.1093/ije/22.2.262. [DOI] [PubMed] [Google Scholar]
  • 66.Kulaylat NA, Narchi H. A twelve year study of the incidence of childhood type 1 diabetes mellitus in the Eastern Province of Saudi Arabia. J. Pediatr. Endocrinol. Metab. 2000;13:135–40. doi: 10.1515/JPEM.2000.13.2.135. [DOI] [PubMed] [Google Scholar]
  • 67.Habeb AM, et al. High incidence of childhood type 1 diabetes in Al-Madinah, North West Saudi Arabia (2004-2009) Pediatr Diabetes. 2011;12:676–81. doi: 10.1111/j.1399-5448.2011.00765.x. [DOI] [PubMed] [Google Scholar]
  • 68.Abduljabbar MA, Aljubeh JM, Amalraj A, Cherian MP. Incidence trends of childhood type 1 diabetes in eastern Saudi Arabia. Saudi. Med. J. 2010;31:413–8. [PubMed] [Google Scholar]
  • 69.Schober E, Rami B, Waldhoer T. Steep increase of incidence of childhood diabetes since 1999 in Austria. Time trend analysis 1979-2005. A nationwide study. Eur. J. Pediatr. 2008;167:293–7. doi: 10.1007/s00431-007-0480-5. [DOI] [PubMed] [Google Scholar]
  • 70.Martinucci ME, et al. Incidence of childhood type 1 diabetes mellitus in Gomel, Belarus. J. Pediatr. Endocrinol. Metab. 2002;15:53–7. doi: 10.1515/JPEM.2002.15.1.53. [DOI] [PubMed] [Google Scholar]
  • 71.Bratina, N. U., Tahirovic, H., Battelino, T. & Krzisnik, C. Incidence of childhood-onset Type I diabetes in Slovenia and the Tuzia region (Bosnia and Herzegovina) in the period 1990–1998. Diabetologia. 44 (Suppl 3) B27–31 (abstract) (2001). [DOI] [PubMed]
  • 72.Atanasova, M. et al. Incidence of diabetes mellitus type 1 in Bulgarian children. Diabetologia. 35 (Suppl 1) A131 (Abstract) (1992).
  • 73.Roglic G, et al. Incidence of IDDM during 1988–1992 in Zagreb, Croatia. Diabetologia. 1995;38:550–4. doi: 10.1007/BF00400723. [DOI] [PubMed] [Google Scholar]
  • 74.Cinek O, et al. Type 1 diabetes mellitus in Czech children diagnosed in 1990–1997: a significant increase in incidence and male predominance in the age group 0–4 years. Collaborators of the Czech Childhood Diabetes Registry. Diabet. Med. 2000;17:64–9. doi: 10.1046/j.1464-5491.2000.00202.x. [DOI] [PubMed] [Google Scholar]
  • 75.Cinek O, Sumnik Z, Vavrinec J. Continuing increase in incidence of childhood-onset type 1 diabetes in the Czech Republic 1990–2001. Eur. J. Pediatr. 2003;162:428–9. doi: 10.1007/s00431-003-1211-1. [DOI] [PubMed] [Google Scholar]
  • 76.Podar, T. et al. Increasing incidence of childhood-onset type I diabetes in 3 Baltic countries and Finland 1983–1998. Diabetologia. 44 (Suppl 3) B17–20 (abstract) (2001). [DOI] [PubMed]
  • 77.Tuomilehto J, et al. Increase in incidence of insulin-dependent diabetes mellitus among children in Finland. Int. J. Epidemiol. 1995;24:984–92. doi: 10.1093/ije/24.5.984. [DOI] [PubMed] [Google Scholar]
  • 78.Karvonen M, et al. Regional differences in the incidence of insulin-dependent diabetes mellitus among children in Finland from 1987 to 1991. Childhood Diabetes in Finland (DiMe) Study Group. Ann. Med. 1997;29:297–304. doi: 10.3109/07853899708999351. [DOI] [PubMed] [Google Scholar]
  • 79.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;52:859–62. doi: 10.1203/00006450-200212000-00008. [DOI] [PubMed] [Google Scholar]
  • 80.Bendas A, et al. Trends in Incidence Rates during 1999–2008 and Prevalence in 2008 of Childhood Type 1 Diabetes Mellitus in Germany–Model-Based National Estimates. PLoS One. 2015;10:e0132716. doi: 10.1371/journal.pone.0132716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Ehehalt S, et al. Baden-Wurttemberg DI-sG. Continuous rise in incidence of childhood Type 1 diabetes in Germany. Diabet. Med. 2008;25:755–7. doi: 10.1111/j.1464-5491.2008.02450.x. [DOI] [PubMed] [Google Scholar]
  • 82.Dacou-Voutetakis C, Karavanaki K, Tsoka-Gennatas H. National data on the epidemiology of IDDM in Greece. Cases diagnosed in 1992. Hellenic Epidemiology Study Group. Diabetes Care. 1995;18:552–4. doi: 10.2337/diacare.18.4.552. [DOI] [PubMed] [Google Scholar]
  • 83.Soltesz G, Madacsy L, Bekefi D, Danko I. Rising incidence of type 1 diabetes in Hungarian children (1978–1987). Hungarian Childhood Diabetes Epidemiology Group. Diabet. Med. 1990;7:111–4. doi: 10.1111/j.1464-5491.1990.tb01343.x. [DOI] [PubMed] [Google Scholar]
  • 84.Bruno G, et al. Age-period-cohort analysis of 1990–2003 incidence time trends of childhood diabetes in Italy: the RIDI study. Diabetes. 2010;59:2281–7. doi: 10.2337/db10-0151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 85.Bruno G, et al. Comparison of incidence of insulin-dependent diabetes mellitus in children and young adults in the Province of Turin, Italy, 1984–91. Piedmont Study Group for Diabetes Epidemiology. Diabet. Med. 1997;14:964–9. doi: 10.1002/(SICI)1096-9136(199711)14:11&#x0003c;964::AID-DIA493&#x0003e;3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  • 86.Sebastiani L, et al. A 5-year (1989–1993) prospective study of the incidence of IDDM in Rome and the Lazio region in the age-group 0–14 years. Diabetes Care. 1996;19:70–3. doi: 10.2337/diacare.19.1.70. [DOI] [PubMed] [Google Scholar]
  • 87.Cotellessa M, et al. High incidence of childhood type 1 diabetes in Liguria, Italy, from 1989 to 1998. Diabetes Care. 2003;26:1786–9. doi: 10.2337/diacare.26.6.1786. [DOI] [PubMed] [Google Scholar]
  • 88.Helgason T, Danielsen R, Thorsson AV. Incidence and prevalence of type 1 (insulin-dependent) diabetes mellitus in Icelandic children 1970-1989. Diabetologia. 1992;35:880–3. doi: 10.1007/BF00399936. [DOI] [PubMed] [Google Scholar]
  • 89.Pundziute-Lycka A, Dahlquist G, Urbonaite B, Zalinkevicius R. Swedish Childhood Diabetes Study G, Lithuanian Childhood Diabetes Study G. Time trend of childhood type 1 diabetes incidence in Lithuania and Sweden, 1983–2000. Acta. Paediatr. 2004;93:1519–24. doi: 10.1111/j.1651-2227.2004.tb02640.x. [DOI] [PubMed] [Google Scholar]
  • 90.Karvonen M, Tuomilehto J, Libman I, LaPorte R. A review of the recent epidemiological data on the worldwide incidence of type 1 (insulin-dependent) diabetes mellitus. World Health Organization DIAMOND Project Group. Diabetologia. 1993;36:883–92. doi: 10.1007/BF02374468. [DOI] [PubMed] [Google Scholar]
  • 91.Schranz AG, Prikatsky V. Type 1 diabetes in the Maltese Islands. Diabet. Med. 1989;6:228–31. doi: 10.1111/j.1464-5491.1989.tb01152.x. [DOI] [PubMed] [Google Scholar]
  • 92.Formosa N, Calleja N, Torpiano J. Incidence and modes of presentation of childhood type 1 diabetes mellitus in Malta between 2006 and 2010. Pediatr. Diabetes. 2012;13:484–8. doi: 10.1111/j.1399-5448.2011.00839.x. [DOI] [PubMed] [Google Scholar]
  • 93.Samardzic M, Marinkovic J, Kocev N, Curovic N, Terzic N. Increasing incidence of childhood type 1 diabetes in Montenegro from 1997 to 2006. Pediatr. Diabetes. 2010;11:412–6. doi: 10.1111/j.1399-5448.2009.00617.x. [DOI] [PubMed] [Google Scholar]
  • 94.Joner G, Sovik O. Increasing incidence of diabetes mellitus in Norwegian children 0–14 years of age 1973–1982. Diabetologia. 1989;32:79–83. doi: 10.1007/BF00505178. [DOI] [PubMed] [Google Scholar]
  • 95.Skrivarhaug T, Stene LC, Drivvoll AK, Strom H, Joner G. Incidence of type 1 diabetes in Norway among children aged 0–14 years between 1989 and 2012: has the incidence stopped rising? Results from the Norwegian Childhood Diabetes Registry. Diabetologia. 2014;57:57–62. doi: 10.1007/s00125-013-3090-y. [DOI] [PubMed] [Google Scholar]
  • 96.Jarosz-Chobot P, Deja G, Polanska J. Epidemiology of type 1 diabetes among Silesian children aged 0–14 years, 1989–2005. Acta. Diabetol. 2010;47:29–33. doi: 10.1007/s00592-009-0094-7. [DOI] [PubMed] [Google Scholar]
  • 97.Michalkova D, Minarik P, Hlava P, Camajova J, Nazarov V. Trends in the incidence of childhood-onset type 1 diabetes in Slovakia 1985–2000. Cent. Eur. J. Public Health. 2004;12:75–7. [PubMed] [Google Scholar]
  • 98.Fernandez-Ramos C, Arana-Arri E, Jimenez-Huertas P, Vela A, Rica I. Incidence of childhood-onset type 1 diabetes in Biscay, Spain, 1990–2013. Pediatr. Diabetes. 2017;18:71–6. doi: 10.1111/pedi.12354. [DOI] [PubMed] [Google Scholar]
  • 99.Gimeno Benitez A, Luengo Perez LM, Suero Villa P, Suero Villa S, Sanchez Vega J. [Incidence of childhood type I diabetes in Extremadura, Spain, 2003–2007] Semergen. 2014;40:177–82. doi: 10.1016/j.semerg.2013.10.005. [DOI] [PubMed] [Google Scholar]
  • 100.Serrano Rios M, et al. Incidence of type 1 (insulin-dependent) diabetes mellitus in subjects 0–14 years of age in the Comunidad of Madrid, Spain. Diabetologia. 1990;33:422–4. doi: 10.1007/BF00404093. [DOI] [PubMed] [Google Scholar]
  • 101.Nystrom L, Dahlquist G, Rewers M, Wall S. The Swedish childhood diabetes study. An analysis of the temporal variation in diabetes incidence 1978–1987. Int. J. Epidemiol. 1990;19:141–6. doi: 10.1093/ije/19.1.141. [DOI] [PubMed] [Google Scholar]
  • 102.Berhan Y, Waernbaum I, Lind T, Mollsten A, Dahlquist G. Swedish Childhood Diabetes Study G. Thirty years of prospective nationwide incidence of childhood type 1 diabetes: the accelerating increase by time tends to level off in Sweden. Diabetes. 2011;60:577–81. doi: 10.2337/db10-0813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 103.Vlajinac HD, et al. Insulin dependent diabetes mellitus: incidence in childhood in Belgrade 1982–92. J. Epidemiol. Community Health. 1995;49:107–8. doi: 10.1136/jech.49.1.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 104.Sipetic S, et al. Rising incidence of type 1 diabetes in Belgrade children aged 0–14 years in the period from 1982 to 2005. J. Endocrinol. Invest. 2013;36:307–12. doi: 10.3275/8619. [DOI] [PubMed] [Google Scholar]
  • 105.Demirbilek H, Ozbek MN, Baran RT. Incidence of type 1 diabetes mellitus in Turkish children from the southeastern region of the country: a regional report. J. Clin. Res. Pediatr. Endocrinol. 2013;5:98–103. doi: 10.4274/Jcrpe.954. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 106.Burden AC, Hearnshaw JR, Swift PG. Childhood diabetes mellitus: an increasing incidence. Diabet. Med. 1989;6:334–6. doi: 10.1111/j.1464-5491.1989.tb01175.x. [DOI] [PubMed] [Google Scholar]
  • 107.Gardner SG, Bingley PJ, Sawtell PA, Weeks S, Gale EA. Rising incidence of insulin dependent diabetes in children aged under 5 years in the Oxford region: time trend analysis. The Bart’s-Oxford Study Group. BMJ. 1997;315:713–7. doi: 10.1136/bmj.315.7110.713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 108.Harron KL, et al. Incidence rate trends in childhood type 1 diabetes in Yorkshire, UK 1978–2007: effects of deprivation and age at diagnosis in the South Asian and non-South Asian populations. Diabet. Med. 2011;28:1508–13. doi: 10.1111/j.1464-5491.2011.03413.x. [DOI] [PubMed] [Google Scholar]
  • 109.Feltbower RG, et al. Trends in the incidence of childhood diabetes in south Asians and other children in Bradford, UK. Diabet. Med. 2002;19:162–6. doi: 10.1046/j.1464-5491.2002.00691.x. [DOI] [PubMed] [Google Scholar]
  • 110.Zhao HX, et al. Incidence of childhood-onset Type 1 diabetes mellitus in Devon and Cornwall, England, 1975–1996. Diabet. Med. 1999;16:1030–5. doi: 10.1046/j.1464-5491.1999.00175.x. [DOI] [PubMed] [Google Scholar]
  • 111.Alaghehbandan R, Collins KD, Newhook LA, MacDonald D. Childhood type 1 diabetes mellitus in Newfoundland and Labrador, Canada. Diabetes Res. Clin. Pract. 2006;74:82–9. doi: 10.1016/j.diabres.2006.03.001. [DOI] [PubMed] [Google Scholar]
  • 112.Newhook LA, et al. High incidence of childhood type 1 diabetes in the Avalon Peninsula, Newfoundland, Canada. Diabetes Care. 2004;27:885–8. doi: 10.2337/diacare.27.4.885. [DOI] [PubMed] [Google Scholar]
  • 113.Amos, A. F., McCarty, D. J. & Zimmet, P. The rising global burden of diabetes and its complications: estimates and projections to the year 2010. Diabet. Med. 14(Suppl 5) S1–85 (abstract) (1997). [PubMed]
  • 114.Smith TL, Drum ML, Lipton RB. Incidence of childhood type I and non-type 1 diabetes mellitus in a diverse population: the Chicago Childhood Diabetes Registry, 1994 to 2003. J. Pediatr. Endocrinol. Metab. 2007;20:1093–107. doi: 10.1515/JPEM.2007.20.10.1093. [DOI] [PubMed] [Google Scholar]
  • 115.Kostraba JN, et al. Incidence of insulin-dependent diabetes mellitus in Colorado. Epidemiology. 1992;3:232–8. doi: 10.1097/00001648-199205000-00008. [DOI] [PubMed] [Google Scholar]
  • 116.Karvonen M, et al. Diabetes Metab. Rev. 1997. Sex difference in the incidence of insulin-dependent diabetes mellitus: an analysis of the recent epidemiological data. World Health Organization DIAMOND Project Group; pp. 275–91. [DOI] [PubMed] [Google Scholar]
  • 117.Lipman TH. The epidemiology of type I diabetes in children 0–14 yr of age in Philadelphia. Diabetes Care. 1993;16:922–5. doi: 10.2337/diacare.16.6.922. [DOI] [PubMed] [Google Scholar]
  • 118.Sereday MS, Marti ML, Damiano MM, Moser ME. Establishment of a registry and incidence of IDDM in Avellaneda, Argentina. Diabetes Care. 1994;17:1022–5. doi: 10.2337/diacare.17.9.1022. [DOI] [PubMed] [Google Scholar]
  • 119.Ferreira SR, et al. Population-based incidence of IDDM in the state of Sao Paulo, Brazil. Diabetes Care. 1993;16:701–4. doi: 10.2337/diacare.16.5.701. [DOI] [PubMed] [Google Scholar]
  • 120.Carrasco, E., Lopez Garcia de los Rios, M., an Vargas, N. Incidencia de diabetes mellitus insulinodependiente en menores de 15 anos.periodo 90–91. Santiago, Chile. Rev. Soc. Argent. Diabetes. 26 (Suppl) 14–15 (abstract) (1992).
  • 121.Tull ES, et al. Incidence of childhood-onset IDDM in black African-heritage populations in the Caribbean. The Caribbean African Heritage IDDM Study (CAHIS) Group. Diabetes Care. 1997;20:309–10. doi: 10.2337/diacare.20.3.309. [DOI] [PubMed] [Google Scholar]
  • 122.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;17:428–31. doi: 10.2337/diacare.17.5.428. [DOI] [PubMed] [Google Scholar]
  • 123.Frazer de Llado TE, Gonzalez de Pijem L, Hawk B. Incidence of IDDM in children living in Puerto Rico. Puerto Rican IDDM Coalition. Diabetes Care. 1998;21:744–6. doi: 10.2337/diacare.21.5.744. [DOI] [PubMed] [Google Scholar]
  • 124.Haynes A, Bulsara MK, Bower C, Jones TW, Davis EA. Regular peaks and troughs in the Australian incidence of childhood type 1 diabetes mellitus (2000–2011) Diabetologia. 2015;58:2513–6. doi: 10.1007/s00125-015-3709-2. [DOI] [PubMed] [Google Scholar]
  • 125.Haynes A, Bulsara MK, Bower C, Jones TW, Davis EA. Cyclical variation in the incidence of childhood type 1 diabetes in Western Australia (1985–2010) Diabetes Care. 2012;35:2300–2. doi: 10.2337/dc12-0205. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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