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Original Article

Maternal Age at Birth and Childhood Type 1 Diabetes: A Pooled Analysis of 30 Observational Studies

  1. Chris R. Cardwell1,
  2. Lars C. Stene2,3,
  3. Geir Joner4,
  4. Max K. Bulsara5,
  5. Ondrej Cinek6,
  6. Joachim Rosenbauer7,
  7. Johnny Ludvigsson8,
  8. Mireia Jané9,
  9. Jannet Svensson10,
  10. Michael J. Goldacre11,
  11. Thomas Waldhoer12,
  12. Przemysława Jarosz-Chobot13,
  13. Suely G.A. Gimeno14,
  14. Lee-Ming Chuang15,
  15. Roger C. Parslow16,
  16. Emma J.K. Wadsworth17,
  17. Amanda Chetwynd18,
  18. Paolo Pozzilli19,
  19. Girts Brigis20,
  20. Brone Urbonaitė21,
  21. Sandra Šipetić22,
  22. Edith Schober23,
  23. Gabriele Devoti24,
  24. Constantin Ionescu-Tirgoviste25,
  25. Carine E. de Beaufort26,
  26. Denka Stoyanov27,
  27. Karsten Buschard28 and
  28. Chris C. Patterson1
  1. 1Centre for Public Health, Queen's University Belfast, Belfast, U.K.;
  2. 2Division of Epidemiology, Norwegian Institute of Public Health, Oslo, Norway;
  3. 3Oslo Research Centre, Oslo University Hospital, Oslo, Norway;
  4. 4Institute of Health Management and Health Economics, University of Oslo, Oslo, Norway;
  5. 5Institute of Health and Rehabilitation Research, University of Notre Dame, Freemantle, Australia;
  6. 6The 2nd Medical School, Charles University, Prague, Czech Republic;
  7. 7Institute of Biometrics and Epidemiology, German Diabetes Centre, Leibniz Institute at Dusseldorf University, Dusseldorf, Germany;
  8. 8Department of Paediatrics and Diabetes Research Centre, Linkoping University, Linkoping, Sweden;
  9. 9Public Health Division, Department of Health, Barcelona, Spain;
  10. 10Pediatric Department, Glostrup University Hospital, Glostrup, Denmark;
  11. 11Department of Public Health, Oxford University, Oxford, U.K.;
  12. 12Department of Epidemiology, Medical University of Vienna, Vienna, Austria;
  13. 13Department of Pediatric Endocrinology and Diabetes, Medical University of Silesia, Katowice, Poland;
  14. 14Preventive Medicine Department, Federal University of Sao Paulo, Sao Paulo, Brazil;
  15. 15Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan;
  16. 16Paediatric Epidemiology Group, University of Leeds, Leeds, U.K.;
  17. 17Centre for Occupational and Health Psychology, Cardiff University, Cardiff, U.K.;
  18. 18Mathematics & Statistics Department, Lancaster University, Lancaster, U.K.;
  19. 19University Campus Bio-Medico, Rome, Italy;
  20. 20Department of Public Health and Epidemiology, Riga Stradins University, Riga, Latvia;
  21. 21Institute of Endocrinology, Kaunas University of Medicine, Kaunas, Lithuania;
  22. 22Institute of Epidemiology, School of Medicine, Belgrade University, Belgrade, Serbia;
  23. 23Department of Paediatrics, Medical University of Vienna, Vienna, Austria;
  24. 24Department of Social Sciences and Communication, University of Lecce, Lecce, Italy;
  25. 25Nutrition and Metabolic Diseases Clinic, “N. Paulescu” Institute of Diabetes, Bucharest, Romania;
  26. 26Clinique Pediatrique, Luxembourg, Luxembourg;
  27. 27Children's Diabetic Centre, Sofia, Bulgaria;
  28. 28Bartholin Instituttet, Rigshospitalet, Copenhagen, Denmark.
  1. Corresponding author: Chris Cardwell, c.cardwell{at}qub.ac.uk.
Diabetes 2010 Feb; 59(2): 486-494. https://doi.org/10.2337/db09-1166
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  • FIG. 1.
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    FIG. 1.

    Meta-analysis of the unadjusted association between maternal age (per 5-year increase) and type 1 diabetes (including 14,724 case subjects) using the random effects model; studies are ordered by publication date.

  • FIG. 2.
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    FIG. 2.

    Scatter plot of odds ratio for diabetes per 5-year increase in maternal age by difference in response rates between case and control subjects (size of plotting symbol was proportional to precision of study; line was taken from meta-regression).

Tables

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  • TABLE 1

    Characteristics of included studies investigating the association between maternal age and type 1 diabetes, ordered by publication date

    First author, year* (reference)DesignCountryType 1 diabetic subjectsControl subjectsAvailable confounders‡
    Ascertainment method (year case subjects diagnosed)Age at dx (years)n†Resp rate (%)Source (matching criteria)n†Resp rate (%)BOBWGAMDCSBF# (months)
    Dahlquist, 1992 (9)C-CSwedenSwedish childhood diabetes register (78–88)0–142,75798Medical birth registry (birth year, unit)8,271100
    Bock, 1994 (10)C-CDenmarkHosp. admission from National Patient Registry (78–89)<1683798Birth registry (age, sex)837NA
    Patterson, 1994 (11)C-CScotlandHosp. admission/childhood diabetes register (76–88)0–14271100Maternal discharge records (age, sex, area)1,340100✓✓✓✓✓✓(any)
    Wadsworth, 1997 (25)C-CU.K.British Paediatric Association Surveillance Unit (92)0–521389Health Authority Immunization Register31870✓✓✓✓(4)
    Gimeno, 1997 (26)C-CBrazilDiabetes association/ Hospital admission (95)0–1934491Unclear (neighborhood, sex, age)‖333100✓✓✓✓(3)
    McKinney, 1999 (28)C-CEnglandYorkshire Childhood Diabetes Register (93–94)0–1522094General practitioner's records (age, sex)42382✓✓✓✓✓✓(any)
    Rami, 1999 (29)C-CAustriaVienna type 1 diabetes register (89–94)0–1410386Schools (age, sex)37380✓✓✓✓§✓✓(any)
    Bache, 1999 (19)**C-CDenmarkHospital admission (78–95)0–14857100Medical birth registry (month, sex, district)1,404100✓
    Dahlquist, 1999 (14)C-CBulgariaW. Bulgaria type 1 diabetes register (91–94)0–1412573Schools and policlinics (age)44079✓✓✓✓§✓✓(any)
    C-CLatviaLatvian type 1 diabetes register (89–94)0–1414099Population register (age)30179✓✓✓✓§✓✓(any)
    C-CLithuaniaLithuanian type 1 diabetes register (89–94)0–1411794Policlinics (age)26673✓✓✓✓§✓✓(any)
    C-CLuxembourgLuxembourg type 1 diabetes register (89–95)0–1459100Preschools and schools (age)17295✓✓✓✓§✓✓(any)
    C-CRomaniaBucharest type 1 diabetes register (89–94)0–148174Preschools and schools (age)27781✓✓✓✓§✓✓(any)
    Stene, 2001 (13)CohortNorwayNorwegian Childhood Diabetes Registry (89–98)0–141,810100¶Norwegian medical birth registry1,382,602NA✓✓✓✓✓
    Visalli, 2003 (30)C-CItalyLazio type 1 diabetes register (89–95)0–14139100Schools (age)70391✓✓✓✓✓(3)
    Stene, 2004 (31)C-CNorwayNorwegian Childhood Diabetes Registry (98–00)0–1434673Norwegian population registry1,62656✓✓✓✓§✓✓(3)
    Sadauskaite-Kuehne, 2004 (15)C-CSwedenSE Sweden type 1 diabetes register (95–00)0–15442100Population register1,08473✓✓✓✓§✓(3)
    C-CLithuaniaLithuanian type 1 diabetes register (96–00)0–15281100Outpatient clinic‖80795✓✓✓✓§✓(3)
    Sumnik, 2004 (32)C-CCzech RepublicCzech Republic type 1 diabetes registry (95–00)0–1564079National Birth registry (age)32,000100✓
    Marshall, 2004 (33)C-CEnglandMorecambe Bay/E. Lancashire diabetes clinics (98)0–1519683Health Authorities (sex, birth date)38153✓✓✓✓§✓(any)
    Cardwell, 2005 (34)CohortN. IrelandN. Ireland type 1 diabetes register (71–01)0–1499092¶Northern Ireland Child Health register439,647NA✓✓✓✓✓✓(any)
    Sipetić, 2005 (35)C-CSerbiaBelgrade Hospital admission (94–97)0–1610591Hospital outpatients with skin disease‖ (age, sex, area)210100✓✓✓✓§✓✓(4)
    Svensson, 2005 (36)C-CDenmarkDanish register of childhood diabetes (96–99)0–14602100Danish population register (age, sex)1,459100✓✓✓✓✓✓(4)
    Bottini, 2005 (20)**C-CSardiniaHospital diagnosis?189?Consecutive births in northern Sardinia5,460?
    Polańka, 2006 (37)C-CPolandUpper Silesia Diabetes Register (89–96)0–1439487Central Bureau for Statistics994,460100✓✓
    Wei, 2006 (38)C-CTaiwanSchool-based urine screening program & questionnaire (92–97)0–1826087Randomly selected negatives from screening program53388✓✓✓✓✓(3)
    Tenconi, 2007 (39)C-CItalyPavia type 1 diabetes register (88–00)0–199985Hospital (age, sex, week)194?✓
    Haynes, 2007 (40)CohortAustraliaW. Australian Children's Diabetes Register (80–02)0–1492699¶W. Australia Midwives' Notification System∼557,707NA✓✓✓✓
    Ievins, 2007 (41)CohortEnglandHosp. admission [ICD diabetes code] (63–99)0–14410—Oxfordshire/W. Berkshire maternity records266,665NA✓✓✓✓✓✓(any)
    Borras Perez, 2007 (42)C-CSpainCatalonia type 1 diabetes register (97–08)0–1462672Catalonia Public Health Birth Register3,32098✓✓✓(any)
    Rosenbauer, 2008 (12)C-CGermanyNationwide hosp. based surveillance (92–95)0–474771Local registration offices (age, sex, area)1,82043✓✓✓§✓(4)
    Waldhoer, 2008 (43)CohortAustriaAustrian diabetes register (89–05)0–544485¶Birth certificate registry1,435,385NA✓✓✓
    • *Year of publication.

    • †Number included in analysis of maternal age.

    • ‡Tick denotes data recorded in study and available for analysis.

    • §Maternal type 1 diabetes used in analyses.

    • ‖Not randomly selected and population based.

    • ¶Percentage of case subjects identified in cohort.

    • #Duration of breast-feeding used in adjusted analysis shown in brackets.

    • **Only included in sensitivity analyses. dx, diagnosis; Resp, response; BF, breast-feeding (in months); BO, birth order; BW, birth weight; C-C, case-control; CS, cesarean section; GA, gestational age; Hosp., hospital; MD, maternal diabetes; NA, not applicable.

  • TABLE 2

    Meta-analyses of 30 studies investigating the association between maternal age and type 1 diabetes before and after adjustments for recorded confounders and in subgroups defined by study type and quality

    Maternal age (years)Case subjects (n)Combined OR (95% CI)PHeterogeneity
    χ2 (P)I2
    Overall (n = 30 studies)
        <207640.88 (0.74−1.04)0.1281.4 (<0.001)64
        20–253,9190.95 (0.89−1.00)0.0536.1 (0.17)20
        25–305,4331.00 (ref.)
        30–353,2741.05 (0.97−1.13)0.2859.1 (0.001)51
        ≥351,3341.10 (1.01−1.20)0.0336.4 (0.16)20
        Per 5-year increase14,7241.05 (1.02−1.09)0.00697.7 (<0.001)70
    Adjusted for gestational age, birth weight, and birth order*(n = 20 studies)
        <204030.95 (0.77−1.17)0.6542.7 (0.001)56
        20–251,8460.90 (0.84−0.97)0.00320.9 (0.34)9
        25–302,8261.00 (ref.)
        30–351,7091.05 (0.93−1.19)0.4046.4 (<0.001)59
        ≥357371.12 (0.97−1.29)0.1433.0 (0.024)42
        Per 5-year increase7,5211.06 (1.00−1.12)0.0566.5 (<0.001)71
    Adjusted for all available confounders as shown in Table 1 (n = 30 studies)
        <207360.89 (0.74−1.07)0.2288.9 (<0.001)67
        20–253,7150.93 (0.87−0.99)0.0236.2 (0.17)20
        25–305,1471.00 (ref.)
        30–353,1051.08 (0.99−1.18)0.1062.4 (<0.001)54
        ≥351,2511.12 (1.02−1.24)0.0239.9 (0.09)27
        Per 5-year increase13,9541.06 (1.01−1.11)0.01116.9 (<0.001)75
    Cohort studies (n = 5 studies)
        <202690.80 (0.65−0.99)0.049.3 (0.06)57
        20–251,1050.89 (0.82−0.96)0.0033.8 (0.43)0
        25–301,6811.00 (ref.)
        30–351,0570.99 (0.88−1.12)0.938.7 (0.07)54
        ≥354681.08 (0.96−1.22)0.215.2 (0.26)23
        Per 5-year increase4,5801.06 (1.01−1.11)0.0312.7 (0.01)69
    Case-control studies (n = 25 studies)
        <204950.91 (0.73−1.14)0.4171.5 (<0.001)66
        20–252,8140.97 (0.91−1.05)0.4728.9 (0.22)17
        25–303,7521.00 (ref.)
        30–352,2171.07 (0.97−1.19)0.2049.6 (0.002)52
        ≥358661.12 (0.99−1.25)0.0730.9 (0.16)22
        Per 5-year increase10,1441.05 (1.00−1.11)0.0484.6 (<0.001)72
    Studies with a low risk of bias† (n = 14 studies)
        <205180.81 (0.70−0.94)0.00520.8 (0.08)38
        20–252,5470.90 (0.86−0.96)<0.0019.3 (0.75)0
        25–303,6481.00 (ref.)
        30–352,1951.08 (0.99−1.18)0.1023.8 (0.03)45
        ≥359041.18 (1.06−1.32)0.00318.3 (0.14)29
        Per 5-year increase9,8121.10 (1.06−1.14)<0.00127.6 (0.01)53
    • *Includes only studies for which adjustments for birth weight (in categories <2.5, 2.5−3, 3−3.5, 2−4.5, >4.5 kg), gestational age (in categories ≤ 37, 38−41, ≥42 weeks), and birth order (in categories first, second, or third born or later) could be made.

    • †Excluding case-control studies that have control subjects who were not randomly selected (or population based) or studies in which the response rate in either the case or control subjects was less than 80% (or unknown) as shown in Table 1.

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Maternal Age at Birth and Childhood Type 1 Diabetes: A Pooled Analysis of 30 Observational Studies
Chris R. Cardwell, Lars C. Stene, Geir Joner, Max K. Bulsara, Ondrej Cinek, Joachim Rosenbauer, Johnny Ludvigsson, Mireia Jané, Jannet Svensson, Michael J. Goldacre, Thomas Waldhoer, Przemysława Jarosz-Chobot, Suely G.A. Gimeno, Lee-Ming Chuang, Roger C. Parslow, Emma J.K. Wadsworth, Amanda Chetwynd, Paolo Pozzilli, Girts Brigis, Brone Urbonaitė, Sandra Šipetić, Edith Schober, Gabriele Devoti, Constantin Ionescu-Tirgoviste, Carine E. de Beaufort, Denka Stoyanov, Karsten Buschard, Chris C. Patterson
Diabetes Feb 2010, 59 (2) 486-494; DOI: 10.2337/db09-1166

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Maternal Age at Birth and Childhood Type 1 Diabetes: A Pooled Analysis of 30 Observational Studies
Chris R. Cardwell, Lars C. Stene, Geir Joner, Max K. Bulsara, Ondrej Cinek, Joachim Rosenbauer, Johnny Ludvigsson, Mireia Jané, Jannet Svensson, Michael J. Goldacre, Thomas Waldhoer, Przemysława Jarosz-Chobot, Suely G.A. Gimeno, Lee-Ming Chuang, Roger C. Parslow, Emma J.K. Wadsworth, Amanda Chetwynd, Paolo Pozzilli, Girts Brigis, Brone Urbonaitė, Sandra Šipetić, Edith Schober, Gabriele Devoti, Constantin Ionescu-Tirgoviste, Carine E. de Beaufort, Denka Stoyanov, Karsten Buschard, Chris C. Patterson
Diabetes Feb 2010, 59 (2) 486-494; DOI: 10.2337/db09-1166
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