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Epidemiology/Health Services Research

Early Infant Diet and Islet Autoimmunity in the TEDDY Study

  1. Ulla Uusitalo1⇑,
  2. Hye-Seung Lee1,
  3. Carin Andrén Aronsson2,
  4. Kendra Vehik1,
  5. Jimin Yang1,
  6. Sandra Hummel3,
  7. Katherine Silvis4,
  8. Åke Lernmark2,
  9. Marian Rewers5,
  10. William Hagopian6,
  11. Jin-Xiong She4,
  12. Olli Simell7,
  13. Jorma Toppari8,
  14. Anette-G. Ziegler3,
  15. Beena Akolkar9,
  16. Jeffrey Krischer1,
  17. Suvi M. Virtanen10,11,12,
  18. Jill M. Norris13, and
  19. the TEDDY Study Group*
  1. Corresponding author: Ulla Uusitalo, ulla.uusitalo{at}epi.usf.edu.
    1. 1Health Informatics Institute, Department of Pediatrics, Morsani College of Medicine, University of South Florida, Tampa, FL
    2. 2Department of Clinical Sciences, Lund University, Malmö, Sweden
    3. 3Institute of Diabetes Research, Helmholtz Zentrum München and Forschergruppe Diabetes, Klinikum rechts der Isar, Technische Universität München and Forschergruppe Diabetes e.V., Munich, Germany
    4. 4Medical College of Georgia, Augusta University, Augusta, GA
    5. 5Barbara Davis Center for Childhood Diabetes, University of Colorado School of Medicine, Aurora, CO
    6. 6Pacific Northwest Diabetes Research Institute, Seattle, WA
    7. 7Department of Pediatrics, University of Turku, Turku, Finland
    8. 8Department of Physiology, Institute of Biomedicine, University of Turku; Department of Pediatrics, Turku University Hospital, Turku, Finland
    9. 9National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD
    10. 10Nutrition Unit, National Institute for Health and Welfare, Helsinki, Finland
    11. 11Faculty of Social Sciences and Center for Child Health Research, University of Tampere and Tampere University Hospital, Tampere, Finland
    12. 12The Science Center of Pirkanmaa Hospital District, Tampere, Finland
    13. 13Department of Epidemiology, Colorado School of Public Health, University of Colorado Denver, Aurora, CO
    Diabetes Care 2018 Mar; 41(3): 522-530. https://doi.org/10.2337/dc17-1983
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    Article Figures & Tables

    Tables

    • Table 1

      Description of foods and food groups studied in relation to the risk of IA

      Dietary Exposures
      Breastfeeding and food exposures that were each studied separatelySelected foods: foods associated with IA in previous studies; they were studied as one combined variableAny solid food: all solid foods that were studied as one combined variable
      Exclusive breastfeeding
      Any breastfeeding
      Infant formula
      Cow’s milk (any cow’s milk exposure)
      All cerealsAll cerealsAll cereals
      Gluten-containing cerealsGluten-containing cerealsGluten-containing cereals
      RiceRiceRice
      Fruits and berriesFruits and berriesFruits and berries
      PotatoesPotatoesPotatoes
      Root vegetablesRoot vegetablesRoot vegetables
      Meat (beef, pork, poultry, game)Meat (beef, pork, poultry, game)
      Fish and seafoodFish and seafood
      EggEggEgg
      Milk products (yogurt, sour cream, cheese, commercial baby foods containing yogurt, cottage cheese)
      Spinach
      Peas, green beans
      Cabbages (Chinese cabbage, red cabbage, cauliflower, broccoli, kale, cabbage turnip, collard, mustard green, turnip greens)
      Squash, pumpkin
      Tomato, tomato sauce
      Corn
      Other vegetable
      Sausage, hot dogs
      • Variables studied are shown in bold.

    • Table 2

      Characteristics associated with any IA

      Study population,Any IA (N = 703)IAA (N = 272)GADA (N = 299)
      NN (%)HR (95% CI)P valueN (%)HR (95% CI)P valueN (%)HR (95% CI)P value
      Country
       Finland1,654180 (25.6)1.40 (1.15, 1.71)<0.00189 (32.7)2.28 (1.67, 3.11)<0.001110 (36.8)1.00 (0.72, 1.39)0.999
       Germany51054 (7.7)1.30 (0.96, 1.76)0.09220 (7.4)1.36 (0.82, 2.25)0.23460 (20.1)0.82 (0.47, 1.42)0.471
       Sweden2,283240 (34.1)1.30 (1.08, 1.56)0.00583 (30.5)1.38 (1.02, 1.89)0.03915 (5.0)1.25 (0.96, 1.62)0.103
       U.S.3,116229 (32.6)180 (29.4)1114 (38.1)1
      High-risk HLA genotype (DR3/4)
       Yes2,956344 (48.9)1.61 (1.38, 1.88)<0.001128 (47.1)1.54 (1.21, 1.96)<0.001150 (50.2)1.65 (1.31, 2.07)<0.001
       No4,607359 (51.1)1144 (52.9)1149 (49.8)1
      FDR with T1D
       Yes857136 (19.4)1.99 (1.64, 2.43)<0.00158 (21.3)2.32 (1.71, 3.15)<0.00152 (17.4)1.85 (1.36, 2.53)<0.001
       No6,706567 (80.6)1214 (78.7)1247 (82.6)1
      Sex of the child
       Female3,698322 (45.8)0.87 (0.75, 1.00)0.056152 (44.1)0.81 (0.64, 1.03)0.079144 (48.2)0.95 (0.76, 1.19)0.661
       Male3,865381 (54.2)1120 (55.9)1155 (51.8)1
      Probiotics, age at first exposure
       <28 days53841 (5.8)0.70 (0.50, 0.97)0.02215 (5.5)0.53 (0.31, 0.91)0.02115 (5.0)0.72 (0.42, 1.24)0.237
       ≥28 days7,025662 (94.2)1257 (94.5)1284 (95.0)1
    • Table 3

      Association of timing of dietary exposures with the risk of IA (any IA, IAA, or GADA)

      Dietary exposureIADuration of breastfeeding or age at introduction of food (months)HR (95% CI)*P value*
      Among those who developed autoantibodiesAmong those who did not develop autoantibodies
      NNot breastfed or food was not introduced by the end of follow-up (%)Mean (SD)NNot breastfed or food was not introduced by the end of follow-up (%)Mean (SD)
      Exclusive breastfeedingAny IA70301.3 (1.9)6,86001.2 (1.8)1.00 (0.96, 1.04)0.980
      IAA2721.4 (1.9)7,2911.2 (1.8)1.01 (0.95, 1.07)0.763
      GADA2991.3 (1.9)7,2641.2 (1.8)1.01 (0.95, 1.07)0.810
      Any breastfeedingAny IA6941.38.4 (7.3)6,6173.57.4 (6.4)1.01 (1.00, 1.02)0.118
      IAA2708.5 (6.7)7,0417.5 (6.5)1.01 (0.99, 1.03)0.205
      GADA2948.6 (8.2)7,0177.4 (6.5)1.01 (1.00, 1.03)0.123
      Any infant formulaAny IA59814.91.2 (2.5)6,00612.41.2 (2.3)0.99 (0.96, 1.02)0.522
      IAA2351.4 (2.7)6,3691.2 (2.3)1.02 (0.96, 1.05)0.574
      GADA2571.3 (2.5)6,3471.2 (2.3)1.01 (0.96, 1.06)0.696
      Cow’s milkAny IA7010.32.1 (3.1)6,8240.51.8 (2.8)1.01 (0.98, 1.04)0.474
      IAA2702.2 (3.2)7,2551.8 (2.8)1.02 (0.98, 1.07)0.301
      GADA2992.0 (3.0)7,2261.9 (2.8)1.01 (0.97, 1.05)0.613
      Any solid foodAny IA7010.33.6 (1.4)6,8390.33.5 (1.4)1.03 (0.97, 1.09)0.384
      IAA2723.5 (1.4)7,2683.5 (1.4)0.99 (0.90, 1.08)0.757
      GADA2973.7 (1.3)7,2433.5 (1.4)1.07 (0.97, 1.17)0.159
      Selected foodsAny IA7010.33.7 (1.3)6,8380.33.6 (1.4)1.03 (0.97, 1.09)0.368
      IAA2723.6 (1.3)7,2673.6 (1.4)1.01 (0.91, 1.11)0.873
      GADA2973.7 (1.3)7,2423.6 (1.4)1.00 (1.00, 1.01)0.118
      Cereals, anyAny IA6990.64.4 (1.4)6,8100.74.2 (1.4)1.03 (0.97, 1.10)0.330
      IAA2714.4 (1.4)7,2384.2 (1.4)1.01 (0.91, 1.14)0.789
      GADA2964.3 (1.3)7,2134.2 (1.4)1.03 (0.94, 1.14)0.525
      Gluten-containing cerealsAny IA6990.65.8 (2.1)6,7082.25.7 (2.0)1.05 (1.01, 1.10)0.023
      IAA2715.9 (2.1)7,1365.7 (2.0)1.08 (1.00, 1.16)0.038
      GADA2965.8 (2.0)7,1115.7 (2.0)1.06 (0.99, 1.13)0.121
      RiceAny IA6990.65.0 (1.9)6,7551.54.8 (1.8)1.02 (0.97, 1.07)0.445
      IAA2715.1 (2.0)7,1834.8 (1.8)1.01 (0.93, 1.10)0.779
      GADA2964.8 (1.7)7,1584.8 (1.8)1.00 (0.93, 1.08)0.936
      Root vegetablesAny IA7010.34.3 (1.2)6,8060.84.3 (1.3)1.03 (0.96, 1.10)0.464
      IAA2724.2 (1.2)7,2354.3 (1.3)1.00 (0.90, 1.12)0.942
      GADA2974.4 (1.3)7,2104.3 (1.3)1.05 (0.95, 1.16)0.352
      PotatoesAny IA6990.65.2 (2.2)6,6982.45.3 (2.4)1.05 (1.00, 1.10)0.051
      IAA2715.1 (2.1)7,1265.3 (2.4)1.05 (0.97, 1.14)0.200
      GADA2965.4 (2.4)7,1015.3 (2.3)1.06 (0.99, 1.13)0.116
      Fruits or berriesAny IA7000.44.3 (1.4)6,8060.84.2 (1.5)1.04 (0.98, 1.10)0.167
      IAA2724.3 (1.5)7,2344.2 (1.5)1.04 (0.95, 1.14)0.372
      GADA2964.4 (1.4)7,2104.2 (1.5)1.05 (0.96, 1.14)0.315
      MeatAny IA6921.66.0 (1.8)6,6762.76.1 (2.0)1.02 (0.97, 1.08)0.457
      IAA2696.0 (1.7)7,0996.1 (2.0)1.03 (0.94, 1.12)0.564
      GADA2926.1 (2.0)7,0766.1 (2.0)1.04 (0.96, 1.12)0.364
      EggAny IA6842.78.9 (2.5)6,4585.98.7 (2.5)1.02 (0.99, 1.05)0.288
      IAA2668.9 (2.7)6,8768.7 (2.5)1.00 (0.95, 1.06)0.878
      GADA2908.9 (2.4)6,8528.7 (2.5)1.04 (0.99, 1.09)0.140
      Fish or other seafoodAny IA6625.88.6 (3.6)6,2109.58.6 (3.6)1.01 (0.98, 1.04)0.537
      IAA2568.5 (3.8)6,6168.6 (3.6)0.99 (0.94, 1.05)0.810
      GADA2808.7 (3.6)6,5928.6 (3.6)1.03 (0.98, 1.08)0.258
      • ↵*HR and corresponding P value were obtained from the Cox regression model adjusted for country, HLA genotype, FDR status, sex of the child, and probiotic use <28 days. HRs reflect the change in the risk with 1-month longer breastfeeding or 1-month delay in food introduction.

    • Table 4

      Categorized duration of breastfeeding and timing of introduction of complementary foods and risk of IA (any IA or GADA)

      IADietary exposure*Timing in months*Number of children who developed any IA or GADA, N (%)Number of children who did not develop any IA or GADA, N (%)Unadjusted HR (95% CI)P valueAdjusted† HR (95% CI)P value
      Any IAGluten-containing cereals<428 (6)445 (94)0.68 (0.47, 0.99)0.0470.67 (0.54, 0.98)0.037
      4–9637 (10)6,048 (90)11
      >931 (14)185 (86)1.57 (1.07, 2.31)0.0221.44 (0.97, 2.16)0.074
      Any breastfeeding≤7334 (9)3,575 (91)0.93 (0.80, 1.08)0.3260.94 (0.81, 1.09)0.426
      >7360 (11)3,042 (89)11
      Cow’s milk≤5584 (10)5,922(91)0.83 (0.68, 1.00)0.0550.85 (0.69, 1.04)0.115
      >5117 (11)902 (89)11
      Cereals≤4483 (9)4,765 (91)0.99 (0.85, 1.17)0.9451.09 (0.92, 1.30)0.309
      >4216 (10)2,045 (90)11
      Rice≤7618 (9)6,196 (91)0.79 (0.63, 0.99)0.0460.87 (0.69, 1.10)0.233
      >775 (13)502 (87)11
      Fruit and berries≤4460 (9)4,552 (91)0.99 (0.85, 1.15)0.8681.00 (0.85, 1.18)0.999
      >4240 (10)2,254 (90)11
      Potato≤7578 (10)5,345 (90)1.19 (0.98, 1.45)0.0770.98 (0.77, 1.25)0.898
      >7121 (8)1,353 (92)11
      Meat≤8615 (10)5,762 (90)1.27 (1.01, 1.59)0.0401.13 (0.88, 1.45)0.344
      >877 (8)914 (92)11
      Egg≤9282 (9)3,002 (91)0.86 (0.74, 0.99)0.0450.84 (0.72, 0.99)0.035
      >9402 (10)3,456 (90)11
      GADAAny breastfeeding≤6120 (3)3,476 (97)1.20 (0.95, 1.52)0.1261.17 (0.92, 1.49)0.196
      >6174 (5)3,541 (95)11
      Rice≤6264 (4)6,435 (96)1.25 (0.87, 1.78)0.2241.10 (0.76, 1.58)0.623
      >628 (4)664 (96)11
      Fish and seafood≤9188 (4)4,538 (96)0.88 (0.70, 1.12)0.2901.11 (0.81, 1.53)0.507
      >992 (4)2,054 (96)11
      • ↵*Dietary exposure: timing of breastfeeding or food; categorization of timing of gluten-containing cereals’ introductions was based on martingale residuals whereas dichotomizations of timing of other dietary exposures in relation to the risk of any IA or GADA were based on change-point methods using log-rank test (28); only statistically significant (P < 0.05) cut points are shown. No statistically significant cut point of timing of a dietary exposure for IAA was detected.

      • ↵†The Cox regression model was adjusted for country, HLA genotype, FDR status, sex of the child, and probiotic use <28 days.

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    Early Infant Diet and Islet Autoimmunity in the TEDDY Study
    Ulla Uusitalo, Hye-Seung Lee, Carin Andrén Aronsson, Kendra Vehik, Jimin Yang, Sandra Hummel, Katherine Silvis, Åke Lernmark, Marian Rewers, William Hagopian, Jin-Xiong She, Olli Simell, Jorma Toppari, Anette-G. Ziegler, Beena Akolkar, Jeffrey Krischer, Suvi M. Virtanen, Jill M. Norris, the TEDDY Study Group
    Diabetes Care Mar 2018, 41 (3) 522-530; DOI: 10.2337/dc17-1983

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    Early Infant Diet and Islet Autoimmunity in the TEDDY Study
    Ulla Uusitalo, Hye-Seung Lee, Carin Andrén Aronsson, Kendra Vehik, Jimin Yang, Sandra Hummel, Katherine Silvis, Åke Lernmark, Marian Rewers, William Hagopian, Jin-Xiong She, Olli Simell, Jorma Toppari, Anette-G. Ziegler, Beena Akolkar, Jeffrey Krischer, Suvi M. Virtanen, Jill M. Norris, the TEDDY Study Group
    Diabetes Care Mar 2018, 41 (3) 522-530; DOI: 10.2337/dc17-1983
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