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The Effects of Type 1 Diabetes on Cognitive Performance

A meta-analysis

  1. Augustina M.A. Brands, MSC123,
  2. Geert Jan Biessels, PHD, MD1,
  3. Edward H.F. de Haan, PHD13,
  4. L. Jaap Kappelle, PHD, MD1 and
  5. Roy P.C. Kessels, PHD13
  1. 1Department of Neurology, University Medical Center, Utrecht, the Netherlands
  2. 2Department of Neuropsychology, Hofpoort Hospital/Regional Psychiatrisch Centrum, Woerden, the Netherlands
  3. 3Helmholtz Instituut, Utrecht University, the Netherlands
  1. Address correspondence and reprint requests to Augustina M.A. Brands, MSc, Department of Neuropsychology, Hofpoort Hospital, Blekerijlaan 3, 3447 AC Woerden, Netherlands. E-mail: i.brands{at}altrecht.nl
Diabetes Care 2005 Mar; 28(3): 726-735. https://doi.org/10.2337/diacare.28.3.726
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  • Figure 1—
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    Figure 1—

    Standardized effect sizes (Cohen’s d) and 95% CIs for the cognitive domains in patients with type 1 diabetes compared with nondiabetic control subjects. Number of patients included in each domain is listed between brackets. Nonsignificant P values are not shown. Refs.: a = (1,3,18,19,20–32), b = (18,19,22,27,29, c = (6,18,19,25), d = (3,6,18,20,22,23,25,31), e = (6,18,22,25,29), f = (3,6,18,22,25), g = (6,22,25,29), h = (3,22,25), i = (3,6,18,19,21,22,25,30), j = (20,24,28,29,32), k = (20,27), l = (2,3,21,25,29), m = (18,27,29), n = (25,26,29), o = (25,29,31), p = (3,18,19,20–22,25,27,29), q = (6,18,19,27,29), and r = (2,19,22,25).

  • Figure 2—
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    Figure 2—

    Standardized effect sizes (Cohen’s d) and 95% CIs for the cognitive domains in patients with compared with patients without recurrent episodes of severe hypoglycemia. Number of patients with recurrent episodes of severe hypoglycemia in each domain is listed between brackets. Nonsignificant P values are not shown. Refs.: a = (4,29–31,36,37,39,41), b = (29,30,36,41), c = (4,31,37,39,41), d = (29,36,37,39), e = (29,37,39), f = (30,37,39,41), g = (29,36), h = (4,39,41), i = (29,31,37,39,41), j = (4,29,36,37,39), and k = (29,39)

Tables

  • Figures
  • Table 1—

    Characteristics of studies that have assessed cognitive functioning in patients with type 1 diabetes and nondiabetic control subjects

    First author (ref.)n (grp 1)/(grp 2)% Males (grp 1)/(grp 2)Age (grp 1)/(grp 2) (years)Subjects matched forHbA1c or HbA1 (%)Duration (years)Calculated age at onset (years)Included complications and characteristicsExclusion criteria or absent characteristics
    Meuter et al. 1980 (17)112/11250/5038 ± 14.3/NDEND10.5 ± 9.317H,Hy,N,R,NeND
    Franceschi et al. 1984 (18)37/2643/4225.8 ± 5/26.4 ± 5E,O,SES12.7 ± 2.57.7 ± 5.518Hy,N,RH,Ne,CI,DL,P
    Skenazy et al. 1984 (19)
        Visually impaired20/2470/6728 ± 6.1/22.6 ± 5.6NDND18.7 ± 5.99H,Hy,N,R,NeND
        Nonvisually impaired19/2453/6732.1 ± 6.2/22.6 ± 5.6NDND15.3 ± 7.817H,Hy,N,R,NeND
    Lawson et al. 1984 (5)48/4054/4838.3 ± 14.6/38.8 ± 12.8ND9.113 ± 10.815Hy,NP
    Grill et al. 1990 (20)6/5ND37.1 ± 6.9/30.3 ± 4.5ND6.9 ± 0.719.4 ± 5.118Hy,RCV,Ne,H,CI,N
    Widom et al. 1990 (21)
        Poor metabolic control9/1044/6022 ± 3/27 ± 3.2ND11.8 ± 1.212 ± 610RN,Ne,
        Good metabolic control8/1050/6027 ± 5.7/27 ± 3.2ND8 ± 0.67 ± 2.820NDN,Ne,R
    Dejgaard et al. 1991 (22)20/120ND/ND44 ± 9/NDND9.1 ± 1.426 ± 918Hy,N,R,NeP
    Pozzessere et al. 1991 (23)16/1670/7033.2 ± 12.6/33.4 ± 12.5E7 ± 1.69 ± 7.724HHy,NA,P,DL
    Blackman et al. 1992 (24)14/1043/5029.5 ± 6/26.7 ± 6ND11 ± 1.9NDNDNDHy,N
    Ryan et al. 1992 (2)75/7545/2535.5 ± 5.6/36.2 ± 6.8E,SES10.326.6 ± 6.79Hy,N,R,ND
    Sachon et al. 1992 (3)
        Severe hypoglycemia30/2577/4841 ± 13/38 ± 15O,SES7.4 ± 1.218 ± 1323Hy,N,Ne,RND
        No hypoglycemia25/2560/4834 ± 10/38 ± 15O,SES8.6 ± 1.915 ± 1118N,Ne,RHy,ND
    Wirsen et al. 1992 (25)10/12100/100R 20–43/R 18–32E,7.9 ± 0.6NDNDHyN
    Cox et al. 1993 (26)10/1040/ND34/NDE,O9.81816NDND
    Deary et al. 1993 (1)100/100ND/ND40.9 ± 8.8/40.2 ± 6.7END>5>19Hy,R,N,NeP
    Ryan et al. 1993 (6)
        Females41/410/033.4 ± 5.5/35.2 ± 8.4E,SES10.9 ± 1.825.3 ± 6.68Hy,N,Ne,RND
        Males41/41100/10033.4 ± 5.2/34.7 ± 7.5E,SES10.6 ± 227.1 ± 5.56Hy,N,Ne,RND
    Ryan et al. 1993 (27)142/10051/4733.5 ± 5.6/34.1 ± 6.7E,SES10.6 ± 1.824.8 ± 6.18Hy,N,Ne,RND
    Maran et al. 1995 (28)
        Good metabolic control8/875/6336 ± 3/31 ± 2ND7.7 ± 0.316 ± 220HyND
        Poor metabolic control10/860/6332 ± 4/31 ± 2ND10.1 ± 0.217 ± 315NDND
    Hershey et al. 1997 (29)
        Severe hypoglycemia26/21ND/ND26.2 ± 6.6/27.8 ± 8.1END>5<14HyR,N
        No hypoglycemia12/21ND/ND22.8 ± 7.7/27.8 ± 8.1END>5<14—Hy,R,N
    Kramer et al. 1998 (30)108/10845/ND36 ± 13/36 ± 13NDND>1>16H,Hy,N,R,P,Ne
    Snoek et al. 1998 (31)
        Severe hypoglycemia9/9100/10036.9 ± 6.7/NDND7.413.424HyP,
        No hypoglycemia9/9100/10036.9 ± 6.7/NDND7.413.424—Hy,P,
    Lobmann et al. 2000 (32)12/1233/5831 ± 7/27 ± 3ND7.4 ± 1.87.8 ± 8.623HyN,R,H,CI,Ne,
    • Data are means ± SD, unless otherwise indicated. CI, cardiac insufficiency; DL, dyslipidemia; E, education; H, hypertension or hypertensive treatment; Hy, severe hypoglycemic episodes; N, neuropathy; ND, not specifically defined; Ne, nephropathy and/or microalbuminuria; O, occupation; P, psychiatric problems and/or use of psychoactive drugs and/or addiction to alcohol or other substances; R, retinopathy; SES, socioeconomic status.

  • Table 2—

    Characteristics of studies that have assessed cognitive functioning in patients with type 1 diabetes, comparing different diabetic characteristics

    First author (ref.)Type (grp 1/grp 2)n (grp 1/grp 2)% Males (grp 1/grp 2)Age (grp 1/grp 2)HbA1 (grp 1/grp 2)Duration (grp 1/grp 2)Calculated age at onset (grp 1/grp 2)Included complications and characteristicsExclusion criteria or absent characteristicsSubjects matched for
    Hung et al. 1984 (33)Poor MC/good MC12/2067/6535.1/34.1513 ± 0.9/10 ± 0.820.2/22.815/14R,NNeND
    Skenazy et al. 1984 (19)Vis imp/non-vis imp20/1970/5328 ± 6.1/32.1 ± 6ND/ND18.7 ± 5.9/15.3 ± 7.89/17H,N,R,NeNDND
    Holmes 1986 (7)Poor MC/good MC8/19100/10020.9 ± 2.4/23.4 ± 5.412.4 ± 0.7/8.2 ± 1.67.8 ± 4.1/8.4 ± 5.713/15NDPE,SES
    Holmes et al. 1988 (34)Poor MC/good MC6/10100/10022.2 ± 4.3/24 ± 5.310.1 ± 1/6.9 ± 0.87.5 ± 3.8/6.7 ± 4.415/14NDRND
    Prescott et al. 1990 (35)Poor MC/good MC20/2050/5040.3 ± 11.6/39.8 ± 1013.1 ± 1.6/8.9 ± 115.2 ± 10.5/14 ± 10.325/26NDNDSES
    Widom et al. 1990 (21)Poor MC/good MC9/844/5022 ± 3/27 ± 5.711.8 ± 1.2/8 ± 0.612 ± 6/7 ± 2.810/20R,NDN,NeND
    Wredling et al. 1990 (4)Sev hy/no sev hy17/17ND/ND49 ± 18/48 ± 177.9 ± 1.6/8.8 ± 1.628 ± 18/29 ± 1321/19N,R,PNDE
    Langan et al. 1991 (36)Sev hy/no sev hy24/2358/4837.9 ± 6.4/38.5 ± 5.310 ± 2.3/10.2 ± 1.810.7 ± 4/13 ± 427/25R,N,Ne,HCV,P,PDND
    Sachon et al. 1992 (3)IHA/NHA30/2577/6041 ± 13/34 ± 107.4 ± 1.2/8.6 ± 1.918 ± 13/15 ± 1124/19N,Ne,RNDO,SES
    Ryan et al. 1993 (27)Compl/no compl113/2949/5534.3 ± 5.4/30.7 ± 5.610.6 ± 1.7/10.7 ± 1.925.9 ± 5.6/20.5 ± 5.88/10N,Ne,RNDE,SES
    Chabriat et al. 1994 (37)Sev hy/no sev hy15/6ND/ND47.6 ± 17/42.8 ± 197.2 ± 1.7/7.1 ± 0.819.6 ± 16/11.3 ± 728/32H,R,M,N,CVE
    Gold et al. 1995 (38)IHA/NHA10/10ND/ND35 ± 7.7/37.4 ± 5.19.7 ± 1/10.3 ± 2.212.8 ± 4.4/17.9 ± 7.823/19HP,R,NND
    Maran et al. 1995 (28)Poor MC/good MC10/860/7532 ± 4/36 ± 310.1 ± 0.2/7.7 ± 0.317 ± 3/16 ± 215/20NDNDND
    DCCT 1996 (39)
        >5 episodesSev hy/no sev hy23/1,045ND/ND<50/<50ND/ND>6/>6ND—R,Ne,N,PND
        1–5 episodesSev hy/no sev hy314/1,045ND/ND<50/<50ND/ND>6/>6ND—R,Ne,N,PND
    Reichard et al. 1996 (40)Poor MC/good MC48/43NDND/ND8.3 ± 1/7.2 ± 0.6ND/NDNDRND
    Hershey et al. 1997 (29)Sev hy/no sev hy26/12ND/ND26.2 ± 6.6/22.8 ± 7.7ND/ND>5/>5<14—R,NE
    Kramer et al. 1998 (30)
        HypoglycemiaSev hy/no sev hy55/5335/5738 ± 14/34 ± 127 ± 1.6/6.9 ± 1.317.6 ± 11.6/10.8 ± 10.620/23H,N,RP,NeA
        MCHbA1c >6.5/HbA1c <6.5ND/NDND/NDND/NDND/NDND/ND>16H,N,RP,NeA
    Snoek et al. 1998 (31)Sev hy/no sev hy9/936.9 ± 6.7/36.9 ± 6.77.4/7.413.4/13.424/27—PA,S
    Howorka et al. 2000 (41)Sev hy/no sev hy13/1446/3636.1 ± 10.2/36.1 ± 107.6 ± 1/7.3 ± 1.216.7 ± 7.4/15.6 ± 8.619/20RP,CV,N,CIA,S
    Strachan et al. 2000 (42)IHA/NHA20/2065/6036.4 ± 14.7/34 ± 12.58.3 ± 1.3/10 ± 1.715.5 ± 7.6/13 ± 8.220/21NDPA,S
    Ferguson et al. 2003 (8)R/no R25/4650/4031.5 ± 6/26.4 ± 4.68.9 ± 1.3/8.4 ± 1.221.6 ± 5.9/17 ± 4.610/9HyN,Ne,H,PND
    • Data are means ± SD, unless otherwise indicated. A, age; CI, cardiac insufficiency; Compl, diabetes complications; DL, dyslipidemia; E, education; Gluc, hypoglycemia prevented during testing; H, hypertension or hypertensive treatment; Hy, severe hypoglycemic episodes; IHA, impaired awareness of hypoglycemia; MC, metabolic control; N, neuropathy; ND, not specifically defined; Ne, nephropathy and/or microalbuminuria; NHA, normal awareness of hypoglycemia; O, occupation; P, psychiatric problems and/or use of psychoactive drugs and/or addiction to alcohol or other substances; R, retinopathy; S, sex; SES, socioeconomic status; Sev hy, episodes of severe hypoglycemia; Vis imp, visually impaired.

  • Table 3—

    Domain scores from studies that could not be explored further meta-analytically

    Cognitive domains
    First author (ref.)Group 1Group 2Overall intelligenceWorking memoryLearning immediate memoryDelayed memoryPsychomotor efficiencySpeed of information processMotor speedAttentionCognitive flexibilityVisual perceptionLanguage
    Hung et al. (33)Poor MCGood MC—0.18−0.71—————0.17——
    Skenazy et al. (19)Vis impNon vis imp0.23—————————0.29
    Holmes (7)Poor MCGood MC−0.31————−0.530.38————
    Holmes et al. (34)Poor MCGood MC−0.10———0.14−0.730.64————
    Prescott et al. (35)Good MCGood MC——0————————
    Widom et al. (21)Poor MCGood MC————−0.33——0.170.89——
    Ryan et al. (27)ComplNo compl0.23—−0.24———−0.80−0.280.10−0.35—
    Gold et al. (38)IHANHA−0.33———0——————
    Maran et al. (28)Poor MCGood MC—————0.45—————
    Kramer et al. (30)Poor MCGood MC0.28———0——————
    Strachan et al. (42)IHANHA——−0.10−0.13−0.770—−0.63−0.54——
    Ferguson et al. (8)RNo R−0.31———−0.48−0.59—−0.40−0.34——
    • Data are Cohen’s d. Negative effects sizes reflect worse performance in group 1. Compl, diabetes complications; IHA, impaired awareness of hypoglycemia; MC, metabolic control; NHA, normal awareness of hypoglycemia; Vis imp, visually impaired; R, retinopathy.

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The Effects of Type 1 Diabetes on Cognitive Performance
Augustina M.A. Brands, Geert Jan Biessels, Edward H.F. de Haan, L. Jaap Kappelle, Roy P.C. Kessels
Diabetes Care Mar 2005, 28 (3) 726-735; DOI: 10.2337/diacare.28.3.726

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The Effects of Type 1 Diabetes on Cognitive Performance
Augustina M.A. Brands, Geert Jan Biessels, Edward H.F. de Haan, L. Jaap Kappelle, Roy P.C. Kessels
Diabetes Care Mar 2005, 28 (3) 726-735; DOI: 10.2337/diacare.28.3.726
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