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Sleep apnoea and incident malignancy in type 2 diabetes

Sarah Driendl, Michael Arzt, Claudia S. Zimmermann, Bettina Jung, Tobias Pukrop, Carsten A. Böger, Sebastian Haferkamp, Florian Zeman, Iris M. Heid, Stefan Stadler
ERJ Open Research 2021 7: 00036-2021; DOI: 10.1183/23120541.00036-2021
Sarah Driendl
1Dept of Internal Medicine II, University Hospital Regensburg, Regensburg, Germany
9These authors contributed equally
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Michael Arzt
1Dept of Internal Medicine II, University Hospital Regensburg, Regensburg, Germany
9These authors contributed equally
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Claudia S. Zimmermann
2Dept of Internal Medicine I, University Hospital Regensburg, Regensburg, Germany
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Bettina Jung
3Dept of Nephrology, University Hospital Regensburg, Regensburg, Germany
4Dept of Nephrology, Traunstein, Germany
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Tobias Pukrop
5Dept of Internal Medicine III, University Hospital Regensburg, Regensburg, Germany
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Carsten A. Böger
3Dept of Nephrology, University Hospital Regensburg, Regensburg, Germany
4Dept of Nephrology, Traunstein, Germany
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Sebastian Haferkamp
6Dept of Dermatology, University Hospital Regensburg, Regensburg, Germany
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Florian Zeman
7Centre of Clinical Studies, University Hospital Regensburg, Regensburg, Germany
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Iris M. Heid
8Dept of Genetic Epidemiology, University Hospital Regensburg, Regensburg, Germany
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Stefan Stadler
1Dept of Internal Medicine II, University Hospital Regensburg, Regensburg, Germany
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  • For correspondence: stefan.stadler@ukr.de
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  • FIGURE 1
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    FIGURE 1

    Study flow chart. SDB: sleep disordered breathing.

  • FIGURE 2
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    FIGURE 2

    Cumulative adjusted hazard for incident malignancy in 1239 patients with diabetes mellitus type 2 and a) apnoea–hypopnoea index (AHI) <30 events·h−1 versus ≥30 events·h−1; b) oxygen desaturation index (ODI) <30 events·h−1 versus ≥30 events·h−1; and c) percentage of night-time spent with oxygen saturation <90% (tsat90%) <10.4% versus ≥10.4%.

  • FIGURE 3
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    FIGURE 3

    Cumulative adjusted hazard for incident malignancy in i) 511 females and ii) 728 males with a) apnoea–hypopnoea index (AHI) <30 events·h−1 versus ≥30 events·h−1; b) oxygen desaturation index (ODI) <30 events·h−1 versus ≥30 events·h−1; and c) percentage of night-time spent with oxygen saturation <90% (tsat90%) <10.4% versus ≥10.4%.

Tables

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  • TABLE 1

    Baseline characteristics of the 1239 patients overall and according to severity of sleep disordered breathing

    Entire cohortAHI <30 events·h−1AHI ≥30 events·h−1
    Patients12391111 (89.7)128 (10.3)
    Age years67±966±968±8
    Female511 (41.2)482 (43.4)29 (22.7)
    BMI kg·m−230.9±5.330.5±5.233.6±5.9
    Waist–hip ratio0.95±0.080.95±0.081.00±0.08
    Obesity622 (50.2)533 (48.0)89 (69.5)
    HbA1c mmol·mol−151±1151±1250±9
    Former or current smokers701 (56.6)624 (56.2)77 (60.2)
    High alcohol intake#353 (28.5)309 (27.8)44 (34.4)
    Socioeconomic status¶2 (1–2)2 (1–2)2 (2–2)
    Physical inactivity+699 (56.4)620 (55.8)79 (61.7)
    Follow-up time years2.7 (2.2–4.5)2.8 (2.2–4.5)2.4 (2.1–4.5)
    Excessive daytime sleepiness§87 (7.1)77 (7.0)10 (7.8)
    AHI events·h−110 (5–19)9 (4–15)44 (36–52)
    ODI events·h−19 (5–19)8 (5–15)39 (33–49)
    tsat90%10.4 (2.5–30.6)8.8 (2.1–28.4)23.5 (13.7–45.4)

    Data are presented as n, mean±sd, n (%) or median (interquartile range). AHI: apnoea–hypopnoea index; BMI: body mass index; ODI: oxygen-desaturation index; tsat90%: percentage of night-time spent with oxygen saturation <90%. #: ≥3 drinks per week; ¶: according to Robert Koch Institute (Germany) [37] subdivided into four groups ranging from 1 (lowest) to 4 (highest) and including educational level, professional qualification and income; +: light activity ≤2 times per week; §: Epworth Sleepiness Scale ≥11.

    • TABLE 2

      Tumour entities

      Total sample1239
       Skin tumours#20 (25.3)
       Prostate carcinoma9 (11.5)
       Colorectal carcinoma7 (8.9)
       Pancreatic carcinoma7 (8.9)
       Breast cancer5 (6.3)
       Pulmonary carcinoma5 (6.3)
       Malignancy of the haematopoietic and lymphatic system5 (6.3)
       Malignancy of the female genital organ5 (6.3)
       Malignancy of the urinary organ5 (6.3)
       Others¶11 (13.9)
       Total79 (100)
      Males728
       Skin tumours#15 (28.3)
       Prostate carcinoma9 (17.0)
       Colorectal carcinoma7 (13.2)
       Malignancy of the urinary organ5 (9.4)
       Pulmonary carcinoma4 (7.5)
       Pancreatic carcinoma3 (5.7)
       Malignancy of the haematopoietic and lymphatic system2 (3.8)
       Others¶8 (15.1)
       Total53 (100)
      Females511
       Skin tumours#5 (19.2)
       Breast cancer5 (19.2)
       Malignancy of the female genital organ5 (19.2)
       Pancreatic carcinoma4 (15.4)
       Malignancy of the haematopoietic and lymphatic system3 (11.6)
       Pulmonary carcinoma1 (3.8)
       Others¶3 (11.6)
       Total26 (100)

      Data are presented as n or n (%). #: malignant melanomas, squamous cell carcinomas and lentiginous melanomas (basal cell carcinomas were excluded); ¶: cancer types observed only in few or single persons, e.g. liver tumour, parotid tumour, meningioma.

      • TABLE 3

        Adjusted hazard ratios (HRs) for the incidence of malignancy in 1239 patients with type 2 diabetes during a median follow-up of 2.7 years (number of events 79)

        Adjusted HR (95% CI)#p-value
        AHI events·h−1
         AHI (continuous)1.01 (0.99–1.03)0.416
         AHI ≥301.30 (0.64–2.62)0.473
        ODI events·h−1
         ODI (continuous)1.00 (0.98–1.02)0.799
         ODI ≥301.24 (0.57–2.68)0.584
        tsat90%
          tsat90% (continuous)1.00 (1.00–1.01)0.395
          tsat90% ≥10.4%1.59 (0.94–2.68)0.085

        HRs calculated using Cox proportional hazards regression analysis. The multivariable analyses were adjusted for sex, age, body mass index, smoking status, alcohol intake, socioeconomic status and HbA1c. AHI: apnoea–hypopnoea index; ODI: oxygen desaturation index; tsat90%: percentage of night-time spent with oxygen saturation <90%.

        • TABLE 4

          Adjusted hazard ratios (HRs) for the incidence of malignancy in 1239 patients with type 2 diabetes during a median follow-up of 2.7 years stratified by sex and age

          MalesFemales≥70 years<70 years
          Adjusted HR (95% CI)p-valueAdjusted HR (95% CI)p-valueAdjusted HR (95% CI)p-valueAdjusted HR (95% CI)p-value
          Patients n728511472767
          Events n53264336
          AHI events·h−1
           AHI (continuous)1.00 (0.97–1.02)0.6591.03 (1.00–1.06)0.0281.00 (0.98–1.03)0.7511.01 (0.98–1.03)0.538
           AHI ≥300.76 (0.31–1.87)0.5504.19 (1.38–12.77)0.0121.21 (0.48–3.09)0.6861.28 (0.44–3.78)0.651
          ODI events·h−1
           ODI (continuous)0.99 (0.96–1.01)0.3571.04 (1.00–1.07)0.0321.00 (0.97–1.03)0.9331.00 (0.97–1.03)0.972
           ODI ≥300.62 (0.22–1.79)0.3805.64 (1.78–17.90)0.0031.34 (0.53–3.36)0.5390.88 (0.20–3.83)0.863
          tsat90%
            tsat90% (continuous)1.00 (0.99–1.01)0.6701.02 (1.00–1.03)0.0351.00 (0.99–1.01)0.9121.01 (1.00–1.02)0.236
            tsat90% ≥10.4%1.28 (0.66–2.46)0.4672.57 (1.03–6.41)0.0430.91 (0.51–2.11)0.9132.43 (1.09–5.42)0.030

          HRs calculated by Cox proportional hazards regression analysis. The multivariable analyses were adjusted for sex, age, body mass index, smoking status, alcohol intake, socioeconomic status and HbA1c. AHI: apnoea–hypopnoea index; ODI: oxygen desaturation index; tsat90%: percentage of night-time spent with oxygen saturation <90%.

          • TABLE 5

            Association of sleep apnoea and incidence# of malignancy, comparison of existing studies

            First author (year) [ref.]Population n (% female)T2D %Study designFollow-up yearsSleep apnoea diagnosisMain outcomesMain findingsKey limitations
            Sleep apnoea diagnosis with PSG or PG
             Prospective
              Driendl   (2020;   present   study)1239
            (41)
            100Prospective cohort study2.7PGCancer incidence (n=79)Association between AHI ≥30 events·h−1 and cancer incidence in femalesUse of PG
              Marshall   (2014) [39]390
            (26)
            3Prospective cohort study20PGCancer incidence (n=125)Association between elevated RDI (≥15 events·h−1) and cancer incidenceSmall population
            Lack of control of some cancer risk factors
            Lack of information on PAP therapy
             Retrospective
              Justeau   (2020) [40]8748
            (36)
            15Retrospective cohort study, multicentre5.8PSG, PGCancer incidence (n=718)Association between nocturnal hypoxaemia (tsat90% >13%) and cancer incidenceLack of control of some cancer risk factors
            Partial use of PG
              Campos-   Rodriguez   (2013) [9]4910
            (33)
            n/sRetrospective cohort study, multicentre4.5PSG (32%), PG (68%)Cancer incidence
            (n=261)
            Association between severe OSA (tsat90% >12%) and cancer incidence, limited to male patients <65 yearsLack of control of some cancer risk factors
            Major use of PG
              Brenner   (2019) [10]5243
            (26)
            n/sRetrospective cohort study5.9PSGCancer incidence (n=265)Association between AHI >57 events·h−1 and cancer incidence for patients <45 yearsLack of control of some cancer risk factors
            Lack of information on PAP therapy
              Kendzerska   (2014) [41]10 149
            (38)
            14Retrospective cohort study, multicentre7.8PSGCancer incidence (n=627)No association between OSA and cancer incidence
             Cross-sectional
              Pataka (2019)   [42]19 556
            (29)
            n/sCross-sectional analysis, multicentrePSG, PGCancer prevalence (n=388)Association between cancer prevalence and OSA and nocturnal hypoxaemia in femalesLack of control of some cancer risk factors
            Lack of information on PAP therapy
             Meta-analysis
              Shantha   (2015) [21]112 228
            (26–100)
            4–22Meta-analysis, five studies4.5–20PSG, PGCancer incidence
            (n=864)
            Patients with SDB had a nearly 50% greater overall cancer risk compared with patients without SDB
              Zhang (2017)   [22]86 460
            (26–38)
            n/sMeta-analysis, six studies4.5–20PSG, PGCancer incidence (n=965)OSA was not independently associated with cancer incidence
            OSA diagnosed according to ICD-9 or symptoms
             Prospective
              Christensen   (2013) [43]8783
            (55)
            n/sProspective cohort study13Symptoms of OSACancer incidence (n=1985)No association between symptoms of OSA and cancer incidenceOSA diagnosis based on symptoms
            Lack of information on PAP therapy
             Retrospective
              Gozal (2016)   [11]5.6 million
            (50)
            14 in OSA-groupRetrospective cohort study3.2–3.9According to ICD-9-CMCancer incidence (n=167 022)Elevated risk for malignant melanoma and kidney and pancreatic cancer for patients with OSA
            Lower risk for colorectal, breast and prostate cancer for patients with OSA
            Potential bias by use of administrative claims database
            Lack of control of some cancer risk factors
              Sillah (2018)   [12]34 402
            (43)
            n/sRetrospective cohort study5.3According to ICD-9-CMCancer incidence (n=1575)Elevated risk for malignant melanoma and kidney, uterine and breast cancer for patients with OSA
            Lower risk for colorectal and lung cancer for patients with OSA
            Lack of control of some cancer risk factors
            Lack of information on PAP therapy

            T2D: type 2 diabetes mellitus; PSG: polysomnography; PG: polygraphy; OSA: obstructive sleep apnoea; ICD-9-CM: International Classification of Diseases, 9th Revision, Clinical Modification; AHI: apnoea–hypopnoea index; RDI: respiratory disturbance index; n/s: not specified; PAP: positive airway pressure; SDB: sleep disordered breathing; tsat90%: percentage of night-time spent with oxygen saturation <90%. #: prevalence shown for Pataka et al. [42].

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            Sleep apnoea and incident malignancy in type 2 diabetes
            Sarah Driendl, Michael Arzt, Claudia S. Zimmermann, Bettina Jung, Tobias Pukrop, Carsten A. Böger, Sebastian Haferkamp, Florian Zeman, Iris M. Heid, Stefan Stadler
            ERJ Open Research Apr 2021, 7 (2) 00036-2021; DOI: 10.1183/23120541.00036-2021

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            Sleep apnoea and incident malignancy in type 2 diabetes
            Sarah Driendl, Michael Arzt, Claudia S. Zimmermann, Bettina Jung, Tobias Pukrop, Carsten A. Böger, Sebastian Haferkamp, Florian Zeman, Iris M. Heid, Stefan Stadler
            ERJ Open Research Apr 2021, 7 (2) 00036-2021; DOI: 10.1183/23120541.00036-2021
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