PDF herunterladen
CC BY 4.0 · TH Open 2024; 08(01): e146-e154
DOI: 10.1055/a-2275-9590
Original Article

Risk of Bleeding and Venous Thromboembolism after Colorectal Cancer Surgery in Patients with and without Type 2 Diabetes: A Danish Cohort Study

Frederik Pagh Bredahl Kristensen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Aarhus University, Aarhus N, Denmark
,
Erzsébet Horváth-Puhó
1   Department of Clinical Epidemiology, Aarhus University Hospital and Aarhus University, Aarhus N, Denmark
,
Szimonetta Komjáthiné Szépligeti
1   Department of Clinical Epidemiology, Aarhus University Hospital and Aarhus University, Aarhus N, Denmark
,
Frederikke Schoenfeldt Troelsen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Aarhus University, Aarhus N, Denmark
,
Henrik Toft Sørensen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Aarhus University, Aarhus N, Denmark
› Institutsangaben Source of Funding F.P.B. Kristensen is supported by a PhD grant from Aarhus University.
› Weitere Informationen
Auch verfügbar auf
   Lizenzen und Reprints

Abstract

Background Bleeding and venous thromboembolism (VTE) are adverse outcomes after colorectal cancer (CRC) surgery. Type 2 diabetes (T2D) clusters with bleeding and VTE risk factors. We examined the bleeding and VTE risk in patients with T2D undergoing CRC surgery and the prognosis after these adverse outcomes.

Methods We conducted a prognostic population-based cohort study of 48,295 patients with and without T2D undergoing surgery for incident CRC during 2005 to 2019. Patients with T2D were diagnosed in a hospital setting or had redeemed a glucose-lowering drug prescription; the remaining cohort was patients without diabetes. We estimated the 30-day and 1-year risks of bleeding and VTE and used a Fine–Gray model to compute age-, sex-, and calendar year-adjusted subdistribution hazard ratios (SHRs). The Kaplan–Meier method was used to calculate 1-year mortality after bleeding or VTE.

Results Within 30 days after CRC surgery, the risk of bleeding was 2.7% in patients with T2D and 2.0% in patients without diabetes (SHR: 1.30 [95% confidence interval [CI]: 1.10–1.53]). For VTE, the 30-day risks were 0.6% for patients with T2D and 0.6% for patients without diabetes (SHR: 1.01 [95% CI: 0.71–1.42]). The SHRs for bleeding and VTE within 1 year after CRC surgery were similar. The 1-year mortality was 26.0% versus 24.9% in the bleeding cohort and 25.8% versus 27.5% in the VTE cohort for patients with T2D versus without diabetes, respectively.

Conclusion Although absolute risks were low, patients with T2D have an increased risk of bleeding but not VTE after CRC surgery.

Keywords

type 2 diabetes - bleeding - venous thromboembolism - colorectal cancer

Author Contributions

F.P.B. Kristensen: conception and design, interpretation of data, drafting of the manuscript, and critical revision of the manuscript for important intellectual content. E. Horváth-Puhó: conception and design, interpretation of data, data management, statistical analyses, and critical revision of the manuscript for important intellectual content. S.K. Szépligeti: conception and design, interpretation of data, data management, statistical analyses, and critical revision of the manuscript for important intellectual content. F.S. Troelsen: conception and design, interpretation of data, drafting of the manuscript, and critical revision of the manuscript for important intellectual content. H.T. Sørensen: acquisition of data, conception and design, interpretation of data, critical revision of the manuscript for important intellectual content, and supervision.


Supplementary Material



Publikationsverlauf

Eingereicht: 15. November 2023

Angenommen: 23. Februar 2024

Accepted Manuscript online:
26. Februar 2024

Artikel online veröffentlicht:
26. März 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68 (06) 394-424
    CrossrefPubMedGoogle Scholar
  • 2 Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet 2019; 394 (10207): 1467-1480
    CrossrefPubMedGoogle Scholar
  • 3 Ling S, Brown K, Miksza JK. et al. Association of type 2 diabetes with cancer: a meta-analysis with bias analysis for unmeasured confounding in 151 cohorts comprising 32 million people. Diabetes Care 2020; 43 (09) 2313-2322
    CrossrefPubMedGoogle Scholar
  • 4 Ahmad E, Lim S, Lamptey R, Webb DR, Davies MJ. Type 2 diabetes. Lancet 2022; 400 (10365): 1803-1820
    CrossrefPubMedGoogle Scholar
  • 5 Zanders MM, Vissers PA, Haak HR, van de Poll-Franse LV. Colorectal cancer, diabetes and survival: epidemiological insights. Diabetes Metab 2014; 40 (02) 120-127
    CrossrefPubMedGoogle Scholar
  • 6 Iversen LH. Aspects of survival from colorectal cancer in Denmark. Dan Med J 2012; 59 (04) B4428
    PubMedGoogle Scholar
  • 7 Ketelaers SHJ, Orsini RG, Burger JWA, Nieuwenhuijzen GAP, Rutten HJT. Significant improvement in postoperative and 1-year mortality after colorectal cancer surgery in recent years. Eur J Surg Oncol 2019; 45 (11) 2052-2058
    CrossrefPubMedGoogle Scholar
  • 8 Qiang JK, Sutradhar R, Giannakeas V, Bhatia D, Singh S, Lipscombe LL. Impact of diabetes on colorectal cancer stage and mortality risk: a population-based cohort study. Diabetologia 2020; 63 (05) 944-953
    CrossrefPubMedGoogle Scholar
  • 9 Fransgaard T, Thygesen LC, Gögenur I. Increased 30-day mortality in patients with diabetes undergoing surgery for colorectal cancer. Colorectal Dis 2016; 18 (01) O22-O29
    CrossrefPubMedGoogle Scholar
  • 10 Walker JJ, Brewster DH, Colhoun HM, Fischbacher CM, Lindsay RS, Wild SH. Scottish Diabetes Research Network (SDRN) Epidemiology Group. Cause-specific mortality in Scottish patients with colorectal cancer with and without type 2 diabetes (2000-2007). Diabetologia 2013; 56 (07) 1531-1541
    CrossrefPubMedGoogle Scholar
  • 11 De Bruijn KM, Arends LR, Hansen BE, Leeflang S, Ruiter R, van Eijck CH. Systematic review and meta-analysis of the association between diabetes mellitus and incidence and mortality in breast and colorectal cancer. Br J Surg 2013; 100 (11) 1421-1429
    CrossrefPubMedGoogle Scholar
  • 12 Birch RJ, Downing A, Finan PJ, Howell S, Ajjan RA, Morris EJA. Improving outcome prediction in individuals with colorectal cancer and diabetes by accurate assessment of vascular complications: Implications for clinical practice. Eur J Surg Oncol 2021; 47 (05) 999-1004
    CrossrefPubMedGoogle Scholar
  • 13 Barone BB, Yeh HC, Snyder CF. et al. Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis. JAMA 2008; 300 (23) 2754-2764
    CrossrefPubMedGoogle Scholar
  • 14 Becattini C, Rondelli F, Vedovati MC. et al. Incidence and risk factors for venous thromboembolism after laparoscopic surgery for colorectal cancer. Haematologica 2015; 100 (01) e35-e38
    CrossrefPubMedGoogle Scholar
  • 15 Lewis-Lloyd CA, Pettitt EM, Adiamah A, Crooks CJ, Humes DJ. Risk of postoperative venous thromboembolism after surgery for colorectal malignancy: a systematic review and meta-analysis. Dis Colon Rectum 2021; 64 (04) 484-496
    CrossrefPubMedGoogle Scholar
  • 16 Lewis-Lloyd CA, Crooks CJ, West J, Peacock O, Humes DJ. Time trends in the incidence rates of venous thromboembolism following colorectal resection by indication and operative technique. Colorectal Dis 2022; 24 (11) 1405-1415
    CrossrefPubMedGoogle Scholar
  • 17 Iannuzzi JC, Aquina CT, Rickles AS. et al. Risk factors for postdischarge venothromboembolism after colorectal resection. Dis Colon Rectum 2016; 59 (03) 224-229
    CrossrefPubMedGoogle Scholar
  • 18 Felder S, Rasmussen MS, King R. et al. Prolonged thromboprophylaxis with low molecular weight heparin for abdominal or pelvic surgery. Cochrane Database Syst Rev 2019; 8 (08) CD004318
    PubMedGoogle Scholar
  • 19 Fleming F, Gaertner W, Ternent CA. et al. The American Society of Colon and Rectal Surgeons clinical practice guideline for the prevention of venous thromboembolic disease in colorectal surgery. Dis Colon Rectum 2018; 61 (01) 14-20
    CrossrefPubMedGoogle Scholar
  • 20 Ageno W, Becattini C, Brighton T, Selby R, Kamphuisen PW. Cardiovascular risk factors and venous thromboembolism: a meta-analysis. Circulation 2008; 117 (01) 93-102
    CrossrefPubMedGoogle Scholar
  • 21 Tsai AW, Cushman M, Rosamond WD, Heckbert SR, Polak JF, Folsom AR. Cardiovascular risk factors and venous thromboembolism incidence: the longitudinal investigation of thromboembolism etiology. Arch Intern Med 2002; 162 (10) 1182-1189
    CrossrefPubMedGoogle Scholar
  • 22 den Exter PL, Woller SC, Robert-Ebadi H. et al. Management of bleeding risk in patients who receive anticoagulant therapy for venous thromboembolism: communication from the ISTH SSC Subcommittee on Predictive and Diagnostic Variables in Thrombotic Disease. J Thromb Haemost 2022; 20 (08) 1910-1919
    CrossrefPubMedGoogle Scholar
  • 23 Klok FA, Huisman MV. How I assess and manage the risk of bleeding in patients treated for venous thromboembolism. Blood 2020; 135 (10) 724-734
    CrossrefPubMedGoogle Scholar
  • 24 Baigent C, Blackwell L, Collins R. et al; Antithrombotic Trialists' (ATT) Collaboration. Aspirin in the primary and secondary prevention of vascular disease: collaborative meta-analysis of individual participant data from randomised trials. Lancet 2009; 373 (9678) 1849-1860
    CrossrefPubMedGoogle Scholar
  • 25 De Berardis G, Lucisano G, D'Ettorre A. et al. Association of aspirin use with major bleeding in patients with and without diabetes. JAMA 2012; 307 (21) 2286-2294
    CrossrefPubMedGoogle Scholar
  • 26 Selak V, Jackson R, Poppe K. et al. Predicting bleeding risk to guide aspirin use for the primary prevention of cardiovascular disease: a cohort study. Ann Intern Med 2019; 170 (06) 357-368
    CrossrefPubMedGoogle Scholar
  • 27 Raposeiras Roubín S, Abu Assi E, Muñoz Pousa I. et al. Incidence and predictors of bleeding in patients with cancer and atrial fibrillation. Am J Cardiol 2022; 167: 139-146
    CrossrefPubMedGoogle Scholar
  • 28 Gustafsson UO, Scott MJ, Hubner M. et al. Guidelines for perioperative care in elective colorectal surgery: Enhanced Recovery After Surgery (ERAS®) society recommendations: 2018. World J Surg 2019; 43 (03) 659-695
    CrossrefPubMedGoogle Scholar
  • 29 Vendler MMI, Haidari TA, Waage JE. et al; Copenhagen cOmplete Mesocolic Excision Study group (COMES). Incidence of venous thromboembolic events in enhanced recovery after surgery for colon cancer: a retrospective, population-based cohort study. Colorectal Dis 2017; 19 (11) O393-O401
    PubMedGoogle Scholar
  • 30 Carrier M, Altman AD, Blais N. et al. Extended thromboprophylaxis with low-molecular weight heparin (LMWH) following abdominopelvic cancer surgery. Am J Surg 2019; 218 (03) 537-550
    CrossrefPubMedGoogle Scholar
  • 31 Laugesen K, Ludvigsson JF, Schmidt M. et al. Nordic health registry-based research: a review of health care systems and key registries. Clin Epidemiol 2021; 13: 533-554
    CrossrefPubMedGoogle Scholar
  • 32 Schmidt M, Schmidt SA, Sandegaard JL, Ehrenstein V, Pedersen L, Sørensen HT. The Danish National Patient Registry: a review of content, data quality, and research potential. Clin Epidemiol 2015; 7: 449-490
    CrossrefPubMedGoogle Scholar
  • 33 Gjerstorff ML. The Danish cancer registry. Scand J Public Health 2011; 39 (7, Suppl): 42-45
    CrossrefPubMedGoogle Scholar
  • 34 Pottegård A, Schmidt SAJ, Wallach-Kildemoes H, Sørensen HT, Hallas J, Schmidt M. Data resource profile: the Danish National Prescription Registry. Int J Epidemiol 2017; 46 (03) 798-798f
    PubMedGoogle Scholar
  • 35 Isaksen AA, Sandbæk A, Bjerg L. Validation of register-based diabetes classifiers in Danish data. Clin Epidemiol 2023; 15: 569-581
    CrossrefPubMedGoogle Scholar
  • 36 Carstensen B, Rønn PF, Jørgensen ME. Prevalence, incidence and mortality of type 1 and type 2 diabetes in Denmark 1996-2016. BMJ Open Diabetes Res Care 2020; 8 (01) e001071
    CrossrefPubMedGoogle Scholar
  • 37 Zalfani J, Frøslev T, Olsen M. et al. Positive predictive value of the International Classification of Diseases, 10th edition diagnosis codes for anemia caused by bleeding in the Danish National Registry of Patients. Clin Epidemiol 2012; 4: 327-331
    PubMedGoogle Scholar
  • 38 Viborg S, Søgaard KK, Farkas DK, Nørrelund H, Pedersen L, Sørensen HT. Lower gastrointestinal bleeding and risk of gastrointestinal cancer. Clin Transl Gastroenterol 2016; 7 (04) e162
    CrossrefPubMedGoogle Scholar
  • 39 Schmidt M, Cannegieter SC, Johannesdottir SA, Dekkers OM, Horváth-Puhó E, Sørensen HT. Statin use and venous thromboembolism recurrence: a combined nationwide cohort and nested case-control study. J Thromb Haemost 2014; 12 (08) 1207-1215
    CrossrefPubMedGoogle Scholar
  • 40 Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987; 40 (05) 373-383
    CrossrefPubMedGoogle Scholar
  • 41 Latouche A, Allignol A, Beyersmann J, Labopin M, Fine JP. A competing risks analysis should report results on all cause-specific hazards and cumulative incidence functions. J Clin Epidemiol 2013; 66 (06) 648-653
    CrossrefPubMedGoogle Scholar
  • 42 Pearson-Stuttard J, Cheng YJ, Bennett J. et al. Trends in leading causes of hospitalisation of adults with diabetes in England from 2003 to 2018: an epidemiological analysis of linked primary care records. Lancet Diabetes Endocrinol 2022; 10 (01) 46-57
    CrossrefPubMedGoogle Scholar
  • 43 Sørensen HT, Pedersen L, van Es N, Büller HR, Horváth-Puhó E. Impact of venous thromboembolism on the mortality in patients with cancer: a population-based cohort study. Lancet Reg Health Eur 2023; 34: 100739
    CrossrefPubMedGoogle Scholar
  • 44 Schmidt M, Schmidt SAJ, Adelborg K. et al. The Danish health care system and epidemiological research: from health care contacts to database records. Clin Epidemiol 2019; 11: 563-591
    CrossrefPubMedGoogle Scholar
  • 45 Sundbøll J, Adelborg K, Munch T. et al. Positive predictive value of cardiovascular diagnoses in the Danish National Patient Registry: a validation study. BMJ Open 2016; 6 (11) e012832
    CrossrefPubMedGoogle Scholar
  • 46 Ingeholm P, Gögenur I, Iversen LH. Danish colorectal cancer group database. Clin Epidemiol 2016; 8: 465-468
    CrossrefPubMedGoogle Scholar
  • 47 Yland JJ, Wesselink AK, Lash TL, Fox MP. Misconceptions about misclassification: non-differential misclassification does not always bias results toward the null. Am J Epidemiol 2022; 191 (08) 1485-1495
    PubMedGoogle Scholar