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Thromb Haemost 2023; 123(12): 1165-1176
DOI: 10.1055/s-0042-1759879
Stroke, Systemic or Venous Thromboembolism

Increased Cancer Risk in Patients with Kidney Disease and Venous Thromboembolism: A Population-Based Cohort Study

Jakob Rønnow Sand 
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
,
Frederikke Schønfeldt Troelsen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
,
Dávid Nagy
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
,
Dóra Körmendiné Farkas
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
,
Rune Erichsen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
2   Department of Surgery, Randers Regional Hospital, Randers NØ, Denmark
,
Christian Fynbo Christiansen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
,
Henrik Toft Sørensen
1   Department of Clinical Epidemiology, Aarhus University Hospital and Clinical Institute of Arhus University, Aarhus N, Denmark
› Author Affiliations Funding This work was supported by Aarhus University. The sponsor had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Abstract

Background Venous thromboembolism (VTE) may be a harbinger of cancer in the general population. Patients with kidney disease have an a priori increased VTE risk. However, it remains unknown how a VTE affects subsequent cancer risk in these patients.

Objectives To examine the cancer risk in patients with kidney disease following a VTE.

Methods We conducted a nationwide population-based cohort study in Denmark (1996–2017), including all VTE patients with a diagnosis of kidney disease. We calculated absolute risks of cancer (accounting for competing risk of death) and age-, sex-, and calendar-period standardized incidence ratios (SIRs) comparing the observed cancer incidence with national cancer incidence rates and cancer incidence rates of VTE patients without kidney disease.

Results We followed 3,362 VTE patients with kidney disease (45.9% females) for a median follow-up time of 2.4 years (interquartile range: 0.6–5.4). During follow-up, 464 patients were diagnosed with cancer, of whom 169 (36.4%) were diagnosed within the first year. The 1-year absolute risk of any cancer was 5.0% (95% confidence interval [CI]: 4.3–5.8), with a SIR of 2.9 (95% CI: 2.5–3.4) when compared with the general population, and 2.0 (95% CI: 1.8–2.4) when compared with VTE patients without kidney disease. During subsequent years of follow-up, the SIRs declined to 1.5 (95% CI: 1.3–1.6) when compared with the general population, and 1.1 (95% CI: 0.9–1.2) compared with VTE patients without kidney disease.

Conclusion Patients with hospital-diagnosed kidney disease have increased cancer risk after VTE, especially within the first year following the VTE diagnosis.

Keywords

venous thromboembolism - deep vein thrombosis - pulmonary embolism - kidney disease - cancer - epidemiology - cohort study

Authors' Contribution

All authors contributed to the methodology of the study. H.T.S. acquired the data. J.R.S., F.S.T., R.E., C.F.C., and H.T.S. directed the formal analyses, which were performed by D.N. and D.K.F. J.R.S. and F.S.T. wrote the initial draft. All authors contributed to the discussion and interpretation of the results, which secured the intellectual content of the manuscript. All authors reviewed, edited, and approved the final version of the manuscript for submission.


Data Availability Statement

All data generated or analyzed during this study are included in this published article (and in the Supplementary Material). All authors had full access to the data of this study.


Supplementary Material



Publication History

Received: 05 January 2022

Accepted: 18 October 2022

Article published online:
27 December 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

Comment to this article:

Kidney Disease and Cancer Risk in Patients with Venous Thromboembolism: What Does It Mean for Clinical Practice?Thromb Haemost 2023; 123(12): 1177-1179
DOI: 10.1055/a-2152-4762

 

  • References

  • 1 Trousseau A. Lectures on Clinical Medicine. Delivered at the Hotel-Dieu, Paris. In: Cormack JR. ed. London: New Sydenham Society; 1872: 281-295
    Google Scholar
  • 2 Goldhaber SZ, Bounameaux H. Pulmonary embolism and deep vein thrombosis. Lancet 2012; 379 (9828): 1835-1846
    CrossrefPubMedGoogle Scholar
  • 3 Qureshi W, Ali Z, Amjad W. et al. Venous thromboembolism in cancer: an update of treatment and prevention in the era of newer anticoagulants. Front Cardiovasc Med 2016; 3: 24
    CrossrefPubMedGoogle Scholar
  • 4 Di Nisio M, van Es N, Büller HR. Deep vein thrombosis and pulmonary embolism. Lancet 2016; 388 (10063): 3060-3073
    CrossrefPubMedGoogle Scholar
  • 5 Sørensen HT, Mellemkjaer L, Steffensen FH, Olsen JH, Nielsen GL. The risk of a diagnosis of cancer after primary deep venous thrombosis or pulmonary embolism. N Engl J Med 1998; 338 (17) 1169-1173
    CrossrefPubMedGoogle Scholar
  • 6 Baron JA, Gridley G, Weiderpass E, Nyrén O, Linet M. Venous thromboembolism and cancer. Lancet 1998; 351 (9109): 1077-1080
    CrossrefPubMedGoogle Scholar
  • 7 Murchison JT, Wylie L, Stockton DL. Excess risk of cancer in patients with primary venous thromboembolism: a national, population-based cohort study. Br J Cancer 2004; 91 (01) 92-95
    CrossrefPubMedGoogle Scholar
  • 8 Sørensen HT, Sværke C, Farkas DK. et al. Superficial and deep venous thrombosis, pulmonary embolism and subsequent risk of cancer. Eur J Cancer 2012; 48 (04) 586-593
    CrossrefPubMedGoogle Scholar
  • 9 Sørensen HT, Mellemkjaer L, Olsen JH, Baron JA. Prognosis of cancers associated with venous thromboembolism. N Engl J Med 2000; 343 (25) 1846-1850
    CrossrefPubMedGoogle Scholar
  • 10 Christiansen CF, Onega T, Sværke C. et al. Risk and prognosis of cancer in patients with nephrotic syndrome. Am J Med 2014; 127 (09) 871.e1-877.e1
    CrossrefPubMedGoogle Scholar
  • 11 Birkeland SA, Storm HH. Glomerulonephritis and malignancy: a population-based analysis. Kidney Int 2003; 63 (02) 716-721
    CrossrefPubMedGoogle Scholar
  • 12 Heaf JG, Hansen A, Laier GH. Hypertensive nephropathy is associated with an increased risk of myeloma, skin, and renal cancer. J Clin Hypertens (Greenwich) 2019; 21 (06) 786-791
    CrossrefPubMedGoogle Scholar
  • 13 Yu TM, Chuang YW, Yu MC. et al. Risk of cancer in patients with polycystic kidney disease: a propensity-score matched analysis of a nationwide, population-based cohort study. Lancet Oncol 2016; 17 (10) 1419-1425
    CrossrefPubMedGoogle Scholar
  • 14 Cheung CY, Ma MKM, Chak WL, Tang SCW. Cancer risk in patients with diabetic nephropathy: a retrospective cohort study in Hong Kong. Medicine (Baltimore) 2017; 96 (38) e8077
    CrossrefPubMedGoogle Scholar
  • 15 Tveit DP, Hypolite IO, Hshieh P. et al. Chronic dialysis patients have high risk for pulmonary embolism. Am J Kidney Dis 2002; 39 (05) 1011-1017
    CrossrefPubMedGoogle Scholar
  • 16 Wattanakit K, Cushman M, Stehman-Breen C, Heckbert SR, Folsom AR. Chronic kidney disease increases risk for venous thromboembolism. J Am Soc Nephrol 2008; 19 (01) 135-140
    CrossrefPubMedGoogle Scholar
  • 17 Kayali F, Najjar R, Aswad F, Matta F, Stein PD. Venous thromboembolism in patients hospitalized with nephrotic syndrome. Am J Med 2008; 121 (03) 226-230
    CrossrefPubMedGoogle Scholar
  • 18 Hippisley-Cox J, Coupland C. Development and validation of risk prediction algorithm (QThrombosis) to estimate future risk of venous thromboembolism: prospective cohort study. BMJ 2011; 343: d4656
    CrossrefPubMedGoogle Scholar
  • 19 Mahmoodi BK, Gansevoort RT, Næss IA. et al. Association of mild to moderate chronic kidney disease with venous thromboembolism: pooled analysis of five prospective general population cohorts. Circulation 2012; 126 (16) 1964-1971
    CrossrefPubMedGoogle Scholar
  • 20 Christiansen CF, Schmidt M, Lamberg AL. et al. Kidney disease and risk of venous thromboembolism: a nationwide population-based case-control study. J Thromb Haemost 2014; 12 (09) 1449-1454
    CrossrefPubMedGoogle Scholar
  • 21 Heaf JG, Hansen A, Laier GH. Quantification of cancer risk in glomerulonephritis. BMC Nephrol 2018; 19 (01) 27
    CrossrefPubMedGoogle Scholar
  • 22 Prandoni P, Lensing AW, Büller HR. et al. Deep-vein thrombosis and the incidence of subsequent symptomatic cancer. N Engl J Med 1992; 327 (16) 1128-1133
    CrossrefPubMedGoogle Scholar
  • 23 Sørensen GV, Erichsen R, Svaerke C, Farkas DK, Sørensen HT. Risk of cancer in patients with inflammatory bowel disease and venous thromboembolism: a nationwide cohort study. Inflamm Bowel Dis 2012; 18 (10) 1859-1863
    CrossrefPubMedGoogle Scholar
  • 24 Montomoli J, Erichsen R, Søgaard KK, Körmendiné Farkas D, Bloch Münster AM, Sørensen HT. Venous thromboembolism and subsequent risk of cancer in patients with liver disease: a population-based cohort study. BMJ Open Gastroenterol 2015; 2 (01) e000043
    CrossrefPubMedGoogle Scholar
  • 25 Christensen DH, Horváth-Puhó E, Thomsen RW. et al. Venous thromboembolism and risk of cancer in patients with diabetes mellitus. J Diabetes Complications 2016; 30 (04) 603-607
    CrossrefPubMedGoogle Scholar
  • 26 Pedersen AB, Vandenbroucke J, Horváth-Puhó E, Sørensen HT. Venous thromboembolism and risk of cancer in patients with rheumatoid arthritis. J Thromb Haemost 2017; 15 (12) 2325-2332
    CrossrefPubMedGoogle Scholar
  • 27 Schmidt M, Pedersen L, Sørensen HT. The Danish Civil Registration System as a tool in epidemiology. Eur J Epidemiol 2014; 29 (08) 541-549
    CrossrefPubMedGoogle Scholar
  • 28 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
  • 29 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
  • 30 Gjerstorff ML. The Danish Cancer Registry. Scand J Public Health 2011; 39 (7, Suppl): 42-45
    CrossrefPubMedGoogle Scholar
  • 31 Severinsen MT, Kristensen SR, Overvad K, Dethlefsen C, Tjønneland A, Johnsen SP. Venous thromboembolism discharge diagnoses in the Danish National Patient Registry should be used with caution. J Clin Epidemiol 2010; 63 (02) 223-228
    CrossrefPubMedGoogle Scholar
  • 32 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
  • 33 Danish National Board of Health. Annual Cancer Report. 2018. Accessed November 13, 2020 at: https://sundhedsdatastyrelsen.dk/-/media/sds/filer/find-tal-og-analyser/sygdomme/cancerregisteret/kraefttilfaelde-2018.pdf
    PubMed
  • 34 Heit JA, Spencer FA, White RH. The epidemiology of venous thromboembolism. J Thromb Thrombolysis 2016; 41 (01) 3-14
    CrossrefPubMedGoogle Scholar
  • 35 Thygesen SK, Christiansen CF, Christensen S, Lash TL, Sørensen HT. The predictive value of ICD-10 diagnostic coding used to assess Charlson comorbidity index conditions in the population-based Danish National Registry of Patients. BMC Med Res Methodol 2011; 11: 83
    CrossrefPubMedGoogle Scholar
  • 36 Breslow NE, Day NE. Statistical methods in cancer research. Volume II–the design and analysis of cohort studies. IARC Sci Publ 1987; (82) 1-406
    PubMedGoogle Scholar
  • 37 Cheung CY, Tang SCW. An update on cancer after kidney transplantation. Nephrol Dial Transplant 2019; 34 (06) 914-920
    CrossrefPubMedGoogle Scholar
  • 38 Komaki Y, Komaki F, Micic D, Ido A, Sakuraba A. Risk of colorectal cancer in chronic kidney disease: a systematic review and meta-analysis. J Clin Gastroenterol 2018; 52 (09) 796-804
    CrossrefPubMedGoogle Scholar
  • 39 Lin HF, Li YH, Wang CH, Chou CL, Kuo DJ, Fang TC. Increased risk of cancer in chronic dialysis patients: a population-based cohort study in Taiwan. Nephrol Dial Transplant 2012; 27 (04) 1585-1590
    CrossrefPubMedGoogle Scholar
  • 40 Hortlund M, Arroyo Mühr LS, Storm H, Engholm G, Dillner J, Bzhalava D. Cancer risks after solid organ transplantation and after long-term dialysis. Int J Cancer 2017; 140 (05) 1091-1101
    CrossrefPubMedGoogle Scholar
  • 41 Robertson L, Yeoh SE, Broderick C, Stansby G, Agarwal R. Effect of testing for cancer on cancer- or venous thromboembolism (VTE)-related mortality and morbidity in people with unprovoked VTE. Cochrane Database Syst Rev 2018; 11 (11) CD010837
    PubMedGoogle Scholar
  • 42 Vestergaard SV, Christiansen CF, Thomsen RW, Birn H, Heide-Jørgensen U. Identification of patients with CKD in medical databases: a comparison of different algorithms. Clin J Am Soc Nephrol 2021; 16 (04) 543-551
    CrossrefPubMedGoogle Scholar
  • 43 Lowrance WT, Ordoñez J, Udaltsova N, Russo P, Go AS. CKD and the risk of incident cancer. J Am Soc Nephrol 2014; 25 (10) 2327-2334
    CrossrefPubMedGoogle Scholar
  • 44 Jones ME, Swerdlow AJ. Bias in the standardized mortality ratio when using general population rates to estimate expected number of deaths. Am J Epidemiol 1998; 148 (10) 1012-1017
    CrossrefPubMedGoogle Scholar