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Increased risk of zoonotic Salmonella and Campylobacter gastroenteritis in patients with haematological malignancies: a population-based study

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We hypothesised that haematological malignancies increase the risk of acquiring zoonotic Salmonella or Campylobacter gastroenteritis. The population-based study comprised all first-time Salmonella/Campylobacter gastroenteritis cases in two Danish counties (1991–2003), with age- and gender-matched controls from the background population. We linked the study cohort to registries to obtain data on malignancies, chemotherapy (yes/no), and main comorbidities diagnosed before Salmonella/Campylobacter gastroenteritis. Based on this design, we determined incidence rate ratios (IRR) in conditional logistic regression analyses, and we used weighted mean regression curves to evaluate fluctuations in risk 0–5 years after the malignancy diagnosis. Sixty-eight of 13,324 cases (0.5%) and 29 of 26,648 controls (0.1%) had haematological malignancy before their Salmonella/Campylobacter gastroenteritis. Comorbidity-adjusted IRR for Salmonella/Campylobacter gastroenteritis in patients with haematological malignancy as compared to patients without malignancy were 4.46 [95% confidence intervals (CI), 2.88–6.90] for all individuals, 8.33 (95% CI, 4.31–16.1) for Salmonella, and 2.17 (95% CI, 1.15–4.08) for Campylobacter. Stratification on chemotherapy treatment did not change these estimates. In time-related analyses, IRR were 7–8 in the first 2 years after the haematological malignancy diagnosis and 4–5 in the following 3 years. Patients with haematological malignancy had increased long-term risk of enquiring Salmonella or Campylobacter gastroenteritis.

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  1. 1.

    Andersen TF, Madsen M, Jørgensen J, Mellemkjær L, Olsen JH (1999) The Danish National Hospital Register. A valuable source of data for modern health sciences. Dan Med Bull 46:263–268

  2. 2.

    Blaser MJ, Allos BM (2005) Campylobacter jejuni and related species. In: Mandell GL, Bennett JE, Dolin R (eds) Principles and practice of infectious diseases. Churchill Livingstone, Philadelphia, pp 2548–2557

  3. 3.

    Blom M, Meyer A, Gerner-Smidt P, Gaarslev K, Espersen F (1999) Evaluation of Statens Serum Institut enteric medium for detection of enteric pathogens. J Clin Microbiol 37:2312–2316

  4. 4.

    Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383 doi:10.1016/0021-9681(87)90171-8

  5. 5.

    Cherubin CE, Fodor T, Denmark LI, Master CS, Fuerst HT, Winter JW (1969) Symptoms, septicemia and death in salmonellosis. Am J Epidemiol 90:285–291

  6. 6.

    Cleveland WS (1993) Visualizing data. Hobart, Summit

  7. 7.

    Coburn B, Grassl GA, Finlay BB (2007) Salmonella, the host and disease: a brief review. Immunol Cell Biol 85:112–118 doi:10.1038/sj.icb.7100007

  8. 8.

    Danmarks Statistik (2004) Population statistics, Denmark. www.statistikbanken.dk (accessed 1 September 2007)

  9. 9.

    Delaloye J, Merlani G, Petignat C, Wenger A, Zaman K, Monnerat C, Matzinger O, Beck PM, Vuichard P, Ketterer N, Tarr PE (2004) Nosocomial nontyphoidal salmonellosis after antineoplastic chemotherapy: reactivation of asymptomatic colonization. Eur J Clin Microbiol Infect Dis 23:751–758 doi:10.1007/s10096-004-1206-5

  10. 10.

    Engberg J, On SL, Harrington CS, Gerner-Smidt P (2000) Prevalence of Campylobacter, Arcobacter, Helicobacter, and Sutterella spp. in human fecal samples as estimated by a reevaluation of isolation methods for Campylobacters. J Clin Microbiol 38:286–291

  11. 11.

    Fernandez LA, MacSween JM, Langley GR (1983) Immunoglobulin secretory function of B cells from untreated patients with chronic lymphocytic leukemia and hypogammaglobulinemia: role of T cells. Blood 62:767–774

  12. 12.

    Gradel KO, Dethlefsen C, Schønheyder HC, Ejlertsen T, Sørensen HT, Thomsen RW, Nielsen H (2007) Severity of infection and seasonal variation of non-typhoid Salmonella occurrence in humans. Epidemiol Infect 135:93–99 doi:10.1017/S0950268806006686

  13. 13.

    Gruenewald R, Blum S, Chan J (1994) Relationship between human immunodeficiency virus infection and salmonellosis in 20- to 59-year-old residents of New York City. Clin Infect Dis 18:358–363

  14. 14.

    Han T, Sokal JE, Neter E (1967) Salmonellosis in disseminated malignant diseases. A seven-year review (1959–1965). N Engl J Med 276:1045–1052

  15. 15.

    Heineman HS, Jensen WN, Cooper WM, Braude AI (1964) Hodgin’s disease and Salmonella Typhimurium infection. JAMA 188:632–634

  16. 16.

    Hsu RB, Chen RJ, Chu SH (2005) Nontyphoid Salmonella bacteremia in patients with liver cirrhosis. Am J Med Sci 329:234–237 doi:10.1097/00000441-200505000-00004

  17. 17.

    Hung CC, Hung MN, Hsueh PR, Chang SY, Chen MY, Hsieh SM, Sheng WH, Sun HY, Huang YT, Lo YC, Hsiao CF, Chang SC (2007) Risk of recurrent nontyphoid Salmonella bacteremia in HIV-infected patients in the era of highly active antiretroviral therapy and an increasing trend of fluoroquinolone resistance. Clin Infect Dis 45:e60–e67 doi:10.1086/520681

  18. 18.

    Kosmaczewska A, Frydecka I, Bocko D, Ciszak L, Teodorowska R (2002) Correlation of blood lymphocyte CTLA-4 (CD152) induction in Hodgkin’s disease with proliferative activity, interleukin 2 and interferon-gamma production. Br J Haematol 118:202–209 doi:10.1046/j.1365-2141.2002.03572.x

  19. 19.

    Lecuit M, Abachin E, Martin A, Poyart C, Pochart P, Suarez F, Bengoufa D, Feuillard J, Lavergne A, Gordon JI, Berche P, Guillevin L, Lortholary O (2004) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med 350:239–248 doi:10.1056/NEJMoa031887

  20. 20.

    Lievonen S, Havulinna AS, Maiala R (2004) Egg consumption patterns and Salmonella risk in Finland. J Food Prot 67:2416–2423

  21. 21.

    Nagai H, Fisher RI, Cossman J, Oppenheim JJ (1986) Decreased expression of class II major histocompatibility antigens on monocytes from patients with Hodgkin’s disease. J Leukoc Biol 39:313–321

  22. 22.

    Noriega LM, Van der AP, Daneau D, Meunier F, Aoun M (1994) Salmonella infections in a cancer center. Support Care Cancer 2:116–122 doi:10.1007/BF00572093

  23. 23.

    Novak R, Feldman S (1979) Salmonellosis in children with cancer: review of 42 cases. Am J Dis Child 133:298–300

  24. 24.

    Pedersen CB, Gøtzsche H, Møller JO, Mortensen PB (2006) The Danish Civil Registration System. A cohort of eight million persons. Dan Med Bull 53:441–449

  25. 25.

    Popoff MY, Le Minor L (1997) Antigenic formulas of the Salmonella serovars. WHO Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur, Paris, France

  26. 26.

    Rothman KJ (2002) Epidemiology: an introduction. Oxford University Press, Oxford, UK

  27. 27.

    Saeed AM, Gast RK, Potter ME, Wall PG (1999) Salmonella enterica serovar Enteritidis in humans and animals—epidemiology, pathogenesis, and control. Iowa State University Press, Ames, Iowa

  28. 28.

    Simonsen J, Strid MA, Mølbak K, Krogfelt KA, Linneberg A, Teunis P (2008) Sero-epidemiology as a tool to study the incidence of Salmonella infections in humans. Epidemiol Infect 136:895–902 doi:10.1017/S0950268807009314

  29. 29.

    Sinkovics JG, Smith JP (1969) Salmonellosis complicating neoplastic diseases. Cancer 24:631–636 doi:10.1002/1097-0142(196909)24:3<631::AID-CNCR2820240331>3.0.CO;2-J

  30. 30.

    Sørensen HT (1997) Regional administrative health registries as a resource in clinical epidemiology. Int J Risk Saf Med 10:1–22

  31. 31.

    Sorvillo FJ, Lieb LE, Waterman SH (1991) Incidence of campylobacteriosis among patients with AIDS in Los Angeles County. J Acquir Immune Defic Syndr 4:598–602

  32. 32.

    Storm HH, Michelsen EV, Clemmensen IH, Pihl J (1997) The Danish Cancer Registry—history, content, quality and use. Dan Med Bull 44:535–539

  33. 33.

    Ternhag A, Torner A, Ekdahl K, Giesecke J (2006) Salmonella-associated deaths, Sweden, 1997–2003. Emerg Infect Dis 12:337–339

  34. 34.

    Twomey JJ, Laughter AH, Rice L, Ford R (1980) Spectrum of immunodeficiencies with Hodgkin’s disease. J Clin Invest 66:629–637 doi:10.1172/JCI109898

  35. 35.

    Voetsch AC, Van Gilder TJ, Angulo FJ, Farley MM, Shallow S, Marcus R, Cieslak PR, Deneen VC, Tauxe RV (2004) FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 38(Suppl 3):S127–S134 doi:10.1086/381578

  36. 36.

    Wacholder S, Silverman DT, McLaughlin JK, Mandel JS (1992) Selection of controls in case–control studies. III. Design options. Am J Epidemiol 135:1042–1050

  37. 37.

    Wheeler JG, Sethi D, Cowden JM, Wall PG, Rodrigues LC, Tompkins DS, Hudson MJ, Roderick PJ (1999) Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. The Infectious Intestinal Disease Study Executive. BMJ 318:1046–1050

  38. 38.

    Wolfe MS, Louria DB, Armstrong D, Blevins A (1971) Salmonellosis in patients with neoplastic disease. A review of 100 episodes at Memorial Cancer Center over a 13-year period. Arch Intern Med 128:546–554 doi:10.1001/archinte.128.4.546

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This study was financed by Det Obelske Familiefond, Aase og Ejnar Danielsens Fond, Eva og Henry Frænkels Mindefond and Nordjyllands Lægekredsforenings Forskningsfond.

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Correspondence to Kim O. Gradel.

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Gradel, K.O., Nørgaard, M., Dethlefsen, C. et al. Increased risk of zoonotic Salmonella and Campylobacter gastroenteritis in patients with haematological malignancies: a population-based study. Ann Hematol 88, 761–767 (2009). https://doi.org/10.1007/s00277-008-0662-x

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  • Haematologic neoplasms
  • Salmonella food poisoning
  • Campylobacter infections
  • Gastroenteritis