Abstract
Bloodstream nontyphoidal salmonella (NTS) infection is rare, but its associated characteristics and microbiological features in immunocompromised patients are worth paying attention to, particularly for those receiving allogeneic hematopoietic stem cell transplantation (SCT). No studies so far have analyzed post-transplant bloodstream NTS infection. Therefore, we reviewed 423 adult patients undergoing allogeneic hematopoietic SCT from 2003 to 2014. Nine out of four hundred twenty-three patients (2.13%) developed post-transplant bloodstream NTS infection, including two patients who had subsequent or combined metastatic infections. The median age at SCT was 35 years (interquartile range, 29–46) among the nine patients with bloodstream NTS infection. Male patients were predominant (78%). The median onset of bloodstream NTS infection was at 315 days after SCT (range, 207–629). Multivariate analysis revealed that extensive chronic graft-versus-host disease (GVHD) (OR 8.054, p = 0.003) and nonmyeloablative transplant conditioning (OR 4.604, p = 0.037) were significant associated characteristics for NTS infection. Currently, there are no published data analyzing and exploring post-transplant bloodstream NTS infections in adult allogeneic hematopoietic SCT. Our study determined the associated characteristics and microbiological features for this infection.
Similar content being viewed by others
References
Appelbaum FR (2007) Hematopoietic-cell transplantation at 50. N Engl J Med 357:1472–1475
Kang G, Srivastava A, Pulimood AB, Dennison D, Chandy M (2002) Etiology of diarrhea in patients undergoing allogeneic bone marrow transplantation in South India. Transplantation 73:1247–1251
Styczynski J, Czyzewski K, Wysocki M, Gryniewicz-Kwiatkowska O, Kolodziejczyk-Gietka A, Salamonowicz M, Hutnik L, Zajac-Spychala O, Zaucha-Prazmo A, Chelmecka-Wiktorczyk L et al (2016) Increased risk of infections and infection-related mortality in children undergoing haematopoietic stem cell transplantation compared to conventional anticancer therapy: a multicentre nationwide study. Clin Microbiol Infect. doi:10.1016/j.cmi.2015.10.017
Mosaad YM (2014) Immunology of hematopoietic stem cell transplant. Immunol Investig 43:858–887
Stuehler C, Kuenzli E, Jaeger VK, Baettig V, Ferracin F, Rajacic Z, Kaiser D, Bernardini C, Forrer P, Weisser M, Elzi L, Battegay M, Halter J, Passweg J, Khanna N (2015) Immune reconstitution after allogeneic hematopoietic stem cell transplantation and association with occurrence and outcome of invasive aspergillosis. J Infect Dis 212:959–967
Liu YC, Chien SH, Fan NW, Hu MH, Gau JP, Liu CJ, Yu YB, Liu CY, Hsiao LT, Liu JH, Chiou TJ, Tzeng CH (2015) Risk factors for pericardial effusion in adult patients receiving allogeneic haematopoietic stem cell transplantation. Br J Haematol 169:737–745
Mikulska M, Del Bono V, Viscoli C (2014) Bacterial infections in hematopoietic stem cell transplantation recipients. Curr Opin Hematol 21:451–458
Thomas ED, Storb R, Clift RA, Fefer A, Johnson L, Neiman PE, Lerner KG, Glucksberg H, Buckner CD (1975) Bone-marrow transplant. N Engl J Med 292:895–902
Filipovich AH, Weisdorf D, Pavletic S, Socie G, Wingard JR, Lee SJ, Martin P, Chien J, Przepiorka D, Couriel D, Cowen EW, Dinndorf P, Farrell A, Hartzman R, Henslee-Downey J, Jacobsohn D, McDonald G, Mittleman B, Rizzo JD, Robinson M, Schubert M, Schultz K, Shulman H, Turner M, Vogelsang G, Flowers ME (2005) National Institutes of Health consensus development project on criteria for clinical trials in chronic graft-versus-host disease: I. Diagnosis and staging working group report. Biol Blood Marrow Transplant 11:945–956
Schwartz S, Vergoulidou M, Schreier E, Loddenkemper C, Reinwald M, Schmidt-Hieber M, Flegel WA, Thiel E, Schneider T (2011) Norovirus gastroenteritis causes severe and lethal complications after chemotherapy and hematopoietic stem cell transplantation. Blood 117:5850–5856
Boyle NM, Podczervinski S, Jordan K, Stednick Z, Butler-Wu S, McMillen K, Pergam SA (2014) Bacterial foodborne infections after hematopoietic cell transplantation. Biol Blood Marrow Transplant 20:1856–1861
Maki DG (2009) Coming to grips with foodborne infection—peanut butter, peppers and nationwide salmonella outbreaks. N Engl J Med 360:949–953
Woc-Colburn L, Bobak DA (2009) The expanding spectrum of disease due to Salmonella: an international perspective. Curr Infect Dis Rep 11:120–124
Majwicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal salmonella gastroenteritis. Clin Infect Dis 50:882–889
Medalla F, Hoekstra RM, Whichard JM, Barzilay EJ, Chiller TM, Joyce K, Rickert R, Krueger A, Stuart A, Griffin PM (2013) Increase in resistance to ceftriaxone and nonsusceptibility to ciprofloxacin and decrease in multidrug resistance among salmonella strains, United States, 1996-2009. Foodborne Pathog Dis 10:302–309
Gordon MA (2008) Salmonella infections in immunocompromised adults. J Inf Secur 56:413–422
Dadwal SS, Tegtmeier B, Nakamura R, Kriengkauykiat J, Ito J, Forman SJ, Pullarkat V (2011) Nontyphoidal salmonella infection among recipients of hematopoietic SCT. Bone Marrow Transplant 46:880–883
Dhanoa A, Fatt QK (2009) Non-typhoidal salmonella bacteraemia: epidemiology, clinical characteristics and its’ association with severe immunosuppression. Ann Clin Microbiol Antimicrob 8:15
Shaikh ZH, Ueno NT, Kontoyiannis DP (2001) Fatal salmonella group G enteritis mimicking intestinal graft-versus-host disease in a bone marrow transplant recipient. Transpl Infect Dis 3:29–33
Brown M, Eykyn SJ (2000) Non-typhoidal salmonella bacteremia without gastroenteritis: a marker of underlying immunosuppression: review of cases at St Thomas’ hospital 1970–1999. J Inf Secur 41:256–259
Matsubara H, Kobayashi M, Tokumasu M, Nakanishi H, Miyazaki M, Mizushima Y, Hiramatsu H, Adachi S, Nakayama T, Onishi E, Nakahata T (2006) Salmonella enteritidis septic arthritis after allogeneic peripheral blood stem cell transplantation. Leuk Lymphoma 47:1435–1437
Hsu RB, Chen RJ, Chu SH (2004) Risk factors for recurrent bacteremia in adult patients with nontyphoid salmonellosis. Am J Med Sci 328:315–318
Slavin S, Nagler A, Naparstek E, Kapelushnik Y, Aker M, Cividalli G, Varadi G, Kirschbaum M, Ackerstein A, Samuel S, Amar A, Brautbar C, Ben-Tal O, Eldor A, Or R (1998) Nonmyeloablative stem cell transplantation and cell therapy as an alternative to conventional bone marrow transplantation with lethal cytoreduction for the treatment of malignant and nonmalignant hematologic diseases. Blood 91:756–763
Mielcarek M, Martin PJ, Leisenring W, Flowers ME, Maloney DG, Sandmaier BM, Maris MB, Storb R (2003) Graft-versus-host disease after nonmyeloablative versus conventional hematopoietic stem cell transplantation. Blood 102:756–762
Holtick U, Albrecht M, Chemnitz JM, Theurich S, Shimabukuro-Vornhagen A, Skoetz N, Scheid C, von Bergwelt-Baildon M (2015) Comparison of bone marrow versus peripheral blood allogeneic hematopoietic stem cell transplantation for hematological malignancies in adults—a systematic review and meta-analysis. Crit Rev Oncol Hematol 94:179–188
Yang CH, Tseng HH, Chen KJ, Liu JD (1996) Salmonella infections: a retrospective 10-year analysis of 134 cases in a regional hospital in Taiwan. Scand J Infect Dis 28:171–175
Hohmann EL (2001) Nontyphoidal salmonellosis. Clin Infect Dis 32:263–269
Wang JY, Hwang JJ, Hsu CN, Lin LC, Hsueh PR (2006) Bacteraemia due to ciprofloxacin-resistant Salmonella enterica serotype Choleraesuis in adult patients at a university hospital in Taiwan, 1996-2004. Epidemiol Infect 134:977–984
Acknowledgments
This work was partially supported by grants from the Taipei Veterans General Hospital (V104B-023), the Taiwan Clinical Oncology Research Foundation, the Szu-Yuan Research Foundation of Internal Medicine, and the Chong Hin Loon Memorial Cancer and Biotherapy Research Center, National Yang-Ming University. The funding sources had no role in the study design or conduct or in the decision to submit it for publication.
Author information
Authors and Affiliations
Contributions
Y-CL, P-SK, H-YW, and C-YW had full access to all of the data in the study and take responsibility for the integrity of the data. Y-CL and P-SK wrote the manuscript. P-SK, H-YW, C-YW, Y-CL, and N-WF analyzed the data. J-PG, C-JL, Y-BY, L-TH, T-JC, C-HT, and J-HL finally confirmed the complete data and manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The retrospective review of medical records was approved by the institutional ethical committee in agreement with the Helsinki Declaration of 1975, revised in 2008. For this type of study, formal consent is not required.
Electronic supplementary material
ESM 1
(DOCX 15 kb)
Rights and permissions
About this article
Cite this article
Ko, PS., Liu, YC., Wang, HY. et al. Clinical-associated characteristics and microbiological features of bloodstream nontyphoidal salmonella infection in adult patients receiving allogeneic hematopoietic stem cell transplantation. Ann Hematol 96, 1533–1540 (2017). https://doi.org/10.1007/s00277-017-3054-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00277-017-3054-2