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Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Predictive implications of albumin and C-reactive protein for progression to pneumonia and poor prognosis in Stenotrophomonas maltophilia bacteremia following allogeneic hematopoietic stem cell transplantation

Authors: Kaito Harada, Noritaka Sekiya, Tatsuya Konishi, Akihito Nagata, Yuta Yamada, Toshiaki Takezaki, Satoshi Kaito, Shuhei Kurosawa, Masahiro Sakaguchi, Shunichiro Yasuda, Shugo Sasaki, Kosuke Yoshioka, Kyoko Watakabe-Inamoto, Aiko Igarashi, Yuho Najima, Takeshi Hagino, Hideharu Muto, Takeshi Kobayashi, Noriko Doki, Kazuhiko Kakihana, Hisashi Sakamaki, Kazuteru Ohashi

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

Stenotrophomonas maltophilia (S. maltophilia) bacteremia causes significant morbidity and mortality in immunocompromised hosts. However, incidence and risk factors for mortality in S. maltophilia bacteremia following allogeneic hematopoietic stem cell transplantation (allo-HSCT) remain controversial. The primary aim of this study is to clarify factors associated with poor prognosis of allo-HSCT recipients with S. maltophilia bacteremia.

Methods

From January 2005 to December 2014, patients with hematological diseases and S. maltophilia bacteremia at a single transplantation center in Japan were examined for incidence and 90-day mortality. Prognostic factors associated with 90-day mortality among allo-HSCT recipients were analyzed by log-rank test, and significant variables in the univariate analysis were included in the multivariate Cox proportional-hazards regression model.

Results

A total of 65 patients, including 47 patients undergoing allo-HSCT, developed S. maltophilia bacteremia. The incidence of S. maltophilia bacteremia was significantly higher in allo-HSCT recipients compared to patients not receiving allo-HSCT (6.53 vs. 0.36 per 100 admissions, respectively; p < 0.01). The overall 90-day mortality in allo-HSCT recipients was 43%. Independent risk factors for 90-day mortality were low serum albumin (<3.0 g/dl) (HR = 10.86; 95% CI, 3.27–36.12) and high serum C-reactive protein (CRP) (≥10.0 mg/dl) (HR = 3.28; 95% CI, 1.00–10.72). Among 9 patients with both high CRP and low albumin, 5 had pneumonia at the onset of bacteremia and the remaining 4 patients developed pneumonia in a median of 3 days (range, 1 to 8 days) even under effective treatment. All 9 patients eventually died in a median of 2 days (range, 2 to 32 days). The probabilities of developing pneumonia in patients with or without high CRP and low albumin levels were 100% (9/9) and 10.5% (4/38), respectively (p < 0.01).

Conclusions

Allo-HSCT recipients had higher rates of S. maltophilia bacteremia than did patients not receiving allo-HSCT. High serum CRP and low serum albumin at the onset of bacteremia are predictive of disease progression to pneumonia and poor prognosis.
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Literature
1.
go back to reference Denton M, Kerr KG. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev. 1998;11:57–80.PubMedPubMedCentral Denton M, Kerr KG. Microbiological and clinical aspects of infection associated with Stenotrophomonas maltophilia. Clin Microbiol Rev. 1998;11:57–80.PubMedPubMedCentral
3.
go back to reference Al-Anazi KA, Al-Jasser AM. Infections caused by Stenotrophomonas maltophilia in recipients of hematopoietic stem cell transplantation. Front Oncol. 2014;4:232.PubMedPubMedCentral Al-Anazi KA, Al-Jasser AM. Infections caused by Stenotrophomonas maltophilia in recipients of hematopoietic stem cell transplantation. Front Oncol. 2014;4:232.PubMedPubMedCentral
4.
go back to reference Safdar A, Rolston KV. Stenotrophomonas maltophilia: changing spectrum of a serious bacterial pathogen in patients with cancer. Clin Infect Dis. 2007;45:1602–9.CrossRefPubMed Safdar A, Rolston KV. Stenotrophomonas maltophilia: changing spectrum of a serious bacterial pathogen in patients with cancer. Clin Infect Dis. 2007;45:1602–9.CrossRefPubMed
5.
go back to reference Chaplow R, Palmer B, Heyderman R, Moppett J, Marks DI. Stenotrophomonas maltophilia bacteraemia in 40 haematology patients: risk factors, therapy and outcome. Bone Marrow Transplant. 2010;45:1109–10. Chaplow R, Palmer B, Heyderman R, Moppett J, Marks DI. Stenotrophomonas maltophilia bacteraemia in 40 haematology patients: risk factors, therapy and outcome. Bone Marrow Transplant. 2010;45:1109–10.
6.
go back to reference Demiraslan H, Sevim M, Pala Ç, Durmaz S, Berk V, Kaynar L, et al. Risk factors influencing mortality related to Stenotrophomonas maltophilia infection in hematology-oncology patients. Int J Hematol. 2013;97:414–20.CrossRefPubMed Demiraslan H, Sevim M, Pala Ç, Durmaz S, Berk V, Kaynar L, et al. Risk factors influencing mortality related to Stenotrophomonas maltophilia infection in hematology-oncology patients. Int J Hematol. 2013;97:414–20.CrossRefPubMed
7.
go back to reference Tada K, Kurosawa S, Hiramoto N, Okinaka K, Ueno N, Asakura Y, et al. Stenotrophomonas maltophilia infection in hematopoietic SCT recipients: high mortality due to pulmonary hemorrhage. Bone Marrow Transplant. 2013;48:74–9. Tada K, Kurosawa S, Hiramoto N, Okinaka K, Ueno N, Asakura Y, et al. Stenotrophomonas maltophilia infection in hematopoietic SCT recipients: high mortality due to pulmonary hemorrhage. Bone Marrow Transplant. 2013;48:74–9.
8.
go back to reference Araoka H, Fujii T, Izutsu K, Kimura M, Nishida A, Ishiwata K, et al. Rapidly progressive fatal hemorrhagic pneumonia caused by Stenotrophomonas maltophilia in hematologic malignancy. Transpl Infect Dis. 2012;14:355–63.CrossRefPubMed Araoka H, Fujii T, Izutsu K, Kimura M, Nishida A, Ishiwata K, et al. Rapidly progressive fatal hemorrhagic pneumonia caused by Stenotrophomonas maltophilia in hematologic malignancy. Transpl Infect Dis. 2012;14:355–63.CrossRefPubMed
9.
go back to reference Shiratori S, Wakasa K, Okada K, Sugita J, Akizawa K, Shigematsu A, et al. Stenotrophomonas maltophilia infection during allogeneic hematopoietic stem cell transplantation: a single-center experience. Clin Transpl. 2014;28:656–61. Shiratori S, Wakasa K, Okada K, Sugita J, Akizawa K, Shigematsu A, et al. Stenotrophomonas maltophilia infection during allogeneic hematopoietic stem cell transplantation: a single-center experience. Clin Transpl. 2014;28:656–61.
10.
go back to reference Yeshurun M, Grafter-Gvili A, Thaler M, Keller N, Nagler A, Shimoni A. Clinical characteristics of Stenotrophomonas maltophilia infection in hematopoietic stem cell transplantation recipients: a single center experience. Infection. 2010;38:211–5.CrossRefPubMed Yeshurun M, Grafter-Gvili A, Thaler M, Keller N, Nagler A, Shimoni A. Clinical characteristics of Stenotrophomonas maltophilia infection in hematopoietic stem cell transplantation recipients: a single center experience. Infection. 2010;38:211–5.CrossRefPubMed
11.
go back to reference Cho SY, Lee DG, Choi SM, Park C, Chun HS, Park YJ, et al. Stenotrophomonas maltophilia bloodstream infection in patients with hematologic malignancies: a retrospective study and in vitro activities of antimicrobial combinations. BMC Infect Dis. 2015;15:69. Cho SY, Lee DG, Choi SM, Park C, Chun HS, Park YJ, et al. Stenotrophomonas maltophilia bloodstream infection in patients with hematologic malignancies: a retrospective study and in vitro activities of antimicrobial combinations. BMC Infect Dis. 2015;15:69.
12.
go back to reference Wu PS, Lu CY, Chang LY, Hsueh PR, Lee PI, Chen JM, et al. Stenotrophomonas maltophilia bacteremia in pediatric patients -- a 10-year analysis. J Microbiol Immunol Infect. 2006;39:144–9.PubMed Wu PS, Lu CY, Chang LY, Hsueh PR, Lee PI, Chen JM, et al. Stenotrophomonas maltophilia bacteremia in pediatric patients -- a 10-year analysis. J Microbiol Immunol Infect. 2006;39:144–9.PubMed
13.
go back to reference Micozzi A, Venditti M, Monaco M, Friedrich A, Taglietti F, Santilli S, et al. Bacteremia due to Stenotrophomonas maltophilia in patients with hematologic malignancies. Clin Infect Dis. 2000;31:705–11.CrossRefPubMed Micozzi A, Venditti M, Monaco M, Friedrich A, Taglietti F, Santilli S, et al. Bacteremia due to Stenotrophomonas maltophilia in patients with hematologic malignancies. Clin Infect Dis. 2000;31:705–11.CrossRefPubMed
14.
go back to reference Raad I, Hanna HA, Alakech B, Chatzinikolaou I, Johnson MM, Tarrand J, et al. Differential time to positivity: a useful method for diagnosing catheter-related bloodstream infections. Ann Intern Med. 2004;140:18–25.CrossRefPubMed Raad I, Hanna HA, Alakech B, Chatzinikolaou I, Johnson MM, Tarrand J, et al. Differential time to positivity: a useful method for diagnosing catheter-related bloodstream infections. Ann Intern Med. 2004;140:18–25.CrossRefPubMed
15.
go back to reference Araoka H, Baba M, Yoneyama A. Risk factors for mortality among patients with Stenotrophomonas maltophilia bacteremia in Tokyo, Japan, 1996-2009. Eur J Clin Microbiol Infect Dis. 2010;29:605–8.CrossRefPubMed Araoka H, Baba M, Yoneyama A. Risk factors for mortality among patients with Stenotrophomonas maltophilia bacteremia in Tokyo, Japan, 1996-2009. Eur J Clin Microbiol Infect Dis. 2010;29:605–8.CrossRefPubMed
16.
go back to reference Reimer LG, Wilson ML, Weinstein MP. Update on detection of bacteremia and fungemia. Clin Microbiol Rev. 1997;10:444–65.PubMedPubMedCentral Reimer LG, Wilson ML, Weinstein MP. Update on detection of bacteremia and fungemia. Clin Microbiol Rev. 1997;10:444–65.PubMedPubMedCentral
17.
go back to reference Paez JI, Tengan FM, Barone AA, Levin AS, Costa SF. Factors associated with mortality in patients with bloodstream infection and pneumonia due to Stenotrophomonas maltophilia. Eur J Clin Microbiol Infect Dis. 2008;27:901–6.CrossRefPubMed Paez JI, Tengan FM, Barone AA, Levin AS, Costa SF. Factors associated with mortality in patients with bloodstream infection and pneumonia due to Stenotrophomonas maltophilia. Eur J Clin Microbiol Infect Dis. 2008;27:901–6.CrossRefPubMed
18.
go back to reference Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med. 2013;39:165–228.CrossRefPubMed Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med. 2013;39:165–228.CrossRefPubMed
19.
go back to reference Giralt S, Ballen K, Rizzo D, Bacigalupo A, Horowitz M, Pasquini M, et al. Reduced-intensity conditioning regimen workshop: defining the dose spectrum. Report of a workshop convened by the center for international blood and marrow transplant research. Biol Blood Marrow Transplant. 2009;15:367–9.CrossRefPubMedPubMedCentral Giralt S, Ballen K, Rizzo D, Bacigalupo A, Horowitz M, Pasquini M, et al. Reduced-intensity conditioning regimen workshop: defining the dose spectrum. Report of a workshop convened by the center for international blood and marrow transplant research. Biol Blood Marrow Transplant. 2009;15:367–9.CrossRefPubMedPubMedCentral
20.
go back to reference Freifeld AG, Bow EJ, Sepkowitz KA, Boeckh MJ, Ito JI, Mullen CA, et al. Clinical practice guideline for the use of antimicrobial agents in neutropenic patients with cancer: 2010 update by the infectious diseases society of america. Clin Infect Dis. 2011;52:e56–93.CrossRefPubMed Freifeld AG, Bow EJ, Sepkowitz KA, Boeckh MJ, Ito JI, Mullen CA, et al. Clinical practice guideline for the use of antimicrobial agents in neutropenic patients with cancer: 2010 update by the infectious diseases society of america. Clin Infect Dis. 2011;52:e56–93.CrossRefPubMed
21.
go back to reference Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48:452–8.CrossRefPubMed Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48:452–8.CrossRefPubMed
22.
go back to reference Rolston KV, Kontoyiannis DP, Yadegarynia D, Raad II. Nonfermentative gram-negative bacilli in cancer patients: increasing frequency of infection and antimicrobial susceptibility of clinical isolates to fluoroquinolones. Diagn Microbiol Infect Dis. 2005;51:215–8.CrossRefPubMed Rolston KV, Kontoyiannis DP, Yadegarynia D, Raad II. Nonfermentative gram-negative bacilli in cancer patients: increasing frequency of infection and antimicrobial susceptibility of clinical isolates to fluoroquinolones. Diagn Microbiol Infect Dis. 2005;51:215–8.CrossRefPubMed
23.
go back to reference Lai CH, Chi CY, Chen HP, Chen TL, Lai CJ, Fung CP, et al. Clinical characteristics and prognostic factors of patients with Stenotrophomonas maltophilia bacteremia. J Microbiol Immunol Infect. 2004;37:350–8.PubMed Lai CH, Chi CY, Chen HP, Chen TL, Lai CJ, Fung CP, et al. Clinical characteristics and prognostic factors of patients with Stenotrophomonas maltophilia bacteremia. J Microbiol Immunol Infect. 2004;37:350–8.PubMed
24.
go back to reference Gradel KO, Thomsen RW, Lundbye-Christensen S, Nielsen H, Schønheyder HC. Baseline C-reactive protein level as a predictor of mortality in bacteraemia patients: a population-based cohort study. Clin Microbiol Infect. 2011;17:627–32.CrossRefPubMed Gradel KO, Thomsen RW, Lundbye-Christensen S, Nielsen H, Schønheyder HC. Baseline C-reactive protein level as a predictor of mortality in bacteraemia patients: a population-based cohort study. Clin Microbiol Infect. 2011;17:627–32.CrossRefPubMed
25.
go back to reference Ho KM, Lee KY, Dobb GJ, Webb SA. C-reactive protein concentration as a predictor of in-hospital mortality after ICU discharge: a prospective cohort study. Intensive Care Med. 2008;34:481–7.CrossRefPubMed Ho KM, Lee KY, Dobb GJ, Webb SA. C-reactive protein concentration as a predictor of in-hospital mortality after ICU discharge: a prospective cohort study. Intensive Care Med. 2008;34:481–7.CrossRefPubMed
26.
go back to reference Lee JH, Kim J, Kim K, Jo YH, Rhee J, Kim TY, et al. Albumin and C-reactive protein have prognostic significance in patients with community-acquired pneumonia. J Crit Care. 2011;26:287–94.CrossRefPubMed Lee JH, Kim J, Kim K, Jo YH, Rhee J, Kim TY, et al. Albumin and C-reactive protein have prognostic significance in patients with community-acquired pneumonia. J Crit Care. 2011;26:287–94.CrossRefPubMed
27.
go back to reference Yin M, Si L, Qin W, Li C, Zhang J, Yang H, et al. Predictive Value of Serum Albumin Level for the Prognosis of Severe Sepsis Without Exogenous Human Albumin Administration. J Intensive Care Med. 2016 Jan;1 [Epub ahead of print] Yin M, Si L, Qin W, Li C, Zhang J, Yang H, et al. Predictive Value of Serum Albumin Level for the Prognosis of Severe Sepsis Without Exogenous Human Albumin Administration. J Intensive Care Med. 2016 Jan;1 [Epub ahead of print]
28.
go back to reference Artero A, Zaragoza R, Camarena JJ, Sancho S, González R, Nogueira JM. Prognostic factors of mortality in patients with community-acquired bloodstream infection with severe sepsis and septic shock. J Crit Care. 2010;25:276–81.CrossRefPubMed Artero A, Zaragoza R, Camarena JJ, Sancho S, González R, Nogueira JM. Prognostic factors of mortality in patients with community-acquired bloodstream infection with severe sepsis and septic shock. J Crit Care. 2010;25:276–81.CrossRefPubMed
29.
go back to reference Ranzani OT, Zampieri FG, Forte DN, Azevedo LC, Park M. C-reactive protein/albumin ratio predicts 90-day mortality of septic patients. PLoS One. 2013;8:e59321.CrossRefPubMedPubMedCentral Ranzani OT, Zampieri FG, Forte DN, Azevedo LC, Park M. C-reactive protein/albumin ratio predicts 90-day mortality of septic patients. PLoS One. 2013;8:e59321.CrossRefPubMedPubMedCentral
30.
go back to reference Kim MH, Ahn JY, Song JE, Choi H, Ann HW, Kim JK, et al. The C-Reactive Protein/Albumin Ratio as an Independent Predictor of Mortality in Patients with Severe Sepsis or Septic Shock Treated with Early Goal-Directed Therapy. PLoS One. 2015;10:e0132109.CrossRefPubMedPubMedCentral Kim MH, Ahn JY, Song JE, Choi H, Ann HW, Kim JK, et al. The C-Reactive Protein/Albumin Ratio as an Independent Predictor of Mortality in Patients with Severe Sepsis or Septic Shock Treated with Early Goal-Directed Therapy. PLoS One. 2015;10:e0132109.CrossRefPubMedPubMedCentral
31.
go back to reference Mori M, Tsunemine H, Imada K, Ito K, Kodaka T, Takahashi T, et al. Life-threatening hemorrhagic pneumonia caused by Stenotrophomonas maltophilia in the treatment of hematologic diseases. Ann Hematol. 2014;93:901–11.CrossRefPubMed Mori M, Tsunemine H, Imada K, Ito K, Kodaka T, Takahashi T, et al. Life-threatening hemorrhagic pneumonia caused by Stenotrophomonas maltophilia in the treatment of hematologic diseases. Ann Hematol. 2014;93:901–11.CrossRefPubMed
32.
go back to reference Tekçe YT, Erbay A, Cabadak H, Sen S. Tigecycline as a therapeutic option in Stenotrophomonas maltophilia infections. J Chemother. 2012;24:150–4. Tekçe YT, Erbay A, Cabadak H, Sen S. Tigecycline as a therapeutic option in Stenotrophomonas maltophilia infections. J Chemother. 2012;24:150–4.
33.
go back to reference Wang YL, Scipione MR, Dubrovskaya Y, et al. Monotherapy with fluoroquinolone or trimethoprim-sulfamethoxazole for treatment of Stenotrophomonas maltophilia infections. Antimicrob Agents Chemother. 2014;58:176–82.CrossRefPubMedPubMedCentral Wang YL, Scipione MR, Dubrovskaya Y, et al. Monotherapy with fluoroquinolone or trimethoprim-sulfamethoxazole for treatment of Stenotrophomonas maltophilia infections. Antimicrob Agents Chemother. 2014;58:176–82.CrossRefPubMedPubMedCentral
34.
go back to reference Averbuch D, Cordonnier C, Livermore DM, Mikulska M, Orasch C, Viscoli C, et al. Targeted therapy against multi-resistant bacteria in leukemic and hematopoietic stem cell transplant recipients: guidelines of the 4th European Conference on Infections in Leukemia (ECIL-4, 2011). Haematologica. 2013;98:1836–47.CrossRefPubMedPubMedCentral Averbuch D, Cordonnier C, Livermore DM, Mikulska M, Orasch C, Viscoli C, et al. Targeted therapy against multi-resistant bacteria in leukemic and hematopoietic stem cell transplant recipients: guidelines of the 4th European Conference on Infections in Leukemia (ECIL-4, 2011). Haematologica. 2013;98:1836–47.CrossRefPubMedPubMedCentral
35.
go back to reference Przepiorka D, Weisdorf D, Martin P, Klingemann HG, Beatty P, Hows J, et al. 1994 Consensus Conference on Acute GVHD Grading. Bone Marrow Transplant. 1995;15:825–8.PubMed Przepiorka D, Weisdorf D, Martin P, Klingemann HG, Beatty P, Hows J, et al. 1994 Consensus Conference on Acute GVHD Grading. Bone Marrow Transplant. 1995;15:825–8.PubMed
Metadata
Title
Predictive implications of albumin and C-reactive protein for progression to pneumonia and poor prognosis in Stenotrophomonas maltophilia bacteremia following allogeneic hematopoietic stem cell transplantation
Authors
Kaito Harada
Noritaka Sekiya
Tatsuya Konishi
Akihito Nagata
Yuta Yamada
Toshiaki Takezaki
Satoshi Kaito
Shuhei Kurosawa
Masahiro Sakaguchi
Shunichiro Yasuda
Shugo Sasaki
Kosuke Yoshioka
Kyoko Watakabe-Inamoto
Aiko Igarashi
Yuho Najima
Takeshi Hagino
Hideharu Muto
Takeshi Kobayashi
Noriko Doki
Kazuhiko Kakihana
Hisashi Sakamaki
Kazuteru Ohashi
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2745-6

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