Please wait a minute...

Frontiers of Medicine

Front. Med.    2019, Vol. 13 Issue (4) : 492-503     https://doi.org/10.1007/s11684-019-0681-0
RESEARCH ARTICLE
Positive stool culture could predict the clinical outcomes of haploidentical hematopoietic stem cell transplantation
Lijuan Hu1, Qi Wang4, Xiaohui Zhang1, Lanping Xu1, Yu Wang1, Chenhua Yan1, Huan Chen1, Yuhong Chen1, Kaiyan Liu1, Hui Wang4, Xiaojun Huang1,2,3, Xiaodong Mo1()
1. Peking University People’s Hospital, Peking University Institute of Hematology, Beijing 100044, China
2. Peking-Tsinghua Center for Life Sciences, Beijing 100044, China
3. Beijing Key Laboratory of Hematopoietic Stem Cell Transplantation, Beijing 100044, China
4. Peking University People’s Hospital, Department of Clinical Laboratory, Beijing 100044, China
Download: PDF(379 KB)   HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
Abstract

We aimed to identify the effect of positive stool cultures (PSCs) on the clinical outcomes of patients undergoing haploidentical hematopoietic stem cell transplantation (haplo-HSCT) (n = 332). PSCs were observed in 61 patients (PSC group, 18.4%). Enterobacteriaceae in stool specimens was associated with a higher risk of bloodstream infection, and Candida in stool specimens was related to a higher risk of platelet engraftment failure. The cumulative incidence of infection-related mortality 1 year after haplo-HSCT in the PSC group was higher than that of the patients who showed persistently negative stool cultures (NSC group; 19.2% vs. 8.9%, P = 0.017). The probabilities of overall survival (71.4% vs. 83.8%, P = 0.031) and disease-free survival (69.6% vs. 81.0%, P = 0.048) 1 year after haplo-HSCT for the PSC group were significantly lower than those for the NSC group, particularly for patients who had Candida in their stool specimens. In multivariate analysis, Candida in stool specimens significantly increased the risk of mortality and was associated with poorer survival. Our results showed that PSC influenced the clinical outcomes after haplo-HSCT, particularly those who had Candida in their stool specimens.

Keywords haploidentical      hematopoietic stem cell transplantation      stool culture      Candida     
Corresponding Authors: Xiaodong Mo   
Just Accepted Date: 01 March 2019   Online First Date: 08 April 2019    Issue Date: 02 August 2019
 Cite this article:   
Lijuan Hu,Qi Wang,Xiaohui Zhang, et al. Positive stool culture could predict the clinical outcomes of haploidentical hematopoietic stem cell transplantation[J]. Front. Med., 2019, 13(4): 492-503.
 URL:  
http://journal.hep.com.cn/fmd/EN/10.1007/s11684-019-0681-0
http://journal.hep.com.cn/fmd/EN/Y2019/V13/I4/492
Service
E-mail this article
E-mail Alert
RSS
Articles by authors
Lijuan Hu
Qi Wang
Xiaohui Zhang
Lanping Xu
Yu Wang
Chenhua Yan
Huan Chen
Yuhong Chen
Kaiyan Liu
Hui Wang
Xiaojun Huang
Xiaodong Mo
Variable Negative stool cultures group (n = 271) Positive stool cultures group (n = 61) P value
Gender of patients, male/female 161/110 34/27 0.599
Median age at transplantation, year (range) 30 (2–67) 27 (7–63) 0.123
Adult/children 227/44 52/9 0.775
Diagnosis, no. (%)
Acute myeloid leukemia 106 (39.1) 20 (32.8) 0.773
Acute lymphoblastic leukemia 76 (28.0) 20 (32.8)
Myelodysplastic syndrome 37 (13.7) 10 (16.4)
Severe aplastic anemia 32 (11.8) 5 (8.2)
Chronic myeloid leukemia 6 (2.2) 2 (3.2)
Others 14 (5.2) 4 (6.6)
Chemotherapy before HSCT, no. (%) 198 (73.1) 45 (73.8) 0.910
Median cycles before HSCT, no. (range) 4 (1–18) 4 (1–14) 0.228
Disease status at transplantation, no. (%)
Standard risk 259 (95.6) 61 (100.0) 0.133
High risk 12 (4.4) 0 (0.0)
Disease risk index before transplantation, no. (%)
Low risk 52 (19.2) 10 (16.4) 0.363
Intermediate risk 187 (69.0) 40 (65.6)
High risk 28 (10.3) 11 (18.0)
Very high risk 4 (1.5) 0 (0.0)
No. of HLA-A, -B, and -DR mismatch, no. (%)
3/6 229 (84.5) 48 (78.7) 0.462
4/6 33 (12.2) 10 (16.4)
5/6 9 (3.3) 3 (4.9)
Previous HSCT, no. (%)a 3 (1.1) 0 (0.0) 1.000
Donor–recipient sex match, no. (%)
Female–male 39 (14.4) 8 (13.1) 0.796
Others 232 (85.6) 53 (86.9)
Donor–recipient relations, no. (%)
Father 123 (45.4) 31 (50.8) 0.207
Mother 12 (4.4) 5 (8.2)
Sibling 55 (20.3) 14 (23.0)
Child 74 (27.3) 9 (14.8)
Others 7 (2.6) 2 (3.2)
Donor–recipient blood type, no. (%)
Matched 142 (52.4) 29 (47.5) 0.660
Major mismatched 55 (20.3) 13 (21.3)
Minor mismatched 58 (21.4) 13 (21.3)
Major and minor mismatched 16 (5.9) 6 (9.9)
Median mononuclear cells, × 108/kg (range) 8.1 (4.6–13.2) 8.0 (5.2–11.4) 0.463
Median CD4+ counts, × 107/kg (range) 1.1 (0.1–4.2) 1.0 (0.2–2.3) 0.870
Median CD34+ counts, × 106/kg (range) 2.3 (0.5–8.2) 2.4 (0.3–7.6) 0.264
Previous broad-spectrum antibiotics before stool cultures, no. (%)
Carbapenem 91 (33.6) 22 (36.1) 0.711
Other β-lactam antibiotics 128 (47.2) 22 (36.1) 0.113
Tigecycline 8 (3.0) 4 (6.6) 0.244
Vancomycin/teicoplanin/linezolid 33 (12.2) 13 (21.3) 0.062
Multiple broad-spectrum antibiotics (≥2) 110 (40.6) 23 (37.7) 0.678
Oral mucositis during preconditioning treatment, no. (%)
None 223 (82.3) 53 (86.9) 0.647
Grades I to II 40 (14.8) 6 (9.8)
≥Grade III 8 (2.9) 2 (3.3)
Gastrointestinal tract toxicities during preconditioning treatment, no. (%)
≥Grade II 64 (23.6) 11 (18.0) 0.637
Cumulative dose of corticosteroid before stool cultures after haplo-HSCT, no. (prednisone, mg/kg) 4.9 (0.3–126.0) 5.1 (0.6–33.8) 0.483
Median duration of follow-up in survivors, day (range) 434 (61–765) 391 (64–756) 0.351
Tab.1  Patient characteristics
Type of organism Number
Enterobacteriaceae Escherichia coli 22
Klebsiella pneumoniae 4
Proteus mirabilis 2
Enterococcus Enterococcus faecalis 5
Enterococcus faecium 9
Other bacteria Pseudomonas aeruginosa 2
Streptococcus salivarius 1
Candida Candida albicans 16
Candida parapsilosis 1
Candida glabrata 7
Candida tropicalis 1
Candida krusei 1
Saccharomyces cerevisiae 2
Tab.2  Microorganisms in stool specimens
30-day neutrophil engraftment failure 100-day platelet engraftment failure
Hazard ratio (95% CI) P Hazard ratio (95% CI) P
Microorganism in stool specimens
No 1.0 0.361 1.0 0.330
Yes 1.13 (0.86–1.53) 1.16 (0.86–1.57)
Enterobacteriaceae in stool specimens
No 1.0 0.201 1.0 0.871
Yes 1.33 (0.86–2.06) 0.96 (0.62–1.50)
Enterococcus in stool specimens
No 1.0 0.926 1.0 0.828
Yes 0.97 (0.57–1.67) 1.06 (0.61–1.86)
Candida in stool specimens
No 1.0 0.480 1.0 0.041
Yes 1.16 (0.77–1.74) 1.60 (1.02–2.50)
100-day grades II to IV aGVHD 100-day grades III to IV aGVHD
Hazard ratio (95% CI) P Hazard ratio (95% CI) P
Microorganism in stool specimens
No 1.0 0.266 1.0 0.629
Yes 0.76 (0.47–1.24) 0.83 (0.39–1.77)
Enterobacteriaceae in stool specimens
No 1.0 0.077 1.0 0.279
Yes 0.45 (0.18–1.09) 0.46 (0.11–1.88)
Enterococcus in stool specimens
No 1.0 0.253 1.0 0.308
Yes 0.51 (0.16–1.61) 0.05 (0.01–16.98)
Candida in stool specimens
No 1.0 0.942 1.0 0.680
Yes 1.02 (0.54–1.96) 0.78 (0.24–2.52)
Tab.3  Effect of PSCs on the engraftment and aGVHD
Fig.1  Clinical outcomes of patients who underwent haplo-HSCT on the basis of the results of stool cultures. (A) relapse, (B) non-relapse mortality, (C) infection-related mortality, (D) overall survival, and (E) disease-free survival. NSC, negative stool cultures; PSC, positive stool cultures.
1-year relapse 1-year non-relapse mortality 1-year infection-related mortality
Hazard ratio (95% CI) P Hazard ratio (95% CI) P Hazard ratio (95% CI) P
Microorganism in stool specimens
No 1.0 0.482 1.0 0.057 1.0 0.016
Yes 1.49 (0.49–4.53) 1.91 (0.98–3.72) 2.54 (1.19–5.43)
Enterobacteriaceae in stool specimens
No 1.0 0.484 1.0 0.397 1.0 0.368
Yes 0.05 (0.01–263.11) 1.56 (0.56–4.37) 1.73 (0.53–5.72)
Enterococcus in stool specimens
No 1.0 0.190 1.0 0.506 1.0 0.799
Yes 2.68 (0.62–11.65) 0.51 (0.07–3.71) 0.77 (0.11–5.67)
Candida in stool specimens
No 1.0 0.117 1.0 0.035 1.0 0.002
Yes 2.70 (0.78–9.34) 2.39 (1.06–5.38) 3.87 (1.66–9.03)
1-year disease-free survival 1-year overall survival
Hazard ratio (95% CI) P Hazard ratio (95% CI) P
Microorganism in stool specimens
No 1.0 0.046 1.0 0.030
Yes 1.79 (1.01–3.17) 1.93 (1.07–3.51)
Enterobacteriaceae in stool specimens
No 1.0 0.893 1.0 0.658
Yes 1.07 (0.39–2.96) 1.26 (0.45–3.49)
Enterococcus in stool specimens
No 1.0 0.832 1.0 0.699
Yes 1.13 (0.36–3.62) 1.26 (0.39–4.03)
Candida in stool specimens
No 1.0 0.008 1.0 0.013
Yes 2.50 (1.27–4.92) 2.48 (1.21–5.07)
Tab.4  Effect of PSCs on relapse, nonrelapse mortality, and survival
Outcome HR (95% CI) P value
Treatment failure as defined by overall survival
Candida in stool specimens
No 1
Yes 2.53 (1.22–5.24) 0.012
Disease risk index
Low risk 1
Intermediate risk 1.41 (0.59–3.38) 0.441
High risk 3.18 (1.19–8.47) 0.021
Very high risk 25.44 (6.91–93.73) <0.001
Treatment failure as defined by disease-free survival
Candida in stool specimens
No 1
Yes 2.60 (1.31–5.18) 0.006
Disease risk index
Low risk 1
Intermediate risk 1.64 (0.69–3.89) 0.263
High risk 3.98 (1.53–10.37) 0.005
Very high risk 41.05 (11.02–152.95) <0.001
Nonrelapse mortality
Candida in stool specimens
No 1
Yes 2.39 (1.06–5.38) 0.035
Infection-related mortality
Candida in stool specimens
No 1
Yes 3.87 (1.66–9.03) 0.002
Relapse
Disease risk index
Low risk 1
Intermediate risk 2.63 (0.34–20.37) 0.355
High risk 11.08 (1.33–92.05) 0.026
Very high risk 470.00 (37.69–5860.29) <0.001
Tab.5  Multivariate analysis of risk factors of clinical outcomes
Fig.2  Survival of haplo-HSCT recipients with and without Candida in stool specimens. (A) Infection-related mortality, (B) overall survival, and (C) disease-free survival.
1 M Lv, XJ Huang. Allogeneic hematopoietic stem cell transplantation in China: where we are and where to go. J Hematol Oncol 2012; 5(1): 10
https://doi.org/10.1186/1756-8722-5-10 pmid: 22424172
2 Y Wang, QF Liu, LP Xu, KY Liu, XH Zhang, X Ma, ZP Fan, DP Wu, XJ Huang. Haploidentical vs. identical-sibling transplant for AML in remission: a multicenter, prospective study. Blood 2015; 125(25): 3956–3962
https://doi.org/10.1182/blood-2015-02-627786 pmid: 25940714
3 Y Wang, QF Liu, LP Xu, KY Liu, XH Zhang, X Ma, MQ Wu, DP Wu, XJ Huang. Haploidentical versus matched-sibling transplant in adults with Philadelphia-negative high-risk acute lymphoblastic leukemia: a biologically phase III randomized study. Clin Cancer Res 2016; 22(14): 3467–3476
https://doi.org/10.1158/1078-0432.CCR-15-2335 pmid: 26927664
4 Y Wang, HX Wang, YR Lai, ZM Sun, DP Wu, M Jiang, DH Liu, KL Xu, QF Liu, L Liu, JB Wang, F Gao, J Ou-Yang, SJ Gao, LP Xu, XJ Huang. Haploidentical transplant for myelodysplastic syndrome: registry-based comparison with identical sibling transplant. Leukemia 2016; 30(10): 2055–2063
https://doi.org/10.1038/leu.2016.110 pmid: 27133816
5 LP Xu, DP Wu, MZ Han, H Huang, QF Liu, DH Liu, ZM Sun, LH Xia, J Chen, HX Wang, C Wang, CF Li, YR Lai, JM Wang, DB Zhou, H Chen, YP Song, T Liu, KY Liu, XJ Huang. A review of hematopoietic cell transplantation in China: data and trends during 2008–2016. Bone Marrow Transplant 2017; 52(11): 1512–1518
https://doi.org/10.1038/bmt.2017.59 pmid: 28436973
6 L Xu, H Chen, J Chen, M Han, H Huang, Y Lai, D Liu, Q Liu, T Liu, M Jiang, H Ren, Y Song, Z Sun, J Wang, D Wu, D Zhou, P Zou, K Liu, X Huang. The consensus on indications, conditioning regimen, and donor selection of allogeneic hematopoietic cell transplantation for hematological diseases in China-recommendations from the Chinese Society of Hematology. J Hematol Oncol 2018; 11(1): 33
https://doi.org/10.1186/s13045-018-0564-x pmid: 29495966
7 XJ Huang, YJ Chang. Unmanipulated HLA-mismatched/haploidentical blood and marrow hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 2011; 17(2): 197–204
https://doi.org/10.1016/j.bbmt.2010.03.006 pmid: 20302961
8 EJ Fuchs. HLA-haploidentical blood or marrow transplantation with high-dose, post-transplantation cyclophosphamide. Bone Marrow Transplant 2015; 50(S2 Suppl 2): S31–S36
https://doi.org/10.1038/bmt.2015.92 pmid: 26039204
9 JU Scher, A Sczesnak, RS Longman, N Segata, C Ubeda, C Bielski, T Rostron, V Cerundolo, EG Pamer, SB Abramson, C Huttenhower, DR Littman. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. eLife 2013; 2: e01202
https://doi.org/10.7554/eLife.01202 pmid: 24192039
10 MI Smith, T Yatsunenko, MJ Manary, I Trehan, R Mkakosya, J Cheng, AL Kau, SS Rich, P Concannon, JC Mychaleckyj, J Liu, E Houpt, JV Li, E Holmes, J Nicholson, D Knights, LK Ursell, R Knight, JI Gordon. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013; 339(6119): 548–554
https://doi.org/10.1126/science.1229000 pmid: 23363771
11 PJ Turnbaugh, M Hamady, T Yatsunenko, BL Cantarel, A Duncan, RE Ley, ML Sogin, WJ Jones, BA Roe, JP Affourtit, M Egholm, B Henrissat, AC Heath, R Knight, JI Gordon. A core gut microbiome in obese and lean twins. Nature 2009; 457(7228): 480–484
https://doi.org/10.1038/nature07540 pmid: 19043404
12 J Qin, Y Li, Z Cai, S Li, J Zhu, F Zhang, S Liang, W Zhang, Y Guan, D Shen, Y Peng, D Zhang, Z Jie, W Wu, Y Qin, W Xue, J Li, L Han, D Lu, P Wu, Y Dai, X Sun, Z Li, A Tang, S Zhong, X Li, W Chen, R Xu, M Wang, Q Feng, M Gong, J Yu, Y Zhang, M Zhang, T Hansen, G Sanchez, J Raes, G Falony, S Okuda, M Almeida, E LeChatelier, P Renault, N Pons, JM Batto, Z Zhang, H Chen, R Yang, W Zheng, S Li, H Yang, J Wang, SD Ehrlich, R Nielsen, O Pedersen, K Kristiansen, J Wang. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490(7418): 55–60
https://doi.org/10.1038/nature11450 pmid: 23023125
13 MD Docampo, JJ Auletta, RR Jenq. Emerging influence of the intestinal microbiota during allogeneic hematopoietic cell transplantation: control the gut and the body will follow. Biol Blood Marrow Transplant 2015; 21(8): 1360–1366
https://doi.org/10.1016/j.bbmt.2015.02.016 pmid: 25708215
14 Y Shono, MRM van den Brink. Gut microbiota injury in allogeneic haematopoietic stem cell transplantation. Nat Rev Cancer 2018; 18(5): 283–295
https://doi.org/10.1038/nrc.2018.10 pmid: 29449660
15 XJ Huang, DH Liu, KY Liu, LP Xu, H Chen, W Han, YH Chen, XH Zhang, DP Lu. Treatment of acute leukemia with unmanipulated HLA-mismatched/haploidentical blood and bone marrow transplantation. Biol Blood Marrow Transplant 2009; 15(2): 257–265
https://doi.org/10.1016/j.bbmt.2008.11.025 pmid: 19167686
16 Y Wang, DH Liu, KY Liu, LP Xu, XH Zhang, W Han, H Chen, YH Chen, FR Wang, JZ Wang, YQ Sun, XJ Huang. Long-term follow-up of haploidentical hematopoietic stem cell transplantation without in vitro T cell depletion for the treatment of leukemia: nine years of experience at a single center. Cancer 2013; 119(5): 978–985
https://doi.org/10.1002/cncr.27761 pmid: 23097265
17 XJ Huang, DH Liu, KY Liu, LP Xu, H Chen, W Han, YH Chen, JZ Wang, ZY Gao, YC Zhang, Q Jiang, HX Shi, DP Lu. Haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion for the treatment of hematological malignancies. Bone Marrow Transplant 2006; 38(4): 291–297
https://doi.org/10.1038/sj.bmt.1705445 pmid: 16883312
18 XD Mo, XH Zhang, LP Xu, Y Wang, CH Yan, H Chen, YH Chen, W Han, FR Wang, JZ Wang, KY Liu, XJ Huang. Late-onset severe pneumonia after allogeneic hematopoietic stem cell transplantation: prognostic factors and treatments. Transpl Infect Dis 2016; 18(4): 492–503
https://doi.org/10.1111/tid.12553 pmid: 27218435
19 P Armand, HT Kim, BR Logan, Z Wang, EP Alyea, ME Kalaycio, RT Maziarz, JH Antin, RJ Soiffer, DJ Weisdorf, JD Rizzo, MM Horowitz, W Saber. Validation and refinement of the Disease Risk Index for allogeneic stem cell transplantation. Blood 2014; 123(23): 3664–3671
https://doi.org/10.1182/blood-2014-01-552984 pmid: 24744269
20 D Przepiorka, D Weisdorf, P Martin, HG Klingemann, P Beatty, J Hows, ED Thomas. 1994 Consensus Conference on Acute GVHD Grading. Bone Marrow Transplant 1995; 15(6): 825–828
pmid: 7581076
21 TA Gooley, W Leisenring, J Crowley, BE Storer. Estimation of failure probabilities in the presence of competing risks: new representations of old estimators. Stat Med 1999; 18(6): 695–706
https://doi.org/10.1002/(SICI)1097-0258(19990330)18:6<695::AID-SIM60>3.0.CO;2-O pmid: 10204198
22 C Huisman, HM van der Straaten, MR Canninga-van Dijk, R Fijnheer, LF Verdonck. Pulmonary complications after T-cell-depleted allogeneic stem cell transplantation: low incidence and strong association with acute graft-versus-host disease. Bone Marrow Transplant 2006; 38(8): 561–566
https://doi.org/10.1038/sj.bmt.1705484 pmid: 16953211
23 CS Chen, M Boeckh, K Seidel, JG Clark, E Kansu, DK Madtes, JL Wagner, RP Witherspoon, C Anasetti, FR Appelbaum, WI Bensinger, HJ Deeg, PJ Martin, JE Sanders, R Storb, J Storek, J Wade, M Siadak, ME Flowers, KM Sullivan. Incidence, risk factors, and mortality from pneumonia developing late after hematopoietic stem cell transplantation. Bone Marrow Transplant 2003; 32(5): 515–522
https://doi.org/10.1038/sj.bmt.1704162 pmid: 12942099
24 MJ Krowka, EC Rosenow 3rd, HC Hoagland. Pulmonary complications of bone marrow transplantation. Chest 1985; 87(2): 237–246
https://doi.org/10.1378/chest.87.2.237 pmid: 2981658
25 P Chevallier, I Hebia-Fellah, L Planche, T Guillaume, C Bressolette-Bodin, M Coste-Burel, F Rialland, M Mohty, BM Imbert-Marcille. Human herpes virus 6 infection is a hallmark of cord blood transplant in adults and may participate to delayed engraftment: a comparison with matched unrelated donors as stem cell source. Bone Marrow Transplant 2010; 45(7): 1204–1211
https://doi.org/10.1038/bmt.2009.326 pmid: 19935727
26 XD Mo, X Yan, W Hu, XH Zhang, LP Xu, Y Wang, XD Xu, LN Wang, XX He, CH Yan, H Chen, YH Chen, KY Liu, XJ Huang. Perianal infections in the phase before engraftment after allogeneic hematopoietic stem cell transplantations: a study of the incidence, risk factors, and clinical outcomes. Acta Haematol 2018; 139(1): 19–27
https://doi.org/10.1159/000481723 pmid: 29320771
27 X Zhao, X Zhao, M Huo, Q Fan, X Pei, Y Wang, X Zhang, L Xu, X Huang, K Liu, Y Chang. Donor-specific anti-human leukocyte antigen antibodies predict prolonged isolated thrombocytopenia and inferior outcomes of haploidentical hematopoietic stem cell transplantation. J Immunol Res 2017; 2017: 1043836
https://doi.org/10.1155/2017/1043836 pmid: 28484721
28 I Zollner-Schwetz, HW Auner, A Paulitsch, W Buzina, PB Staber, P Ofner-Kopeinig, EC Reisinger, H Olschewski, R Krause. Oral and intestinal Candida colonization in patients undergoing hematopoietic stem-cell transplantation. J Infect Dis 2008; 198(1): 150–153
https://doi.org/10.1086/588827 pmid: 18491972
29 M Nucci, E Anaissie. Revisiting the source of candidemia: skin or gut? Clin Infect Dis 2001; 33(12): 1959–1967
https://doi.org/10.1086/323759 pmid: 11702290
30 J Bilinski, K Robak, Z Peric, H Marchel, E Karakulska-Prystupiuk, K Halaburda, P Rusicka, E Swoboda-Kopec, M Wroblewska, W Wiktor-Jedrzejczak, GW Basak. Impact of gut colonization by antibiotic-resistant bacteria on the outcomes of allogeneic hematopoietic stem cell transplantation: a retrospective, single-center study. Biol Blood Marrow Transplant 2016; 22(6): 1087–1093
https://doi.org/10.1016/j.bbmt.2016.02.009 pmid: 26900084
31 A Sadowska-Klasa, A Piekarska, W Prejzner, M Bieniaszewska, A Hellmann. Colonization with multidrug-resistant bacteria increases the risk of complications and a fatal outcome after allogeneic hematopoietic cell transplantation. Ann Hematol 2018; 97(3): 509–517
https://doi.org/10.1007/s00277-017-3205-5 pmid: 29255911
32 Y Taur, JB Xavier, L Lipuma, C Ubeda, J Goldberg, A Gobourne, YJ Lee, KA Dubin, ND Socci, A Viale, MA Perales, RR Jenq, MR van den Brink, EG Pamer. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 2012; 55(7): 905–914
https://doi.org/10.1093/cid/cis580 pmid: 22718773
33 JM Vossen, PJ Heidt, H van den Berg, EJ Gerritsen, J Hermans, LJ Dooren. Prevention of infection and graft-versus-host disease by suppression of intestinal microflora in children treated with allogeneic bone marrow transplantation. Eur J Clin Microbiol Infect Dis 1990; 9(1): 14–23
https://doi.org/10.1007/BF01969527 pmid: 2105890
34 DD Poutsiaka, LL Price, A Ucuzian, GW Chan, KB Miller, DR Snydman. Blood stream infection after hematopoietic stem cell transplantation is associated with increased mortality. Bone Marrow Transplant 2007; 40(1): 63–70
https://doi.org/10.1038/sj.bmt.1705690 pmid: 17468772
35 O Blennow, P Ljungman, E Sparrelid, J Mattsson, M Remberger. Incidence, risk factors, and outcome of bloodstream infections during the pre-engraftment phase in 521 allogeneic hematopoietic stem cell transplantations. Transpl Infect Dis 2014; 16(1): 106–114
https://doi.org/10.1111/tid.12175 pmid: 24372809
36 CH Yan, T Xu, XY Zheng, J Sun, XL Duan, JL Gu, CL Zhao, J Zhu, YH Wu, DP Wu, JD Hu, H Huang, M Jiang, J Li, M Hou, C Wang, ZH Shao, T Liu, Y Hu, XJ Huang. Epidemiology of febrile neutropenia in patients with hematological disease—a prospective multicentre survey in China. Chin J Hematol (Zhonghua Xue Ye Xue Za Zhi) 2016; 37(3): 177–182 (in Chinese)
pmid: 27033752
37 DW van Bekkum, J Roodenburg, PJ Heidt, D van der Waaij. Mitigation of secondary disease of allogeneic mouse radiation chimeras by modification of the intestinal microflora. J Natl Cancer Inst 1974; 52(2): 401–404
https://doi.org/10.1093/jnci/52.2.401 pmid: 4150164
38 JM Jones, R Wilson, PM Bealmear. Mortality and gross pathology of secondary disease in germfree mouse radiation chimeras. Radiat Res 1971; 45(3): 577–588
https://doi.org/10.2307/3573066 pmid: 4396814
39 DW Beelen, A Elmaagacli, KD Müller, H Hirche, UW Schaefer. Influence of intestinal bacterial decontamination using metronidazole and ciprofloxacin or ciprofloxacin alone on the development of acute graft-versus-host disease after marrow transplantation in patients with hematologic malignancies: final results and long-term follow-up of an open-label prospective randomized trial. Blood 1999; 93(10): 3267–3275
pmid: 10233878
40 FB Petersen, CD Buckner, RA Clift, N Nelson, GW Counts, JD Meyers, ED Thomas. Infectious complications in patients undergoing marrow transplantation: a prospective randomized study of the additional effect of decontamination and laminar air flow isolation among patients receiving prophylactic systemic antibiotics. Scand J Infect Dis 1987; 19(5): 559–567
https://doi.org/10.3109/00365548709032423 pmid: 3321413
41 JR Passweg, PA Rowlings, KA Atkinson, AJ Barrett, RP Gale, A Gratwohl, N Jacobsen, JP Klein, P Ljungman, JA Russell, UW Schaefer, KA Sobocinski, JM Vossen, MJ Zhang, MM Horowitz. Influence of protective isolation on outcome of allogeneic bone marrow transplantation for leukemia. Bone Marrow Transplant 1998; 21(12): 1231–1238
https://doi.org/10.1038/sj.bmt.1701238 pmid: 9674857
42 D Weber, RR Jenq, JU Peled, Y Taur, A Hiergeist, J Koestler, K Dettmer, M Weber, D Wolff, J Hahn, EG Pamer, W Herr, A Gessner, PJ Oefner, MRM van den Brink, E Holler. Microbiota disruption induced by early use of broad-spectrum antibiotics is an independent risk factor of outcome after allogeneic stem cell transplantation. Biol Blood Marrow Transplant 2017; 23(5): 845–852
https://doi.org/10.1016/j.bbmt.2017.02.006 pmid: 28232086
43 Y Shono, MD Docampo, JU Peled, SM Perobelli, E Velardi, JJ Tsai, AE Slingerland, OM Smith, LF Young, J Gupta, SR Lieberman, HV Jay, KF Ahr, KA Porosnicu Rodriguez, K Xu, M Calarfiore, H Poeck, S Caballero, SM Devlin, F Rapaport, JA Dudakov, AM Hanash, B Gyurkocza, GF Murphy, C Gomes, C Liu, EL Moss, SB Falconer, AS Bhatt, Y Taur, EG Pamer, MRM van den Brink, RR Jenq. Increased GVHD-related mortality with broad-spectrum antibiotic use after allogeneic hematopoietic stem cell transplantation in human patients and mice. Sci Transl Med 2016; 8(339): 339ra71
https://doi.org/10.1126/scitranslmed.aaf2311 pmid: 27194729
44 A Staffas, M Burgos da Silva, MR van den Brink. The intestinal microbiota in allogeneic hematopoietic cell transplant and graft-versus-host disease. Blood 2017; 129(8): 927–933
https://doi.org/10.1182/blood-2016-09-691394 pmid: 27940475
45 RM Shallis, CM Terry, SH Lim. Changes in intestinal microbiota and their effects on allogeneic stem cell transplantation. Am J Hematol 2018; 93(1): 122–128
https://doi.org/10.1002/ajh.24896 pmid: 28842931
46 C Ubeda, Y Taur, RR Jenq, MJ Equinda, T Son, M Samstein, A Viale, ND Socci, MR van den Brink, M Kamboj, EG Pamer. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 2010; 120(12): 4332–4341
https://doi.org/10.1172/JCI43918 pmid: 21099116
47 Y Taur, RR Jenq, MA Perales, ER Littmann, S Morjaria, L Ling, D No, A Gobourne, A Viale, PB Dahi, DM Ponce, JN Barker, S Giralt, M van den Brink, EG Pamer. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood 2014; 124(7): 1174–1182
https://doi.org/10.1182/blood-2014-02-554725 pmid: 24939656
Related articles from Frontiers Journals
[1] Xiaodong Mo, Xiaohui Zhang, Lanping Xu, Yu Wang, Chenhua Yan, Huan Chen, Yuhong Chen, Wei Han, Fengrong Wang, Jingzhi Wang, Kaiyan Liu, Xiaojun Huang. Minimal residual disease-directed immunotherapy for high-risk myelodysplastic syndrome after allogeneic hematopoietic stem cell transplantation[J]. Front. Med., 2019, 13(3): 354-364.
[2] Xiaodong Mo, Xiaohui Zhang, Lanping Xu, Yu Wang, Chenhua Yan, Huan Chen, Yuhong Chen, Wei Han, Fengrong Wang, Jingzhi Wang, Kaiyan Liu, Xiaojun Huang. Interferon-α salvage treatment is effective for patients with acute leukemia/myelodysplastic syndrome with unsatisfactory response to minimal residual disease-directed donor lymphocyte infusion after allogeneic hematopoietic stem cell transplantation[J]. Front. Med., 2019, 13(2): 238-249.
[3] Meng Lv, Yingjun Chang, Xiaojun Huang. Everyone has a donor: contribution of the Chinese experience to global practice of haploidentical hematopoietic stem cell transplantation[J]. Front. Med., 2019, 13(1): 45-56.
[4] Fei Gao, Jingyu Chen, Dong Wei, Bo Wu, Min Zhou. Lung transplantation for bronchiolitis obliterans syndrome after allogenic hematopoietic stem cell transplantation[J]. Front. Med., 2018, 12(2): 224-228.
[5] Xuying Pei, Xiangyu Zhao, Yu Wang, Lanping Xu, Xiaohui Zhang, Kaiyan Liu, Yingjun Chang, Xiaojun Huang. Comparison of reference values for immune recovery between event-free patients receiving haploidentical allografts and those receiving human leukocyte antigen-matched sibling donor allografts[J]. Front. Med., 2018, 12(2): 153-163.
[6] Lanping Xu,Huanling Zhu,Jianda Hu,Depei Wu,Hao Jiang,Qian Jiang,Xiaojun Huang. Superiority of allogeneic hematopoietic stem cell transplantation to nilotinib and dasatinib for adult patients with chronic myelogenous leukemia in the accelerated phase[J]. Front. Med., 2015, 9(3): 304-311.
[7] Hang Zhou,Yao Jia,Jian Shen,Shaoshuai Wang,Xiong Li,Ru Yang,Kecheng Huang,Ting Hu,Fangxu Tang,Jin Zhou,Jingping Yuan,Lei Huang,Xun Tian,Zhilan Chen,Qinghua Zhang,Changyu Wang,Ling Xi,Dongrui Deng,Hui Wang,Ding Ma,Shuang Li. Gynecologic infections seen in ThinPrep cytological test in Wuhan, China[J]. Front. Med., 2014, 8(2): 236-240.
[8] Xiaodong Mo, Xiaojun Huang. Advancement of human leukocyte antigen-partially matched related hematopoietic stem cell transplantation[J]. Front Med, 2013, 7(3): 306-315.
[9] Quan LI MD , Weiming LI MD , Ping ZOU MD , Jian ZHANG BM , . Gene and protein expression of proteinase-activated receptor-1, 2 in a murine model of acute graft host disease[J]. Front. Med., 2009, 3(3): 309-315.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed