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Streptococcus Mitis Strains Causing Severe Clinical Disease in Cancer Patients Samuel A

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Streptococcus Mitis Strains Causing Severe Clinical Disease in Cancer Patients Samuel A RESEARCH Streptococcus mitis Strains Causing Severe Clinical Disease in Cancer Patients Samuel A. Shelburne, Pranoti Sahasrabhojane, Miguel Saldana, Hui Yao, Xiaoping Su, Nicola Horstmann, Erika Thompson, and Anthony R. Flores The genetically diverse viridans group streptococci in species designation and classification schemes over time (VGS) are increasingly recognized as the cause of a va- (7). From a clinical microbiology laboratory standpoint, riety of human diseases. We used a recently developed automated systems have considerable limitations in VGS multilocus sequence analysis scheme to define the species species identification (8,9). The problematic nature of VGS of 118 unique VGS strains causing bacteremia in patients species assignment also extends to16S rRNA sequencing, with cancer; Streptococcus mitis (68 patients) and S. ora- the most widely used genetic tool for species identification lis (22 patients) were the most frequently identified strains. Compared with patients infected with non–S. mitis strains, in clinical and research settings (9,10). patients infected with S. mitis strains were more likely to Outcomes for patients with VGS bacteremia are highly have moderate or severe clinical disease (e.g., VGS shock variable: some patients have minimal symptoms, and oth- syndrome). Combined with the sequence data, whole-ge- ers have a severe infection characterized by hypotension nome analyses showed that S. mitis strains may more pre- and acute respiratory distress syndrome (11). The severe cisely be considered as >2 species. Furthermore, we found infections have been termed VGS shock syndrome (12). that multiple S. mitis strains induced disease in neutrope- Numerous studies have examined the species distribution nic mice in a dose-dependent fashion. Our data define the of VGS that cause bacteremia (9,13–16). However, these prominent clinical effect of the group of organisms currently studies have found inconsistent results between a particu- classified as S. mitis and lay the groundwork for increased lar VGS species and disease occurrence or clinical severity understanding of this understudied pathogen. of infection (9,13,14,16,17). Moreover, the recently rec- ognized limitations of previously used techniques of VGS iridans group streptococci (VGS), a genetically het- species identification and the low number of clinical cases Verogeneous group of bacteria, are the predominant analyzed preclude definitive conclusions regarding the re- bacteria in the human oropharynx (1). VGS cause a wide lationship between VGS species type and clinical disease range of infections in humans, including bacteremia in pa- (8,9,18). Thus, we sought to combine the species identi- tients with neutropenia, infective endocarditis, and orbital fication of a large number of VGS bloodstream isolates, cellulitis (2–5). However, despite the substantial clinical which we typed by using a recently developed multilocus effect of VGS, the epidemiology and pathogenesis of these sequence analysis (MLSA) technique (19), with patient- bacteria are minimally understood (6). specific clinical data to determine relationships between A major impediment to the study of VGS has been the VGS species and clinical endpoints. inability to consistently and accurately assign VGS strains to specific species, which has resulted in numerous changes Materials and Methods Author affiliations: MD Anderson Cancer Center, Houston, Texas, Study Cohort and Data Abstraction USA (S.A. Shelburne, P. Sahasrabhojane, M. Saldana, H. Yao, X. The study cohort comprised patients at MD Anderson Su, N. Horstmann, E. Thompson); and Baylor College of Medicine, Cancer (MDACC) who had VGS isolated from their blood Houston, Texas, USA (A.R. Flores) between July 1, 2011, and December 1, 2012. MDAAC is DOI: http://dx.doi.org/10.3201/eid2005.130953 a 600-bed referral cancer hospital in Houston, Texas, USA. 762 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 20, No. 5, May 2014 Streptococcus mitis in Cancer Patients We used a standardized data collection form to abstract clini- sequencing libraries. The 03/10libraries were sequenced on cal data from the comprehensive electronic medical records the HiSeq 2000 sequencing System (Illumina, San Diego, of patients with blood culture results positive for VGS. Anti- CA, USA) by using 76-bp, paired-end sequencing. The microbial drug resistance was determined in accordance with raw reads in FASTQ format were aligned to the S. mitis B6 guidelines of the Clinical and Laboratory Standards Institute (GenBank accession no. NC_013853.1) and S. pneumoniae (www.clsi.org/standards/). VGS are known to contaminate TIGR4 (GenBank accession no. NC_003028.3) genomes blood cultures and to cause clinically minor, transient bacte- by using Mosaik (26). There was an average of 250× cov- remia, and differentiating between contamination and infec- erage per base, indicating extremely high confidence for tion is problematic (20). Thus, for the purpose of this study, base calls. Contigs were generated by feeding the raw ge- we considered that patients without signs or symptoms of nome sequence data into the A5 pipeline (27). Gene an- infection had clinically minor bacteremia, even though they notations were obtained by uploading contigs to the Rapid may represent cases of blood culture contamination. Annotation using the Subsystem Technology server at the Severity of infection, as measured by the Pitt bactere- National Microbial Pathogen Data Resource website (28). mia score, was determined as described (21). Pitt bacteremia (Individual gene sequencing data have been deposited into scores were not determined for patients with polymicrobial GenBank. Short-read sequencing data have been depos- bacteremia. VGS shock syndrome was defined by using the ited to the Short Read Archive (www.ncbi.nlm.nih.gov/ accepted definition for septic shock (i.e., hypotension refrac- Traces/sra/sra.cgi?view=announcement) under accession no. tory to fluid replacement in the setting of an infection) (22). PRJNA240080. A focus of the bloodstream infection was defined as isolation of a VGS species from a nonsterile site (e.g., liver abscess) at Mouse Infection Studies the same time that VGS were isolated from the blood, with Experiments in mice were performed according to a the exception of infective endocarditis, which was defined ac- protocol approved by the MDACC Institutional Animal cording the modified Duke criteria (23,24). Neutropenia was Care and Use Committee. To induce neutropenia, we in- defined as an absolute neutrophil count of <500 cells/mL. jected 5-week-old female Balb/C mice intraperitoneally Some patients had signs and symptoms of a lower with 100 μg/kg of cyclophosphamide (Sigma, St. Louis, respiratory infection and x-ray findings compatible with MO, USA) on days –4 and –1 before bacterial injection. a pneumonic process that could not be explained (i.e., no On day 0, mice (10 per bacterial dose) were injected with known respiratory pathogens were isolated and no other 100 mL of phosphate-buffered saline (PBS) containing 10- alternative explanation, e.g., congestive heart failure, was fold increments of bacteria ranging from 103 to 107 CFUs. found). Such patients were defined as having unexplained As a control, 10 mice were injected with PBS alone. Mice pulmonary infiltrates. Because VGS are considered normal were monitored over 7 days for near-death status. The dose flora, isolation of these organisms from a respiratory speci- at which 50% of the mice nearly died (hereafter referred men would not have been considered clinically meaningful to as LD50) was calculated by using the probit method. by the clinical microbiology laboratory and thus would not Neutropenia was confirmed in select mice on postinfection have been reported. The study protocol was approved by days 1, 3, and 6. the MDCC institutional review board. Statistical Analysis VGS Species Type Determination and Differences between categorical variables were as- Whole-Genome Sequencing sessed by using the χ2 test; Fisher exact test was used when Bacterial isolates were identified as VGS on the basis at least 1 category had <5 occurrences. The relationship of the following: presence of α-hemolysis, gram-positive between VGS species and Pitt bacteremia scores was ana- reaction, coccus morphology arranged in chains, negative lyzed by using the Mann-Whitney U test. The Bonferroni catalase test results, and exclusions of pneumococcus and method was employed to account for multiple comparisons enterococci by routine biochemical tests (i.e., optochin, when appropriate. All tests of significance were 2-sided, bile solubility, and pyrrolidonyl arylamidase tests) (25). and statistical significance was defined at p<0.05. SPSS VGS species was determined as described (19). In brief, Statistics version 19 (IBM, Armonk, NY, USA ) was used concatenated sequences of 7 housekeeping genes were used for statistical analysis. for phylogenetic tree construction in MEGA5 (www.mega software.net/); strains were assigned to VGS species on the Results basis of their distance from species type strains (19). For whole-genome sequencing of 9 Streptococcus mitis strains Study Cohort and 1 S. oralis strain, we fragmented 3 µg of genomic DNA A total of 118 consecutive patients with VGS-positive to 350 bp (mean fragment size) and prepared barcoded blood cultures were included in the study cohort; ≈80% of Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 20, No. 5, May 2014 763 RESEARCH the patients had neutropenia and hematologic malignancies
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