Abstract
During a 14-month period of using matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) for group B streptococcus (GBS) identification, we recovered 32 (1%) Streptococcus pseudoporcinus isolates from 3,276 GBS screening cultures from female genital sources (25 isolates from pregnant women and 7 from nonpregnant women). An additional two S. pseudoporcinus isolates were identified from a urine culture and a posthysterectomy wound culture. These isolates were found to cross-react with three different GBS antigen agglutination kits, PathoDx (Remel) (93%), Prolex (Pro-Lab Diagnostics) (38%), and Streptex (Remel) (53%). New approaches to bacterial identification in routine clinical microbiology laboratories may affect the prevalence of S. pseudoporcinus.
TEXT
Streptococcus pseudoporcinus is a beta-hemolytic Gram-positive coccus that was identified as a separate and independent Streptococcus species in 2006 (1). S. pseudoporcinus has been isolated from the female genitourinary tract and has biochemical characteristics similar to those of Streptococcus agalactiae, which is also known as group B streptococcus (GBS) (1–3). The prevalence and clinical significance of genitourinary S. pseudoporcinus and its relationship to peripartum neonatal and maternal infections are not currently known (2, 3). In 2011, Stoner et al. (4) sought to identify the prevalence and epidemiology of S. pseudoporcinus in the genital tracts of nonpregnant women. They found that 5.4% of the women in their study had genital cultures positive for this bacterium. The cross-reactivity of standard GBS testing kits raises concerns that S. pseudoporcinus has been misidentified as GBS in routine GBS screening cultures (1–4). In addition, matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) analysis is coming to be routinely used for organism identification (5, 6). At the Johns Hopkins Hospital (JHH) microbiology laboratory, we became aware of S. pseudoporcinus identification from positive GBS screening cultures after the implementation of MALDI-TOF MS (Bruker Daltonics, Billerica, MA) for organism identification. Thus, we prospectively identified S. pseudoporcinus isolates from GBS screening cultures to determine the prevalence and clinical characteristics of patients with S. pseudoporcinus colonization.
(Some of the data in this paper were presented in poster form at the 115th General Meeting of the American Society for Microbiology, 30 May to 2 June 2015, New Orleans, LA.)
We identified S. pseudoporcinus and S. agalactiae from GBS screening cultures at the JHH between 1 April 2014 and 31 May 2015. Swabs from female genital sources were inoculated into Todd-Hewitt (TH) broth and onto 5% sheep blood agar (SBA; Remel, Lenexa, KS) plates. The broth was incubated at 35°C in a 5% CO2 incubator for 18 to 24 h, subcultured onto 5% SBA, and then incubated for 18 to 24 h. Beta-hemolytic colonies from GBS screening cultures were identified by MALDI-TOF MS (Bruker Microflex, Biotyper software V.3.0, and database v.3.1.66) in accordance with the manufacturer's instructions. All isolates were tested in duplicate. The manufacturer's spectral cutoff score used for interpretation was >2.0 for identification to the species level. Suspected isolates of S. pseudoporcinus had their identification confirmed by sequencing of the first 500 bp of the 16S rRNA gene. Sequence identification was carried out with the PCR 500 and Sequencing 500 MicroSeq kits for bacterial identification (Life Technologies-Applied Biosystems, Foster City, CA). All procedures were performed in accordance with the manufacturer's instructions. Sequencing was performed on an ABI 3500 gene sequencer. Gene assembly, data searching, and generation of the final report were performed with software supplied by SmartGene, Inc. (Raleigh, NC). Sequencing scores were interpreted in accordance with guidelines established by the Clinical and Laboratory Standards Institute (7); that is, sequencing results matching the reference strains at a value of ≥99% were considered acceptable for identification to both the species and genus levels. Available isolates were tested for group B antigen with three commercial beta-hemolytic streptococcus agglutination test kits: PathoDx (Remel, Lenexa, KS), Prolex (Pro-Lab Diagnostics, Round Rock, TX), and Streptex (Remel, Lenexa, KS). Clindamycin and erythromycin susceptibility testing (Thermo Scientific Oxoid Clindamycin and Erythromycin Antimicrobial Susceptibility Disks; Remel, Lenexa, KS) for all S. agalactiae and S. pseudoporcinus isolates was performed in accordance with the Clinical and Laboratory Standards Institute interpretive guidelines (disk diffusion test) (8). To determine whether molecular assays designed for GBS detection directly from enrichment broth would detect S. pseudoporcinus, we randomly selected 10 S. pseudoporcinus isolates recovered from pregnant women for identification with the FDA-cleared PCR-based BD MAX GBS assay kit (Becton Dickinson, Sparks, MD). The isolates were inoculated into TH broth, and GBS identification was performed as previously described (9). In addition, we searched JHH microbiology laboratory reports for S. pseudoporcinus recovered from clinical cultures other than those performed to screen for GBS during the study period. Clinical characteristics of patients colonized with S. pseudoporcinus were reviewed. This study was approved by the Johns Hopkins University School of Medicine Institutional Review Board.
In 3,276 GBS screening cultures, 32 isolates (1.0%) of S. pseudoporcinus and 604 isolates (18.4%) of S. agalactiae were identified by MALTDI-TOF MS. With the manufacturer's cutoff for interpretation, 52.9% of suspected isolates were originally identified as S. pseudoporcinus by MALDI-TOF MS. The remainder, with identification scores of 1.7 to 1.999, were referred for 16S rRNA gene sequencing. Three antigen agglutination kits evaluated with S. pseudoporcinus isolates were found to be positive for B antigen agglutination as follows: PathoDx, 28/30 (93%; in accordance with the Centers of Disease Control and Prevention [CDC] interpretation) (3); Prolex, 13/34 (38.2%); Streptex, 16/30 (53%). In the PathoDx Strep group B latex reagent test, 17 S. pseudoporcinus isolates (57%) reacted strongly, 37% (14 isolates) showed a weak reaction (grainy agglutination), and 6% (2 isolates) did not react. The BD MAX GBS assay did not give a positive result for GBS screening of any of the S. pseudoporcinus isolates selected. In an analysis of antimicrobial susceptibility test results, a lower percentage of clindamycin and erythromycin resistance was found among S. pseudoporcinus isolates by GBS screening (5/32 [15.6%] and 5/32 [15.6%], respectively [Table 1]) than among S. agalactiae isolates (150/3,276 [45.8%] and 203/3,276 [62.0%], respectively [data not shown]; P = 0.003; odds ratio [OR], 3.859; 95% confidence interval [CI], 1.286 to 10.723 [clindamycin resistance]; P = 0.029; OR, 2.803; 95% CI, 0.938 to 7.752 [erythromycin resistance]).
TABLE 1.
Identification and susceptibilities of 34 S. pseudoporcinus isolates
| No. | Specimen typea | Pregnant | Initial MALDI-TOF MS ID scoreb | BD MAX GBS test resultc | Antigen agglutination test resultd |
Susceptibilitye to: |
|||
|---|---|---|---|---|---|---|---|---|---|
| PathoDx | Prolex | Streptex | Clindamycin | Erythromycin | |||||
| 1 | Cervix | Yes | >2.0 | NA | NA | STN | NA | R | R |
| 2 | Vagina | Yes | 1.7–1.999 | Negative | B | STN | STN | S | S |
| 3 | Vagina | Yes | 1.7–1.999 | Negative | B | B | B | S | S |
| 4 | Vagina | Yes | >2.0 | Negative | B (weak) | STN | STN | S | S |
| 5 | Vagina | Yes | >2.0 | NP | STN | STN | STN | S | S |
| 6 | Vagina | Yes | 1.7–1.999 | Negative | B (weak) | STN | STN | S | S |
| 7 | Vagina | Yes | >2.0 | NA | NA | STN | NA | R | R |
| 8 | Vagina | Yes | >2.0 | NA | NA | STN | NA | S | S |
| 9 | Vagina | Yes | 1.7–1.999 | Negative | B (weak) | B | STN | S | S |
| 10 | Vagina | Yes | 1.7–1.999 | Negative | B | STN | B | S | S |
| 11 | Vagina | Yes | >2.0 | Negative | STN | STN | STN | S | S |
| 12 | Vagina | Yes | >2.0 | NP | B (weak) | STN | STN | S | S |
| 13 | Vagina | Yes | >2.0 | NP | B (weak) | STN | STN | R | R |
| 14 | Vagina | Yes | >2.0 | Negative | B | STN | B | S | S |
| 15 | Vagina | Yes | 1.7–1.999 | Negative | B | B | B | S | S |
| 16 | Vagina | Yes | 1.7–1.999 | Negative | B | B | B | S | S |
| 17 | Vagina | Yes | 1.7–1.999 | NP | B | B | B | S | S |
| 18 | Vagina | Yes | >2.0 | Negative | B | STN | B | S | S |
| 19 | Vagina | Yes | 1.7–1.999 | Negative | B | B | B | S | S |
| 20 | Vagina | Yes | 1.7–1.999 | Negative | B | B | B | S | S |
| 21 | Vagina | Yes | >2.0 | Negative | B | B | B | S | S |
| 22 | Vagina | Yes | >2.0 | NP | B | STN | B | S | S |
| 23 | Vagina | Yes | >2.0 | NP | B (weak) | STN | STN | S | S |
| 24 | Vagina | Yes | >2.0 | NP | B (weak) | STN | STN | S | S |
| 25 | Vagina | Yes | >2.0 | NP | B | B | B | S | S |
| 26 | Cervix | No | 1.7–1.999 | NP | B (weak) | STN | STN | R | R |
| 27 | Vagina | No | 1.7–1.999 | NP | B (weak) | STN | STN | S | S |
| 28 | Vagina | No | 1.7–1.999 | NP | B | B | B | R | R |
| 29 | Vagina | No | 1.7–1.999 | NP | B | B | STN | S | S |
| 30 | Cervix | No | 1.7–1.999 | NP | B (weak) | STN | STN | S | S |
| 31 | Vagina | No | >2.0 | NP | B | B | B | S | S |
| 32 | Vagina | No | >2.0 | NP | B | B | B | S | S |
| 33 | Urine | No | >2.0 | NA | NA | STN | NA | NA | NA |
| 34 | Wound | No | 1.7–1.999 | NP | B (weak) | STN | STN | R | R |
Vagina, vaginal-rectal sample.
Subsequent MALDI-TOF MS identification scores of all available S. pseudoporcinus isolates (except isolates 1, 7, 8, and 33) were improved with the addition of more MSP entries to the library database.
NA, isolate not available; NP, not performed.
STN, Streptococcus nontypeable.
S, susceptible; R, resistant.
Of 32 patients with S. pseudoporcinus colonization, 25 were pregnant and 7 were not pregnant (mean age, 27 years; range, 18 to 44 years) (Table 2). Thirty women (93.8%) were African American. All of the colonized patients with underlying obesity were pregnant. Five (16%) patients had underlying diabetes. Thirteen patients (40%) had a history of genitourinary infection. Among the 25 pregnant women, only 1 presented with a history of premature ruptured membranes and 4 developed a fever during delivery and infection of their infants was suspected. In our study, there was no patient with S. pseudoporcinus and S. agalactiae coinfection. The women who developed fever were positive only for S. pseudoporcinus colonization. Using the JHH microbiology laboratory GBS screening and identification protocol, we reported a positive GBS screening result if the isolates carried the B antigen by the Prolex test. We have reported positive GBS screening results for 13 S. pseudoporcinus isolates (9 isolates from pregnant women). However, 19 patients (76%) had received peripartum antimicrobial prophylaxis. The indication for antimicrobial prophylaxis included a positive GBS screening result, a planned caesarean section, and/or a suspected concomitant intrapartum infection such as a urinary tract infection (UTI) or chorioamnionitis. All of the GBS samples from nonpregnant women were collected from patients with a history of abnormal vaginal discharge, and vaginitis was suspected in all seven patients. Some patients had a history of dysuria and dyspareunia.
TABLE 2.
Clinical characteristics of patients colonized with S. pseudoporcinus
| No.a | Specimen typee | Pregnant | Age | Racef | Obesityb | Underlying disease(s)g | Peripartum antibiotic prophylaxis | S. pseudoporcinus clinical infection |
|---|---|---|---|---|---|---|---|---|
| 1 | Cervix | Yes | 28 | AA | No | Smoking | Cefazolin | No |
| 2 | Vagina | Yes | 29 | AA | Yesc | History of UTI, TV | Ceftriaxone | Fever during delivery, suspected neonatal infection |
| 3d | Vagina | Yes | 37 | AA | No | No | Penicillin | No |
| 4 | Vagina | Yes | 28 | AA | Yes | Smoking, history of HSV | Clindamycin | No |
| 5 | Vagina | Yes | 25 | AA | No | NA | NA | NA |
| 6 | Vagina | Yes | 44 | AA | Yesc | History of CT | Penicillin | No |
| 7 | Vagina | Yes | 21 | W | Yesc | Smoking | Cefazolin | No |
| 8 | Vagina | Yes | 33 | AA | Yesc | DM | Penicillin | No |
| 9d | Vagina | Yes | 27 | AA | Yes | No | No | Fever during delivery, suspected neonatal infection |
| 10 | Vagina | Yes | 29 | AA | Yes | No | No | No |
| 11 | Vagina | Yes | 28 | AA | Yes | No | Penicillin | No |
| 12 | Vagina | Yes | 27 | AA | Yesc | DM | No | No |
| 13 | Vagina | Yes | 30 | AA | Yesc | DM, smoking, history of HSV | Cefazolin | No |
| 14 | Vagina | Yes | 27 | AA | Yes | DM, history of HSV | No | No |
| 15d | Vagina | Yes | 23 | AA | Yes | Smoking | Clindamycin | No |
| 16d | Vagina | Yes | 21 | AA | No | Smoking, history of UTI, CT, BV | Ampicillin, gentamicin | Fever during delivery, suspected neonatal infection |
| 17d | Vagina | Yes | 18 | AA | No | No | No | No |
| 18 | Vagina | Yes | 23 | AA | No | History of GC, CT, BV | Cefazolin | No |
| 19d | Vagina | Yes | 30 | AA | Yes | History of GC, CT | Penicillin | No |
| 20d | Vagina | Yes | 24 | AA | Yesc | History of GC, CT | Penicillin, cefazolin | No |
| 21d | Vagina | Yes | 26 | AA | No | DM | Penicillin, cefazolin | No |
| 22 | Vagina | Yes | 25 | AA | Yesc | History of CT | Penicillin | No |
| 23 | Vagina | Yes | 25 | AA | Yesc | UTI | Cefazolin | No |
| 24 | Vagina | Yes | 26 | AA | Yes | Smoking, history of GC, TV | Penicillin, cefazolin | Fever during delivery, suspected neonatal infection |
| 25d | Vagina | Yes | 26 | AA | Yesc | Premature ruptured membranes | Penicillin, cefazolin | No |
| 26 | Cervix | No | 27 | AA | No | No | NA | Vaginitis, UTI |
| 27 | Vagina | No | 24 | AA | No | No | NA | Vaginitis |
| 28d | Vagina | No | 26 | AA | No | History of GC | NA | Vaginitis, positive GC NAAT |
| 29d | Vagina | No | 23 | AA | No | No | NA | Vaginitis |
| 30 | Cervix | No | 39 | AA | No | History of BV | NA | Vaginitis |
| 31d | Vagina | No | 25 | NA | No | NA | Vaginitis and dyspareunia | |
| 32d | Vagina | No | 21 | AA | No | No | NA | Vaginitis and Trichomonas infection |
| 33 | Urine | No | 32 | W | NA | Multiple sclerosis, recurrent UTI | NA | UTI, hematuria, urine culture grew E. coli and S. pseudoporcinus |
| 34 | Wound | No | 50 | AA | NA | DM, endometrial cancer | NA | Posthysterectomy with fever, pelvic abscess with mixed infection |
Thirty-two S. pseudoporcinus isolates were recovered from female genital sources, and two S. pseudoporcinus isolates were from nongenital sources (urine culture and posthysterectomy wound culture).
Obesity was defined as a prepregnancy body mass index of ≥30.
Morbid obesity was defined as a prepregnancy body mass index of ≥40.
Using the JHH microbiology laboratory GBS screening and identification protocol, we reported a positive GBS screening result if the isolates were found to carry the B antigen by the Prolex test.
Vagina, vaginal-rectal sample.
AA, African American; W, white.
NA, data not available; BV, bacterial vaginosis; CT, C. trachomatis infection; DM, diabetes mellitus; GC, gonococcal infection; HSV, herpes simplex virus infection (genital herpes); NAAT, nucleic acid amplification test; TV, T. vaginalis infection.
From the lab database search, we found an additional two isolates of S. pseudoporcinus that were identified by MALDI-TOF MS. One patient had a history of recurrent UTI. The patient presented with hematuria consistent with UTI. A urine culture also grew Escherichia coli along with S. pseudoporcinus. Another isolate was recovered from a surgical wound culture collected from a patient with a history of endometrial cancer who developed fever after a hysterectomy and had a pelvic abscess. This surgical wound culture also grew Enterobacter aerogenes, S. anginosus, and Prevotella species along with S. pseudoporcinus.
This study was a 14-month prospective observational study to evaluate recent data on the prevalence of S. pseudoporcinus at a single institution created as a consequence of beta-hemolytic streptococcus identification by MALDI-TOF MS. Although the clinical significance of S. pseudoporcinus is unclear, microbiologists and clinicians should be aware of this bacterium, as it seems to be associated with clinical syndromes similar to those that involve S. agalactiae. We found a lower prevalence of S. pseudoporcinus colonization in women than in previous studies in the United States (3, 4) and Canada (2) (Table 3). In those studies, the majority of the women with S. pseudoporcinus colonization were African American (3, 4) and from the Caribbean or sub-Saharan Africa (2). In our study, the majority of the women with S. pseudoporcinus colonization were also African American. In addition to S. pseudoporcinus, some (40%) of the patients were also found to have concomitant genitourinary infections or sexually transmitted diseases. These findings are consistent with previous studies (3, 4). Only four pregnant patients had fever, and infections were suspected in their neonates. We did not recover S. pseudoporcinus isolates from the blood or sterile sites of any patients during our study period. In contrast, the previous study reported that 5 (9.1%) of 55 clinical isolates of S. pseudoporcinus were collected from blood cultures (3). However, the majority (76%) of the colonized patients had received peripartum antibiotic prophylaxis, which may have impacted organism recovery from the febrile patients and/or prevented infections in those patients who were colonized.
TABLE 3.
Epidemiology, phenotypic characteristics, and antibiotic susceptibilities of S. pseudoporcinus clinical isolates
| Parameter | Characteristic of reference study |
||||
|---|---|---|---|---|---|
| This study | 1 | 2 | 3 | 4 | |
| Yr or period of isolate collection (duration) | 2014–2015 (14 mo) | 1995–2005 | 1997–2006 | 1984–2010 | 2006 (18 mo) |
| Location(s) | MD, USA | Quebec, Canada | Quebec, Canada | United States, Brazil | United Statesa |
| Patient type(s) | Women | Women | Pregnant women | Men, womenb | Nonpregnant women |
| No. of S. pseudoporcinus isolates | 32 female genital cultures,c 1 urine culture, 1 wound culture | 9 female genital cultures | 14 female genital cultures, 1 urine culture | 72 human sourcesd | 120 female genital cultures (36 patients) |
| Mean (range) or range of patient ages (yr) | 27 (21–44) | 30 (21–49) | 33 (21–43) | NA | 30–40 |
| % S. pseudoporcinus colonization prevalence (no. colonized/total) | 1 (32/3,276) | NAi | NA | NA | 5.4 (36/663) |
| No. (%) of isolates with positive GBS typing, antigen agglutination kit (company) | 28 (93), PathoDx (Remel),e 13 (38), Prolex (Pro-Lab), 16 (53), Streptex (Remel) | 0 (0), Streptex (Murex) | 14 (93), PathoDx (Remel)f | 60 (83), PathoDx (Remel)g | 120 (100), PathoDx (Remel)h |
| Susceptibility test type | Disk diffusion | NA | Disk diffusion | Broth microdilution | NA |
| No. (%) of isolates susceptible to: | |||||
| Clindamycin | 27g (82) | NA | 15 (100) | 70 (97) | NA |
| Erythromycin | 27g (82) | NA | 15 (100) | 70 (97) | NA |
Pittsburgh, PA; Augusta, GA; and Houston, TX.
Three men, 50 women (available clinical characteristics of 50 of 59 patients).
Twenty-five pregnant, 7 nonpregnant.
Blood, wound, cervix, vagina, placenta, throat.
Using the CDC interpretation, PathoDx GBS latex reagent testing revealed that 17 S. pseudoporcinus isolates (57%) reacted strongly and 14 (37%) reacted weakly.
Using Upitt interpretation (4).
Using the CDC interpretation, PathoDx GBS latex reagent testing revealed that 10 S. pseudoporcinus isolates (14%) reacted strongly and 50 (69%) reacted weakly.
Thirty-three isolates were available for susceptibility testing.
NA, data not available.
Outside vaginal colonization and genitourinary infections in pregnant women, to date, only a case report of a thumb infection caused by S. pseudoporcinus has been reported in the literature (10). In our study, we recovered S. pseudoporcinus from a surgical wound that contained mixed pathogens and from the urine of a symptomatic patient who also had an E. coli UTI. Therefore, S. pseudoporcinus infection might not be associated with invasive disease to the same extent that S. agalactiae infection is. More studies are needed to address this hypothesis.
Previous studies reported variability of cross-reactivity of B antigen agglutination tests of S. pseudoporcinus isolates (Table 3) (1–4). In our study, close to 100% of the isolates gave a positive reaction with PathoDx, in contrast to the other kits. We found a higher percentage of strongly positive cross-reactivity of B antigen agglutination tests with PathoDx in accordance with the CDC interpretation than did the study of Shewmaker et al. (57% versus 14%) (3). Lower percentages of S. pseudoporcinus isolates had B antigen cross-reactivity with the Prolex and Streptex kits. A previous study reported that S. pseudoporcinus dairy isolates had no B antigen cross-reactivity with the PathoDx kit (3). This information may be useful when choosing GBS agglutination reagents. Although S. pseudoporcinus and S. agalactiae are beta-hemolytic Gram-positive cocci, S. pseudoporcinus has stronger hemolysis than S. agalactiae. The degree of beta-hemolysis observed can vary by the type of blood agar used for cultures. The combination of colony morphology and B antigen agglutination test results with a less cross-reactive kit would also help to suspect identification of the S. porcinus-S. pseudoporcinus complex (2, 3, 10).
In addition to conventional methods for GBS screening identification, we also reported the use of MALDI-TOF MS and BD MAX GBS assays for S. pseudoporcinus identification. With the manufacturer's cutoff score of 2, only 53% of the isolates were identifiable by MALDI-TOF MS. This poor identification performance was likely related to the limited number of the MS peak (MSP) entries in the database. There is only one MSP of S. pseudoporcinus in the manufacturer's database. Thus, all of the available S. pseudoporcinus isolates were reidentified by MALDI-TOF MS with additional isolates from the JHH database. In the JHH database, MSPs from three additional isolates confirmed as S. pseudoporcinus by 16S rRNA gene sequencing were added to the database. With the manufacturer's cutoff score of 2, MALDI-TOF MS was able to reidentify all (100%) of the S. pseudoporcinus isolates (data not shown). As expected, the BD MAX GBS assay is very specific for the detection of S. agalactiae (10) and no false-positive results with S. pseudoporcinus isolates were seen in our limited testing.
Although the prevalence of S. pseudoporcinus colonization of women in our hospital was low, we found a higher rate of clindamycin and erythromycin resistance (18% for both) than in previous studies (0 to 3%) (Table 3) (2–4). Previous studies reported that S. pseudoporcinus is highly susceptible to β-lactam antibiotics (2, 3).
Our study had some limitations. This was a prospective observational study performed at a single institution. The patient population might be different from that in other places. At the JHH microbiology laboratory, we no longer use conventional biochemical testing for GBS or S. agalactiae confirmation. Thus, the hippurate hydrolysis test and CAMP test were not performed. We did not perform antimicrobial susceptibility testing by the broth microdilution method, and we did not test for β-lactam antibiotic susceptibility.
In conclusion, new approaches to bacterial identification in routine clinical microbiology laboratories may affect the prevalence of S. pseudoporcinus. The rate of clindamycin and erythromycin resistance we found among S. pseudoporcinus isolates was higher than that in previous studies but lower than that observed for GBS. The clinical significance of genitourinary S. pseudoporcinus, patients' clinical characteristics, and their relationship to peripartum neonatal and maternal infections requires further investigation.
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