Asymptomatic Carriage of Sequence Type 398, spa Type t571 Methicillin-Susceptible Staphylococcus aureus in an Urban Jail: a Newly Emerging, Transmissible Pathogenic Strain

Abstract

Sequence type 398 (ST398) Staphylococcus aureus, frequently carried by livestock, has caused severe human infections and often carries transmissible antibiotic resistance genes. Among methicillin-susceptible S. aureus isolates colonizing Dallas County Jail detainees, 13.2% were ST398, spa type t571, and were genetically similar to human colonization isolates from New York, Chicago, and the Dominican Republic.

TEXT

Sequence type 398 (ST398) methicillin-resistant Staphylococcus aureus (MRSA) is often transmitted among livestock and animal handlers but is uncommonly associated with human disease in the United States (1). We unexpectedly identified ST398/t571 methicillin-sensitive S. aureus (MSSA) as the most common genetic background among MSSA isolates colonizing detainees in the Dallas County Jail. In this study, we compared the pulsed-field gel electrophoresis (PFGE) pulsotypes of isolates from the Dallas jail and from a single patient in Chicago with those of strains isolated in previous studies.

Recognized first in Europe (2–9), ST398 MRSA has been isolated in the United States (10), Canada (11), and Latin America (12). ST398 methicillin-susceptible S. aureus (MSSA) isolates have been recovered from pigs (13), humans (14–17), and retail meat (18). Asymptomatic human colonization and infection with ST398 MSSA are rare in the United States and Europe (19–21). However, in New York City in 2004 to 2007, 13 people, mostly of Dominican origin, had nasal carriage of ST398 MSSA with the unusual spa type t571 (ST398/t571) (22). In addition, patients in the Dominican Republic in 2007-2008 were infected by ST398/t571 MSSA (22), as were patients in New Jersey (23).

In January 2009, we screened the anterior nares and the hands of 928 detainees, housed in 68 divisions, called tanks, in the Dallas County Jail, for S. aureus carriage. Tanks had a capacity of 24 to 36 detainees. Detainees can interact with others within a single tank but have little interaction with those in other tanks. The study was approved by the Institutional Review Boards at the University of Chicago Medical Center and the University of Texas-Southwestern Medical Center. Recovered MSSA isolates were genotyped from subjects housed in a stratified random sample of 26 of the 68 tanks; all MRSA isolates were genotyped.

In a separate study of S. aureus colonization among patients and household contacts (24), we also identified one patient in Chicago with ST398/t571 MSSA colonization.

Multilocus sequence typing (MLST) (25), spa typing (26), PCR for the Panton-Valentine leukocidin (PVL) genes (27), and PFGE using Cfr9I digestion (22, 28) were performed. Antimicrobial susceptibilities were determined by automated testing (29).

Among the 345 subjects in the 26 selected tanks, 110 (31.9%) carried MSSA. Of 158 MSSA isolates identified, 152 were available, and 34 MLST types were identified. Twenty isolates (13%) were ST398, the most common ST; all lacked PVL genes. Of the 345 subjects, the 16 (4.6%) who carried the 20 ST398 MSSA isolates were more likely than carriers of other MSSA genetic backgrounds to be female (P = 0.0009) and older (P = 0.01) (Table 1).

Table 1.

Demographic characteristics of ST398 MSSA carriers and subjects carrying other MSSA sequence types in Dallas County Jail

Characteristic	Detainees carrying ST398 MSSA (n = 16)	Detainees carrying other MSSA backgrounds (n = 95)	P value
Gender, no. (%)
Male	7 (44)	77 (81)	0.0009
Female	9 (56)	23 (19)
Race, no. (%)
White	7 (44)	52 (55)	0.5
Black	8 (50)	41 (43)
Unknown	1 (6)	2 (2)
Ethnicity, no. (%)
Hispanic	3 (19)	24 (25)	0.8
Non-Hispanic	13 (81)	70 (74)
Unknown	0	1 (1)
Age, yrs, mean ± SD	40.6 ± 9.5	33.3 ± 10.7	0.01
Median duration of stay in jail, days (range)	50.5 (1–245)	74 (1–675)	0.3

Among the 20 ST398 isolates, 18 were susceptible to ciprofloxacin, gentamicin, rifampin, and trimethoprim-sulfamethoxazole and resistant to clindamycin and erythromycin. The two other isolates differed in that one was susceptible to clindamycin and the other was resistant to ciprofloxacin.

All 20 MSSA ST398 isolates shared the same pulsotype (Fig. 1) and spa type t571. All ST398/t571 MSSA carriers were housed in 4 of the 26 (15%) tanks, designated tanks A, B, C, and D. In tank A, samples from 20 (63%) of the 32 female detainees were cultured; ST398/t571 MSSA was carried by 9 of 17 (53%) S. aureus carriers. All ST398/t571 isolates from tank A shared a common antibiogram. One subject who carried ST398/t571 on the hand had an MSSA isolate obtained from her nose, not available for genotyping, that shared the same antibiogram as the ST398/t571 isolates in tank A, suggesting that it may have been ST398/t571. The culture results from tanks A, B, C, and D are shown in Table 2.

Fig 1.

Analysis of PFGE patterns of ST398 isolates from the Dallas County Jail (C2018, C4159, and C2095; all are spa type t571), New York State Prisons (9657 [t6864], 9834 [t571], and 9323 [t6587]) (30), Chicago colonization isolates (9129320 [t571] and 9129321 [t571]), Northern Manhattan (51166 [t571] and MS553 [t6608], and MS298 [t1451]) (22). Band patterns are compared using the Dice coefficient.

Table 2.

S. aureus culture from nares and hand carriage in tank A, in which all subjects were female, and tanks B, C, and D, in which all subjects were male

Tank	Subject	Length of stay in jail (days)	Hand culturee		Nares culturee
			Result	Genotypea	Result	Genotypea
A	1	56	MSSA	398/pvl−	neg	NA
A	2	8	MSSA	398/pvl−	neg	NA
A	3	25	MSSA	15slvb/pvl−	MSSA	959/pvl−
A	4	91	neg	NA	MSSA	NTc/pvl−
A	5	1	MSSA	1860/pvl−	MSSA	398/pvl−
A	6	4	MSSA	1860/pvl−	MSSA	72/pvl−
A	7	113	MSSA	398/pvl−	MSSA	398/pvl−
A	8	101	MSSA	398/pvl−	MSSA	97/pvl−
A	9	26	MSSA	1860/pvl−	MSSA	72/pvl−
A	10	10	neg	NA	neg	NA
A	11	4	MRSA	8/IV/pvl+	neg	NA
A	12	66	MSSA	398/pvl−	MSSA	Not typedd
A	13	2	MSSA	5/pvl−	neg	NA
A	14	16	neg	NA	neg	NA
A	15	67	MRSA	8/IV/pvl+	neg	NA
A	16	57	neg	NA	neg	NA
A	17	45	MSSA	398/pvl−	neg	NA
A	18	1	MRSA	8/IV/pvl+	neg	NA
A	19	21	neg	NA	MSSA	398/pvl−
A	20	245	MSSA	398/pvl−	MSSA	398/pvl−
B	21	445	neg	NA	MSSA	432/pvl−
B	22	21	MSSA	398/pvl−	MSSA	398/pvl−
B	23	15	MSSA	398/pvl−	MSSA	8/pvl+
B	24	69	MSSA	398/pvl−	MSSA	398/pvl−
B	25	53	neg	NA	neg	NA
B	26	131	neg	NA	MSSA	398/pvl−
B	27	22	MSSA	630/pvl−	neg	NA
C	28	18	neg	NA	MSSA	8/pvl−
C	29	7	MSSA	188/pvl+	MSSA	188/pvl−
C	30	80	MSSA	434/pvl−	MSSA	398/pvl−
C	31	7	neg	NA	MSSA	45/pvl−
D	32	197	neg	NA	MRSA	Not typedd
D	33	66	MSSA	1/pvl−	neg	NA
D	34	45	neg	NA	MRSA	30/IV/pvl+
D	35	38	neg	NA	neg	NA
D	36	49	MRSA	8/IV/pvl+	MRSA	8/IV/pvl+
D	37	42	neg	NA	MSSA	398/pvl−
D	38	22	MSSA	6/pvl−	neg	NA
D	39	11	neg	NA	neg	NA
D	40	18	neg	NA	neg	NA
D	41	149	MSSA	6/pvl−	MSSA	6/pvl−
D	42	23	neg	NA	MSSA	398/pvl−
D	43	23	neg	NA	MSSA	8/pvl+
D	44	78	neg	NA	neg	NA
D	45	184	neg	NA	MSSA	Not typedd
D	46	84	neg	NA	MSSA	8/pvl+
D	47	150	MSSA	6/pvl−	MSSA	6/pvl−
D	48	213	neg	NA	neg	NA
D	49	7	neg	NA	neg	NA
D	50	215	neg	NA	MSSA	Not typedd
D	51	71	neg	NA	neg	NA
D	52	16	neg	NA	neg	NA
D	53	222	neg	NA	neg	NA

^aFormat for genotype is ST/SCCmec type (for MRSA isolates)/presence (pvl+) or absence (pvl−) of carriage of the PVL genes. NA, not applicable.

^b“15slv” indicates a single-locus MLST variant of ST15.

^c“NT” signifies a new MLST type not yet reported in the MLST database.

^dIsolate was not available for genotyping.

^eneg, negative.

For the skin and soft tissue infection (SSTI) patient from Chicago, ST398/t571 MSSA was isolated from the nose and throat. None of his 4 household contacts and no other subject in our study of 350 households was colonized with an MSSA or MRSA ST398 isolate (24).

As determined by PFGE, ST398 isolates from the Dallas County Jail, from New York State Prisons (30), from the patient in Chicago, and from northern Manhattan (22) all shared PFGE patterns with >80% identity by Dice coefficient analysis (Fig. 1). This suggests that this genetic background may be identified in geographic pockets across the United States.

The finding of 9 subjects in a single jail tank with carriage of ST398/t571 MSSA isolates with a common pulsotype suggests local spread and easy transmissibility. No other MSSA strain had a similarly wide distribution in a single tank. This finding contrasts with data from the Netherlands, where ST398 MRSA isolates were less transmissible in the hospital than other MRSA genetic backgrounds (31). Also, carriage of ST398 MRSA by animal workers is often transient and related to persistent exposure to animals (32). It is not known if the ST398/t571 MSSA isolates in our study caused only transient carriage, as shown in the study of ST398 MRSA.

Limitations of the study were that it was cross-sectional and that few demographic data were available for each subject.

ST398 MRSA strains may carry and transfer to other S. aureus backgrounds transposons encoding genes for tetracycline resistance (33, 34) or have resistance to pleuromutilin and lincosamide antimicrobials (4, 35–37). ST398 isolated from humans has been found to carry phages that encode human innate immune modulators (38). Many spa types have been associated with the ST398 background (39), and the t571 type has likely been derived on more than one occasion from strains with related spa types (40).

ST398/t571 MSSA has been found rarely among S. aureus isolates identified in studies of colonization in humans (15, 41, 42) or livestock (43, 44). However, in the United States and Europe, ST398/t571 MSSA isolates have caused fatal necrotizing pneumonia, SSTIs, and bloodstream infections (8, 16, 39, 45–48; N. van der Mee Marquet, personal communication) and after 2001 caused sterile site infections in China (49, 50).

Among ST398 MRSA, ST398/t571 MRSA isolates have been isolated rarely in studies of humans (5, 9, 51–56) or livestock (2, 3, 6, 11, 57), although they were common in an animal study from Peru (12).

The apparent ease of transmission of ST398/t571 MSSA in community settings in the absence of an animal reservoir, the frequent identification of ST398 strains among livestock, concerns about novel mechanisms of resistance in ST398 strains, and reports of invasive infections caused by ST398/t571 MSSA isolates all suggest that continued genotypic surveillance of S. aureus strains in humans and animals is warranted.