J Med Microbiol 56 (2007), 1246-1249; DOI: 10.1099/jmm.0.47180-0
© 2007 Society for General Microbiology
ISSN 1473-5644
Invasive infection with Streptococcus iniae in Taiwan
Jun-Ren Sun1,
Juh-Cheng Yan2,
Ching-Ying Yeh1,
Shih-Yi Lee1 and
Jang-Jih Lu1
1 Division of Clinical Pathology, Department of Internal Medicine, Tri-Service General Hospital and National Defense Medical Center, Taipei, Taiwan, ROC
2 Department of Pathology, Division of Gastroenterology and Hepatology, Department of Internal Medicine, Tri-Service General Hospital and National Defense Medical Center, Taipei, Taiwan, ROC
Correspondence
Jang-Jih Lu
jjl{at}ndmctsgh.edu.tw
Received 21 January 2007
Accepted 18 April 2007
Streptococcus iniae, a common fish pathogen, rarely infects humans. In this report, a case of invasive S. iniae infection in a 51-year-old woman with diabetes mellitus and hepatitis C-related liver cirrhosis is described. The isolate was identified by 16S rDNA sequencing. The patient recovered after 1 week of treatment with ampicillin.
 |
Introduction
|
|---|
Streptococcus iniae was first isolated in 1976 from skin lesions of Amazon freshwater dolphins (Inia geoffrensis) in the United States (Peir & Madin, 1976). It has been found to cause meningoencephalitis in tilapia, coho salmon, rainbow trout and yellowtail, and necrotizing myositis in red drum (Weinstein et al., 1997). Many outbreaks of S. iniae infection with high mortality rates in aquaculture farms all over the world have been reported (Weinstein et al., 1997). Asymptomatic carriage in some fish, such as barramundi and tilapia, has been observed (Shoemaker et al., 2001). The bacterium was first recognized to cause human infection in 1991 in North America (CDC, 1996; Weinstein et al., 1997). In this report, we describe what is believed to be the first case of invasive human S. iniae infection in Taiwan.
|
Case report
|
|---|
A 51-year-old woman was admitted to the Tri-Service General Hospital on July 7, 2003, because of week-long intermittent sweats, fever, dyspnoea and abdomen distension. The patient had a history of diabetes mellitus and hepatitis C-related liver cirrhosis. At admission, she had a temperature of 36.6 °C, a distended abdomen with prominent shifting dullness and a linear scar on the right thumb, but had no wound or injury on the extremities. Three days after admission, the patient had a low-grade fever up to 38 °C with abdomen distension. The blood leukocyte count was 20 000 cells ml–1, and neutrophils were predominant. During a febrile chill the patient's ascitic fluid was tapped, and the leukocyte count was 1000 cells ml–1.
Only blood and ascitic fluid were submitted for bacteriological culture. On the second day of incubation, the aerobic blood culture bottle (BacT/ALERT; bioMérieux) showed Gram-positive cocci arranged in chains. The organism grew on blood agar as slightly mucoid, ß-haemolytic colonies of 1 to 2 mm in diameter after 24 h of incubation at 37 °C, 5 % CO2. The isolate was positive for pyrrolidonyl arylamidase and arginine dihydrolase, and negative for catalase, bile aesculin and Voges–Proskauer tests. It was non-groupable by the Lancefield group A, B, C, D, F or G antisera. Both the Vitek (GPI) and API 20 Strep systems failed to identify the organism. The first 804 bp fragment of the 16S rRNA gene of the isolate was amplified and sequenced in our in-house laboratory. The sequence was found to be identical to that of S. iniae strain ATCC29178 16S rRNA gene (GenBank accession no. AF335572). The isolate was susceptible to ampicillin, penicillin, erythromycin and vancomycin, and intermediately resistant to chloramphenicol and clindamycin by antimicrobial disc diffusion tests (performed according to Clinical and Laboratory Standards Institute guidelines M100-S15 and M2-A7). Based on clinical and laboratory findings, the patient was treated with 500 mg ampicillin every 6 h for a week and recovered.
The patient described in this report was asked specifically about exposure to fresh fish or other aquatic creatures before she became ill. She did not remember having prepared fresh fish before the admission. However, her husband is a fishmonger and sells fish in the market every morning. It is possible that she acquired S. iniae from him, although he was not screened for S. iniae carriage.
|
Discussion
|
|---|
S. iniae was first recognized to cause human infections in 1995 when nine Asian patients in Toronto had invasive S. iniae infections (Weinstein et al., 1997). Eight of these nine patients had bacterial hand cellulitis and one patient had endocarditis, meningitis and arthritis (Weinstein et al., 1997). Based on the data from the Centers for Disease Control and Prevention (CDC) Microbiology Laboratory, two additional cases were discovered retrospectively, including a patient from Texas, USA, with bacterial cellulitis in 1991 and a cook from Ottawa, Canada, with septic arthritis of the knee in 1994 (CDC, 1996). The first two cases of S. iniae infection outside North America were found in Hong Kong in 2001 (Lau et al., 2003); one patient had bacterial cellulites, and the other patient had bacteraemic osteomyelitis of the spine. In 2003, another case of spinal infection caused by S. iniae was reported in Singapore (Koh et al., 2004). In 2004, two additional cases of invasive S. iniae infection were reported in Hong Kong, including one patient with septic arthritis presenting as acute exacerbation of chronic gout and the other with bacterial cellulites (Lau et al., 2006). As summarized in Table 1
, Asian ethnic origin, old age and underlying medical conditions (such as diabetes mellitus and cirrhosis of liver) appear to be risk factors for S. iniae infection (Koh et al., 2004; Lau et al., 2003, 2006; Weinstein et al., 1997). The patients median age was 71 years (mean 70.3, range 40 to 88), and the female: male ratio was 11 : 12. Asians (22/26, 13/26 were described as Chinese) are particularly at risk, probably because of their preference for eating fresh fish. Fresh whole fish are often purchased from the retail wet markets followed by scaling, cutting, and removal of fins and internal organs with bare hands (Lau et al., 2006).
View this table:
[in this window]
[in a new window]
|
Table 1. Demographics of patients with reported S. iniae invasive infections
The patient described in this paper is indicated in bold.
|
|
While clinicians need to be aware of the circumstances where S. iniae infections should be considered, microbiology laboratory staff should also pay special attention to specimens from patients with a history of fish handling. S. iniae grows slowly on solid medium at room temperature. Under such growth conditions, the ß-haemolysis of S. iniae may not be evident, and it may therefore be misidentified as a viridans streptococcus and considered as a contaminant (Weinstein et al., 1997). Because S. iniae is not included in the database of all commercial systems for bacterial identification, previously reported isolates were either unidentified or misidentified as Streptococcus uberis or Streptococcus dysgalactiae (Facklam et al., 2005; Lau et al., 2003, 2006; Weinstein et al., 1997). As suggested by Koh et al. (2004), all ß-haemolytic streptococci ungroupable by the Lancefield grouping method and positive for pyrrolidonyl arylamidase should be suspected to be S. iniae. A recent study showed that S. iniae may be differentiated from other pyrrolidonyl arylamidase-positive, ß-haemolytic streptococci, such as Streptococcus pyogenes and Streptococcus porcinus, by conventional tests (Facklam et al., 2005). Although S. pyogenes can be readily identified by its group A carbohydrate antigen in Lancefield grouping, S. porcinus may possess groups E, P, U or V, or new antigens that are usually not included in the battery of antisera in clinical laboratories, and therefore would also be non-groupable. The Voges–Proskauer test, starch hydrolysis and acid production from sorbitol appeared to be useful for differentiation from S. porcinus. As PCR and sequencing techniques become more readily available in clinical laboratories, nucleic acid-based diagnostic techniques, such as 16S rDNA sequencing, should be performed to identify S. iniae. Several gene targets, including chaperonin 60 (Poyart et al., 1998), lactate oxidase (Mata et al., 2004) and 16S–23S spacer (Berridge et al., 1998), have also been used successfully to identify S. iniae.
S. iniae isolates causing disease in fish or humans were shown to belong to a single clone by PFGE, while isolates from healthy fish were genetically diverse in Canada (Facklam et al., 2005; Fuller et al., 2001). In vitro models have shown that disease-associated S. iniae strains were more resistant to phagocytic clearance than non-disease-causing strains, and exhibited direct cytotoxicity to human endothelial cells unlike the non-disease-causing strains (Fuller et al., 2001). Moreover, only the disease-associated strains were found to cause significant weight loss and bacteraemia in a mouse model of subcutaneous infection (Fuller et al., 2001). However, the PFGE patterns of Hong Kong isolates were different from Canadian isolates (Lau et al., 2003, 2006), suggesting that invasive S. iniae infections can be caused by strains with different genetic profiles, and perhaps a different pathogenic strain was prevalent in Asia. Morphologically, colonies of the isolate in the present study appear larger, more ß-haemolytic and mucoid than the clinical isolates from North America (Koh et al., 2004; Lau et al., 2003, 2006). Similar to our isolate, colonies of Hong Kong strains were also larger, more ß-haemolytic and mucoid. This observation suggests that invasive S. iniae infections in Asia may have been missed as a result of their non-typical appearance.
A careful retrospective review of our laboratory records revealed that S. iniae infection in Taiwan is uncommon: in the past 3 years we have grouped 2425 ß-haemolytic streptococci isolated in our laboratory and all have been typable by Lancefield group A, B, C, D, F or G antisera. However, the reported prevalence of this emerging zoonosis is likely to increase.
|
ACKNOWLEDGEMENTS
|
|---|
This study was supported by grants DOD-92-54 and TSGH-C95-40 from the Department of Defense and Tri-Service General Hospital, Taiwan, ROC.
|
REFERENCES
|
|---|
Berridge, B. R., Fuller, J. D., de Azavedo, J., Low, D. E., Bercovier, H. & Frelier, P. F. (1998). Development of specific nested oligonucleotide PCR primers for the Streptococcus iniae 16S–23S ribosomal DNA intergenic spacer. J Clin Microbiol 36, 2778–2781.[Abstract/Free Full Text]
CDC (1996). Invasive infection with Streptococcus iniae – Ontario, 1995–1996. MMWR Morb Mortal Wkly Rep 45, 650–653.[Medline]
Facklam, R., Elliott, J., Shewmaker, L. & Reingold, A. (2005). Identification and characterization of sporadic isolates of Streptococcus iniae isolated from humans. J Clin Microbiol 43, 933–937.[Abstract/Free Full Text]
Fuller, J. D., Bast, D. J., Nizet, V., Low, D. E. & de Azavedo, J. C. (2001). Streptococcus iniae virulence is associated with a distinct genetic profile. Infect Immun 69, 1994–2000.[Abstract/Free Full Text]
Koh, T. H., Kurup, A. & Chen, J. (2004). Streptococcus iniae discitis in Singapore. Emerg Infect Dis 10, 1694–1696.[Medline]
Lau, S. K., Woo, P. C., Tse, H., Leung, K. W., Wong, S. S. & Yuen, K. Y. (2003). Invasive Streptococcus iniae infections outside North America. J Clin Microbiol 41, 1004–1009.[Abstract/Free Full Text]
Lau, S. K., Woo, P. C., Luk, W. K., Fung, A. M., Hui, W. T., Fong, A. H., Chow, C. W., Wong, S. S. & Yuen, K. Y. (2006). Clinical isolates of Streptococcus iniae from Asia are more mucoid and ß-hemolytic than those from North America. Diagn Microbiol Infect Dis 54, 177–181.[CrossRef][Medline]
Mata, A. I., Blanco, M. M., Dominguez, L., Fernandez-Garayzabal, J. F. & Gibello, A. (2004). Development of a PCR assay for Streptococcus iniae based on the lactate oxidase (lctO) gene with potential diagnostic value. Vet Microbiol 101, 109–116.[CrossRef][Medline]
Peir, G. B. & Madin, S. H. (1976). Streptococcus iniae sp. nov., a beta-hemolytic streptococcus isolated from an Amazon freshwater dolphin, Inia geoffrensis. Int J Syst Bacteriol 26, 545–553.[Abstract/Free Full Text]
Poyart, C., Quesne, G., Coulon, S., Berche, P. & Trieu-Cuot, P. (1998). Identification of streptococci to species level by sequencing the gene encoding the manganese-dependent superoxide dismutase. J Clin Microbiol 36, 41–47.[Abstract/Free Full Text]
Shoemaker, C. A., Klesius, P. H. & Evans, J. J. (2001). Prevalence of Streptococcus iniae in tilapia, hybrid striped bass, and channel catfish on commercial fish farms in the United States. Am J Vet Res 62, 174–177.[CrossRef][Medline]
Weinstein, M. R., Litt, M., Kertesz, D. A., Wyper, P., Rose, D., Coulter, M., McGeer, A., Facklam, R., Ostach, C. & other authors (1997). Invasive infections due to a fish pathogen, Streptococcus iniae. S. iniae Study Group. N Engl J Med 337, 589–594.[Abstract/Free Full Text]
TOP
Introduction
Case report
