Original Article
Invasive Infections Due to a Fish Pathogen, Streptococcus iniae
N Engl J Med 1997; 337:589-594August 28, 1997
- Abstract
Background
Streptococcus iniae is a pathogen in fish, capable of causing invasive disease and outbreaks in aquaculture farms. During the winter of 1995–1996 in the greater Toronto area there was a cluster of four cases of invasive S. iniae infection in people who had recently handled fresh, whole fish from such farms.
Methods
We conducted a prospective and retrospective community-based surveillance for cases of S. iniae infection in humans. To obtain a large sample of isolates, we studied cultures obtained from the surface of fish from aquaculture farms. Additional isolates were obtained from the brains of infected tilapia (oreochromis species). All the isolates were characterized by pulsed-field gel electrophoresis (PFGE).
Results
During one year, our surveillance identified a total of nine patients with invasive S. iniae infection (cellulitis of the hand in eight and endocarditis in one). All the patients had handled live or freshly killed fish, and eight had percutaneous injuries. Six of the nine fish were tilapia, which are commonly used in Asian cooking. Thirteen additional S. iniae isolates (2 from humans and 11 from infected tilapia) were obtained from normally sterile sites. The isolates from the nine patients were indistinguishable by PFGE and were highly related to the other clinical isolates. There was substantial genetic diversity among the 42 surveillance isolates from the surface of fish, but in 10 isolates the PFGE patterns were identical to those from the patients with S. iniae infection.
Conclusions
S. iniae can produce invasive infection after skin injuries during the handling of fresh fish grown by aquaculture. We identified a clone of S. iniae that causes invasive disease in both humans and fish.
Media in This Article
Figure 1
A Tilapia (Oreochromis Species), Also Known as St. Peter's Fish or Hawaiian Sunfish.Figure 2
PFGE Analyses of Strains of S. iniae after the Digestion of Chromosomal DNA with Smal.Article Activity
- Article
Streptococcus iniae was first reported in 1976 to cause subcutaneous abscesses in Amazon freshwater dolphins (Inia geoffrensis) at aquariums in San Francisco and New York.1,2 Since the early 1980s, epizootic meningoencephalitis caused by streptococci has been recognized as an important cause of morbidity and mortality in cultured fishponds.3-8 Outbreaks in Japan, Taiwan, Israel, and the United States have affected tilapia (oreochromis species), yellowtail (Seriola quinqueradiata), rainbow trout, and coho salmon.3-10 Several bacteria, including S. iniae, S. agalactiae, 6,11 and Lactococcus garvieae, 12,13 have been shown to cause meningoencephalitis in fish grown by aquaculture. S. iniae may colonize the surface of fish or cause invasive disease associated with 30 to 50 percent mortality in affected fishponds.6 Infected tilapia become lethargic, swim erratically, have dorsal rigidity, and die within several days. Pathological studies show extensive infection in the central nervous system.7
During the winter of 1995–1996, four persons in the greater Toronto area had bacteremic illnesses due to S. iniae infection. Three had cellulitis, and the fourth had sepsis with endocarditis, meningitis, and arthritis. All the patients were of Asian descent and reported having recently prepared whole, fresh fish for cooking. In three cases the fish was identified as tilapia (also known as St. Peter's fish or Hawaiian sunfish) (Figure 1Figure 1
A Tilapia (Oreochromis Species), Also Known as St. Peter's Fish or Hawaiian Sunfish.). We conducted an investigation of the clinical features and epidemiology of this illness.Methods
Patients
After the first four patients (Patients 1 to 4) were identified at a community hospital in the greater Toronto area (population, 4.2 million) between December 1995 and February 1996,14,15 retrospective and prospective surveillance was carried out to identify additional patients. Twelve hospitals in greater Toronto were invited to participate. Infection-control practitioners were asked to review their medical records according to the codes defined in the International Classification of Diseases, 9th Revision (ICD-9) for all patients hospitalized with cellulitis in the upper limb from October 1, 1995, through March 31, 1996, when there was no predisposing cause for the cellulitis, such as an intravenous line in place, a burn, a chronic skin disease, or lymphedema. Patients were excluded from the study if their blood cultures revealed an etiologic agent other than S. uberis, S. iniae, or some other, unidentified streptococcal species. Once identified, the patients were interviewed with a standardized questionnaire to obtain clinical and epidemiologic data. Beginning on April 1, 1996, the emergency departments at the hospitals were asked to identify prospectively patients who presented with acute upper-limb cellulitis.
Patients in whom S. iniae was isolated from any sterile body site were considered to have confirmed cases of invasive disease. Patients with diagnosed upper-limb cellulitis who had handled fresh, whole fish within the 72 hours before the onset of signs and symptoms were considered to have suspected cases.
Additional Patients and Isolates of S. iniae
We reviewed the records of the Centers for Disease Control and Prevention (CDC), Atlanta; the Public Health Laboratory of Ontario, Toronto; and the National Centre for Streptococcus, Edmonton, Alberta, to determine whether S. iniae had been identified previously. To determine whether workers whose jobs included processing whole fish had had cellulitis, we reviewed injury claims made to the Workers' Compensation Board of Ontario over the preceding five years.
All live tilapia imported to greater Toronto originate in fishponds in the United States. A sample of such fish was taken to identify the extent to which the surface of the fish was colonized with S. iniae. In May and June 1996, officials of the Canadian Department of Fisheries and Oceans identified five shipments of tilapia that entered Canada from five of the seven U.S. farms supplying Toronto. At least three live tilapia were randomly selected from each shipment, and a culture was taken from the surface of each fish.
In addition, surface cultures were obtained from fish grown by aquaculture and purchased at retail in greater Toronto and in Vancouver (courtesy of Dr. N. Press and E.A. Bryce, Vancouver Hospital Health Science Centre). Clinical isolates were also received from tilapia that had acquired meningoencephalitis during epizootics in 1993 in Texas and Virginia (CDC and courtesy of Dr. P. Frelier, Texas A&M University). Strains of S. iniae from the American Type Culture Collection (ATCC, Rockville, Md.; types 29177 and 29178) were used as controls.
Epidemiologic Investigation
We attempted to identify the source of the live tilapia responsible for the infections in humans by tracing the origin of the tilapia sold by retailers to the first four patients. We studied the purchase orders from these retailers and their wholesale suppliers that corresponded to a six-week period preceding the purchase of the fish, because live tilapia may be stored that long before being sold at market. We used importation records from the Inspection Branch of the Department of Fisheries and Oceans to confirm the origin of the live tilapia.
Microbiologic Analysis
Isolates were identified as S. iniae by standard microbiologic methods.1,2,16 The characteristics used to identify streptococcal species as S. iniae were that they had a β-hemolytic reaction on trypticase soy agar with 5 percent sheep's blood; that they were not groupable with Lancefield groups A through V antiserum; that they were susceptible to vancomycin, not gas-producing, nonmotile, and positive for pyrolidonyl arylamidase and leucine aminopeptidase; and that they produced negative results on bile–esculin, Voges–Proskauer, and hippurate tests. Most strains grew at 10°C but not at 45°C, and most did not grow in 6.5 percent sodium chloride. We used a commercial system (Bio-Mérieux Vitek, Hazelwood, Mo.) that identified the isolates as S. uberis or reported them as “unidentified,” since S. iniae is not included in the data base.
Surface swabs obtained from fresh, whole fish were inoculated onto colistin–nalidixic acid blood agar (Unipath, Basingstoke, United Kingdom) and incubated at 35°C in 5 percent carbon dioxide for 18 to 24 hours. In vitro susceptibility testing was carried out by broth microdilution according to the methods of the National Committee for Clinical Laboratory Standards.17
Molecular Typing
Pulsed-field gel electrophoresis (PFGE) was performed on all isolates of S. iniae obtained from humans and fish. PFGE was performed with the CHEF DRII apparatus (Bio-Rad, Mississauga, Ont., Canada) and restriction endonucleases SmaI and ApaI (Boehringer Mannheim, Mannheim, Germany), with use of a modified version of the method of Murray et al.18 The modifications included the supplementation of the Enzyme Commission lysis buffer with 20 μg of mutanolysin per milliliter (Sigma Chemical, Mississauga), a reduction in lysis time from overnight to 2 to 5 hours, and the use of the following for electrophoresis: pulse times of 5 to 60 seconds, a temperature of 12°C, and 175 V for 20 hours. Standard interpretive criteria were used to assess the PFGE patterns.19
Results
Clinical Findings and Characteristics
Eleven of the 12 hospitals agreed to review their clinical records for cases of cellulitis, and 10 of them completed the review. Thirteen emergency departments from 3 tertiary care and 10 community hospitals participated in the prospective case finding.
From December 1995 through December 1996, nine patients with bacteremic S. iniae infections were identified (Table 1Table 1
Demographic Characteristics of Patients with Culture-Confirmed Cases of Invasive S. iniae Infection.). Their median age was 69 years (mean, 67.0; range, 40 to 80), and the female:male ratio was 2:1. All the patients with confirmed infections were of Asian descent: eight Chinese and one Korean. All the patients reported preparing whole, raw fish, and eight patients recalled injuring their hands by puncturing the skin with the dorsal fin, a fish bone, or a knife used in the cleaning and scaling. None had prior breaks in the skin. Six patients were able to identify the fish they were preparing as tilapia; three were not certain of the species. No fish remained for possible culture. For all the clinical isolates tested, the minimal inhibitory concentrations of penicillin, cefazolin, ceftriaxone, erythromycin, clindamycin, and trimethoprim–sulfamethoxazole were 0.25 μg per milliliter or less; that of ciprofloxacin was 0.5 μg per milliliter; and that of gentamicin was 16 μg per milliliter.Eight of the nine patients had cellulitis of the hand. They all had similar clinical presentations, with fever and lymphangitis originating from the site of injury. The cellulitis developed within 16 to 24 hours after the injuries. No patient had evidence of skin necrosis or bulla formation. The leukocyte counts were elevated (range, 12,900 to 33,400 cells per cubic millimeter), with neutrophil predominances and leftward shifts. Patient 4, who did not have cellulitis, met the Duke criteria for infective endocarditis20 of the mitral valve. He also had clinical and laboratory evidence of meningitis and arthritis in his right knee, but cerebrospinal and synovial fluid cultures performed 12 hours after the start of treatment with appropriate antibiotics were negative. All the patients were admitted to the hospital and given parenteral antibiotics; they responded to treatment within two to four days (Table 1).
Twelve patients with suspected cases of S. iniae infection were identified. Their median age was 46 years (mean, 50.0; range, 36 to 68), and the female:male ratio was 1:1. Eleven of the patients with suspected infections were of Asian origin; one was white. All reported having injured themselves while handling whole or partially prepared fresh fish. Nine reported the fish as being tilapia, and one as bass; the remaining two did not know the type of fish they had been preparing. One patient with a suspected infection purchased a tilapia from the same retail store, and on the same day, as a patient with a confirmed infection (Patient 7). Microbiologic cultures were negative, except in the one white patient, whose tissue culture was positive for Aeromonas hydrophila. That patient did not know the type of fish he had been handling when he was injured.
Additional Patients and Isolates of S. iniae
The review of Workers' Compensation Board claims failed to identify any suspected cases of invasive S. iniae infection. The review of the data base at the CDC microbiology laboratory revealed two additional cases in which S. iniae had been isolated (Patients 10 and 11) (Table 1). Patient 10 was employed as a cook in Ottawa, and had S. iniae isolated from synovial fluid from his knee. Patient 11 had S. iniae bacteremia; he was from Texas, but no other demographic information was known. Additional isolates of S. iniae included 11 isolates from tilapia brains obtained during epizootics, 11 from cultures of live fish obtained at retail stores, and 27 from tilapia obtained from fish suppliers (Table 2Table 2
PFGE Patterns Detected in Isolates of S. iniae Obtained from Humans and Fish.).Molecular Typing
The PFGE patterns of the isolates from Patients 1 through 9 were identical and were termed pattern A (Figure 2Figure 2
PFGE Analyses of Strains of S. iniae after the Digestion of Chromosomal DNA with Smal.). Patients 10 and 11 had pattern A', which differed from pattern A by one band. The strains isolated from the tilapia brains had either pattern A (1 isolate) or pattern A' (10 isolates). Pattern A was also found in two cultures of fish from two retail stores in the greater Toronto area, all four isolates from tilapia sampled in Vancouver, and four of the isolates of tilapia from two of the seven fish suppliers sampled. The remaining strains, including the ATCC type strains, yielded a total of 19 different unrelated patterns (Table 2).Epidemiologic Investigation
We were unable to identify any one farm as the probable source of the fish associated with the cases of cellulitis. Each of the first four infected patients purchased tilapia from a different retailer in the greater Toronto area. In the six weeks before each purchase, all these retailers had been supplied, through wholesalers, from a total of six fish farms in the United States — two in North Dakota and one each in Tennessee, Arkansas, Delaware, and Illinois. Only one of the suppliers identified in this investigation exported fish during the period of the sampling. S. iniae was identified from that supplier's fish, but it did not have the A or the A' PFGE pattern.
Discussion
Whether these S. iniae infections represent the emergence of a new pathogen affecting humans or cases of previously unrecognized disease is unclear. Such infections may not have been recognized in the past as a cause of cellulitis, for several reasons. Cellulitis occurring after local injury or spontaneously is by far most often due to S. pyogenes or Staphylococcus aureus. 21 Cultures are usually not diagnostic and are therefore not routinely obtained.22 Hook et al. were able to isolate pathogens from only 26 percent of patients with cellulitis, even though they cultured punch-biopsy specimens, aspirates, and blood.22 Under certain growth conditions the β-hemolysis of S. iniae may not be evident, and it may therefore be misidentified as a viridans streptococcus and considered a contaminant. Even if identification to the species level were performed with current commercial systems of identification, S. iniae would probably not be correctly identified, since it is not found in those data bases. Six of the clinical isolates we studied were originally identified as S. uberis.
Evidence supporting the possibility that S. iniae is a newly emerging pathogen includes the fact that the organism has only recently been identified as a pathogen in fish produced by the aquaculture industry. It has been suggested that streptococcal infections in fish have become increasingly important because of overcrowding in farms and transport.4,9 We do not believe that S. iniae has gone unrecognized in the greater Toronto area because of a failure of identification, since most hospitals routinely refer viridans streptococci isolated from sterile sites to a reference laboratory.
Our surveillance identified 12 patients with suspected infections on the basis of the clinical presentation of cellulitis of the hand and a history of handling fish in the previous 72 hours. Although the case definition may lack specificity, as evidenced by the patient with cellulitis due to A. hydrophila, suspected cases may well have been due to S. iniae infection. The clinical presentations were remarkably similar, and most of the patients had been injured while preparing tilapia.
Although isolates of S. iniae obtained from the surfaces of tilapia and other species of fish are genetically diverse, only two distinct, highly related clones (with PFGE patterns A and A') caused invasive disease. There have been similar findings with regard to other bacteria that cause infectious diseases.23 This suggests that a virulence factor or factors that are not present in all strains may be important for pathogenicity in humans and fish.
The explanation for the finding that tilapia was so frequently associated with disease may be that surface colonization with S. iniae, particularly with the invasive clone, is restricted primarily to that species or to tilapia from farms where the invasive clone is endemic. Our surveillance data do suggest that S. iniae is a common bacterium on tilapia grown by aquaculture. Our results do not rule out other commercial fish as sources of S. iniae. We could not determine from the epidemiologic studies whether the invasive clone of S. iniae was restricted to one or more farms. Although the invasive clone that had PFGE pattern A was isolated from fish from two farms, neither was identified in the epidemiologic investigation. Unfortunately, we could not sample fish or water directly from the potentially implicated farms.
All 9 patients with confirmed S. iniae infection and 11 of the 12 who had culture-negative suspected infections were of Asian origin. Asians make up 5.6 percent of the population of greater Toronto, and they were clearly overrepresented in our study.24 This may be related to the volume of tilapia this population consumes or to the manner in which the fish are processed before cooking. Typically, our patients purchased the fish live from aquariums in retail stores, where they were killed and gutted, but with all their appendages left intact. The fish were kept at 4°C for up to 48 hours, at which point they were cleaned further before cooking. This technique contrasts with the methods of purchasing and preparing fish found in many other ethnic communities, where fish are dead before purchase and kept packed on ice in retail stores. In such communities, fish are usually scaled and cleaned, and the head, tail, and fins are removed, by members of the retail staff. These practices may reduce the potential for the inoculation of pathogens.
Our surveillance for cellulitis associated with injuries during the handling of fish was not population-based, and we do not know the sensitivity of the reports made by the emergency departments during the survey period. Furthermore, current diagnostic tests are not adequate to define the bacterial cause of cellulitis when no cultures are obtained from a sterile site or such cultures are negative. Our data suggest that cellulitis may occur in association with injuries received during fish preparation, but they do not allow an estimate of frequency or of the proportion of cases that may be associated with a given pathogen.
Other streptococcal species have been shown to be capable of causing zoonotic infections.25-34 Outbreaks of S. suis septicemia and meningitis have been documented in pigs, especially under adverse environmental conditions.29,33 Similar disease has been described in humans after contact with live or slaughtered pigs.30-34 The portal of entry is unknown, but it often appears to be the skin. As we found with S. iniae, only certain clones of S. suis are commonly associated with disease in humans.35
The demonstration of another new pathogen linked to the food industry is not surprising, considering that changes in the production, storage, distribution, and preparation of food, as well as environmental changes, provide increased opportunity for humans to be exposed to new organisms that may be pathogenic.36,37 S. iniae can cause invasive disease in humans, but when proper precautionary measures are taken during the handling of whole, uncooked fish, the infections caused by S. iniae should be preventable.
Supported in part by a grant from the Canadian Bacterial Diseases Network and by Physicians Services Incorporated. Presented in part at the Interscience Conference on Antimicrobial Agents and Chemotherapy, New Orleans, September 15–18, 1996.
Source Information
From the Department of Medicine, University of Toronto, Toronto (M.R.W., A.M., D.E.L.); the Laboratory Centre for Disease Control, Ottawa, Ont. (M.L., D.A.K.); the Scarborough Grace Hospital, Scarborough, Ont. (P.W., D.R., M.C.); the Department of Microbiology, Mount Sinai and Princess Margaret Hospitals, Toronto (A.M., B.M.W., D.E.L.); the City of Scarborough Public Health Department, Scarborough, Ont. (C.O.); and the Public Health Laboratory of Ontario, Toronto (A.B.) — all in Canada; and the Centers for Disease Control and Prevention, Atlanta (R.F.).
Address reprint requests to Dr. Low at the Department of Microbiology, Mount Sinai Hospital, 600 University Ave., Toronto, ON M5G 1X5, Canada.
Additional investigators are listed in the Appendix.
Appendix
The following persons were also members of the S. iniae Study Group: M. Patel and J. Fuller, Department of Microbiology, Mount Sinai Hospital, Toronto; M. Baqi and W. Gold, Department of Medicine, University of Toronto, Toronto; J. Hoeve, Fisheries and Oceans Canada, Toronto; J. Urquhart, Toronto Health Department, Toronto; K. Gorman and C. D'Cunha, City of Scarborough Public Health Department, Scarborough, Ont.; and M. Lovgren, National Centre for Streptococcus, Laboratory Centre for Disease Control, Edmonton, Alta.
- References
References
1
Pier GB ,Madin SH . Streptococcus iniae sp. nov., a beta-hemolytic streptococcus isolated from an Amazon freshwater dolphin, Inia geoffrensis. Int J Syst Bacteriol 1976;26:545-553
CrossRef2
Pier GB ,Madin SH ,Al-Nakeeb S . Isolation and characterization of a second isolate of Streptococcus iniae. Int J Syst Bacteriol 1978;28:311-314
CrossRef3
Kitao T ,Aoki T ,Sakoh R . Epizootic caused by β-hemolytic Streptococcus species in cultured freshwater fish. Fish Pathol 1981;15:301-307
CrossRef4
Eldar A ,Bejerano Y ,Livoff A ,Horovitcz A ,Bercovier H . Experimental streptococcal meningo-encephalitis in cultured fish. Vet Microbiol 1995;43:33-40
CrossRef | Web of Science | Medline5
Robinson JA ,Meyer FP . Streptococcal fish pathogen. J Bacteriol 1966;92:512-512
Web of Science | Medline6
Eldar A ,Bejerano Y ,Bercovier H . Streptococcus shiloi and Streptococcus difficile: two new streptococcal species causing a meningoencephalitis in fish. Curr Microbiol 1994;28:139-143
CrossRef | Web of Science7
Kaige N ,Miyazaki T ,Kubota S . The pathogen and histopathology of vertebral deformity in cultured yellowtail Seriola-quinqueradiata. Fish Pathol 1984;19:173-180
CrossRef8
Perera R ,Johnson S ,Collins M ,Lewis DH . Streptococcus iniae associated with mortality of Tilapia nilotica and T. aurea hybrids. J Aquat Anim Health 1994;6:335-340
CrossRef9
Kusuda R . Bacterial fish diseases in mariculture in Japan with special emphasis on streptococcosis. Isr J Aquacult 1992;44:140-14010
Eldar A ,Frelier PF ,Assenta L ,Varner PW ,Lawhon S ,Bercovier H . Streptococcus shiloi, the name for an agent causing septicemic infection in fish, is a junior synonym of Streptococcus iniae. Int J Syst Bacteriol 1995;45:840-842
CrossRef11
Vandamme P ,Devriese LA ,Pot B ,Kersters K ,Melin P . Streptococcus difficile is a nonhemolytic group B type Ib streptococcus. Int J Syst Bacteriol 1997;47:81-85
CrossRef | Medline12
Kusuda R ,Kawai K ,Salati F ,Banner CR ,Fryer JL . Enterococcus seriolicida sp. nov., a fish pathogen. Int J Syst Bacteriol 1991;41:406-409
CrossRef | Medline13
Teixeira LM ,Merquior VLC ,Vianni MCE , et al. Phenotypic and genotypic characterization of atypical Lactococcus garvieae strains isolated from water buffalos with subclinical mastitis and confirmation of L. garvieae as a senior subjective synonym of Enterococcus seriolicida. Int J Syst Bacteriol 1996;46:664-668
CrossRef | Medline14
Weinstein M ,Low D ,McGeer A , et al. Invasive infection due to Streptococcus iniae: a new or previously unrecognized disease -- Ontario, 1995-1996. Can Commun Dis Rep 1996;22:129-131
Medline15
Invasive infection due to Streptococcus iniae -- Ontario, 1995-1996MMWR Morb Mortal Wkly Rep 1996;45:650-653
Medline16
Ruoff KL. Streptococcus. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, eds. Manual of clinical microbiology. Washington, D.C.: ASM Press, 1995:299-307.
17
M7-A3, methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. 3rd ed. Approved standard. Villanova, Pa.: National Committee for Clinical Laboratory Standards, 1994.
18
Murray BE ,Singh KV ,Markowitz SM , et al. Evidence for clonal spread of a single strain of β-lactamase producing Enterococcus (Streptococcus) faecalis to six hospitals in five states. J Infect Dis 1991;163:780-785
CrossRef | Web of Science | Medline19
Tenover FC ,Arbeit RD ,Goering RV , et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995;33:2233-2239
Web of Science | Medline20
Durack DT ,Lukes AS ,Bright DK . New criteria for diagnosis of infective endocarditis: utilization of specific echocardiographic findings. Am J Med 1994;96:200-209
CrossRef | Web of Science | Medline21
Lee PC ,Turnidge J ,McDonald PJ . Fine-needle aspiration biopsy in diagnosis of soft tissue infections. J Clin Microbiol 1985;22:80-83
Web of Science | Medline22
Hook EW III ,Hooton TM ,Horton CA ,Coyle MB ,Ramsey PG ,Turck M . Microbiologic evaluation of cutaneous cellulitis in adults. Arch Intern Med 1986;146:295-297
CrossRef | Web of Science | Medline23
Musser JM . Molecular population genetic analysis of emerged bacterial pathogens: selected insights. Emerg Infect Dis 1996;2:1-17
CrossRef | Web of Science | Medline24
The municipality of metropolitan Toronto key facts 1995. Toronto: Metro Toronto Planning Department, 1995.
25
Weinberg AN. Zoonoses. In: Mandell GL, Bennett JE, Dolin R, eds. Mandell, Douglas and Bennett's principles and practice of infectious diseases. 4th ed. Vol. 2. New York: Churchill Livingstone, 1995:2790-5.
26
Unpasteurized milk and Streptococcus zooepidemicusC D R Wkly Rep 1994;4:241-241
27
Sharp MW ,Prince MJ ,Gibbens J . S. zooepidemicus infection and bovine mastitis. Vet Rec 1995;137:128-128
CrossRef | Web of Science | Medline28
Barnham M ,Neilson DJ . Group L beta-haemolytic streptococcal infection in meat handlers: another streptococcal zoonosis? Epidemiol Infect 1987;99:257-264
CrossRef | Web of Science | Medline29
Windsor RS ,Elliott SD . Streptococcal infection in young pigs. IV. An outbreak of streptococcal meningitis in weaned pigs. J Hyg (Lond) 1975;75:69-78
CrossRef | Web of Science | Medline30
Michaud S ,Duperval R ,Higgins R . Streptococcus suis meningitis: first case reported in Quebec. Can J Infect Dis 1996;7:329-33131
Walsh B ,Williams AE ,Satsangi J . Streptococcus suis type 2: pathogenesis and clinical disease. Rev Med Microbiol 1992;3:65-7132
Arends JP ,Zanen HC . Meningitis caused by Streptococcus suis in humans. Rev Infect Dis 1988;10:131-137
CrossRef | Medline33
Chau PY ,Huang CY ,Kay R . Streptococcus suis meningitis: an important underdiagnosed disease in Hong Kong. Med J Aust 1983;1:414-416
Web of Science | Medline34
Porcine streptococci causing meningitis and septicaemia in manLancet 1975;1:1286-1288
Web of Science | Medline35
Mogollon JD ,Pijoan C ,Murtaugh MP ,Kaplan EL ,Collins JE ,Cleary PP . Characterization of prototype and clinically defined strains of Streptococcus suis by genomic fingerprinting. J Clin Microbiol 1990;28:2462-2466
Web of Science | Medline36
Vidaver A . Emerging and remerging infectious diseases: perspective on plants, animals and humans. ASM News 1996;62:583-58537
Baird-Parker AC . Foods and microbiological risks. Microbiology 1994;140:687-695
CrossRef | Web of Science | Medline
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CrossRef19
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CrossRef20
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CrossRef21
M. Grupper, I. Potasman. (2008) Formal Adult Infectious Disease OutpatientConsultations: A Retrospective 6-Year Survey. Infection 36:6, 543-548
CrossRef22
S M Zhou, M Q Xie, X Q Zhu, Y Ma, Z L Tan, A X Li. (2008) Identification and genetic characterization of Streptococcus iniae strains isolated from diseased fish in China. Journal of Fish Diseases 31:11, 869-875
CrossRef23
N SUANYUK, F KONG, D KO, G GILBERT, K SUPAMATTAYA. (2008) Occurrence of rare genotypes of Streptococcus agalactiae in cultured red tilapia Oreochromis sp. and Nile tilapia O. niloticus in Thailand—Relationship to human isolates?. Aquaculture 284:1-4, 35-40
CrossRef24
P. C. Y. Woo, S. K. P. Lau, J. L. L. Teng, H. Tse, K.-Y. Yuen. (2008) Then and now: use of 16S rDNA gene sequencing for bacterial identification and discovery of novel bacteria in clinical microbiology laboratories. Clinical Microbiology and Infection 14:10, 908-934
CrossRef25
John T. Buchanan, Kelly M. Colvin, Mike R. Vicknair, Silpa K. Patel, Anjuli M. Timmer, Victor Nizet. (2008) Strain-associated virulence factors of Streptococcus iniae in hybrid-striped bass. Veterinary Microbiology 131:1-2, 145-153
CrossRef26
Annelies S. Zinkernagel, Anjuli M. Timmer, Morgan A. Pence, Jeffrey B. Locke, John T. Buchanan, Claire E. Turner, Inbal Mishalian, Shiranee Sriskandan, Emanuel Hanski, Victor Nizet. (2008) The IL-8 Protease SpyCEP/ScpC of Group A Streptococcus Promotes Resistance to Neutrophil Killing. Cell Host & Microbe 4:2, 170-178
CrossRef27
Ahmed H. Al-Harbi, M. Naim Uddin. (2008) Aerobic Bacterial Flora of Common Carp ( Cyprinus carpio L.) Cultured in Earthen Ponds in Saudi Arabia. Journal of Applied Aquaculture 20:2, 108-119
CrossRef28
E. Soto, M.J. Mauel, A. Karsi, M.L. Lawrence. (2008) Genetic and virulence characterization of Flavobacterium columnare from channel catfish (Ictalurus punctatus). Journal of Applied Microbiology 104:5, 1302-1310
CrossRef29
R A Nawawi, J Baiano, A C Barnes. (2008) Genetic variability amongst Streptococcus iniae isolates from Australia. Journal of Fish Diseases 31:4, 305-309
CrossRef30
Jason N. Cole, Anna Henningham, Christine M. Gillen, Vidiya Ramachandran, Mark J. Walker. (2008) Human pathogenic streptococcal proteomics and vaccine development. PROTEOMICS – CLINICAL APPLICATIONS 2:3, 387-410
CrossRef31
Donald C. Vinh, John M. Embil. (2007) Severe skin and soft tissue infections and associated critical illness. Current Infectious Disease Reports 9:5, 415-421
CrossRef32
Toby Lowry, Stephen A. Smith. (2007) Aquatic zoonoses associated with food, bait, ornamental, and tropical fish. Journal of the American Veterinary Medical Association 231:6, 876-880
CrossRef33
Christopher J. Bonar, Ernesto O. Boede, Manuel García Hartmann, Joanne Lowenstein-Whaley, Esmeralda Mujica-Jorquera, Scott V. Parish, James V. Parish, Michael M. Garner, Cynthia K. Stadler. (2007) A RETROSPECTIVE STUDY OF PATHOLOGIC FINDINGS IN THE AMAZON AND ORINOCO RIVER DOLPHIN (INIA GEOFFRENSIS) IN CAPTIVITY. Journal of Zoo and Wildlife Medicine 38:2, 177-191
CrossRef34
M KIM, S CHOI, E LEE, Y NAM, S KIM, K KIM. (2007) α-enolase, a plasmin(ogen) binding and cell wall associating protein from a fish pathogenic Streptococcus iniae strain. Aquaculture 265:1-4, 55-60
CrossRef35
Gee-Wook Shin, K.J. Palaksha, Young-Rim Kim, Sung-Won Nho, Suk Kim, Gang-Joon Heo, Se-Chang Park, Tae-Sung Jung. (2007) Application of immunoproteomics in developing a Streptococcus iniae vaccine for olive flounder (Paralichthys olivaceus). Journal of Chromatography B 849:1-2, 315-322
CrossRef36
Susanna K.P. Lau, Patrick C.Y. Woo, Rachel Y.Y. Fan, Ruby C.M. Lee, Jade L.L. Teng, Kwok-yung Yuen. (2007) Seasonal and tissue distribution of Laribacter hongkongensis, a novel bacterium associated with gastroenteritis, in retail freshwater fish in Hong Kong. International Journal of Food Microbiology 113:1, 62-66
CrossRef37
C-Y C. Wang, H-S Shie, S-C Chen, J-P Huang, I-C Hsieh, M-S Wen, F-C Lin, D. Wu. (2007) Lactococcus garvieae infections in humans: possible association with aquaculture outbreaks. International Journal of Clinical Practice 61:1, 68-73
CrossRef38
JH Creeper, NB Buller. (2006) An outbreak of Streptococcus iniae in barramundi (Lates calcarifera) in freshwater cage culture. Australian Veterinary Journal 84:11, 408-411
CrossRef39
June C. McK. Roach, Paul N. Levett, Marc C. Lavoie. (2006) Identification of Streptococcus iniae by commercial bacterial identification systems. Journal of Microbiological Methods 67:1, 20-26
CrossRef40
R RUSSO, H MITCHELL, R YANONG. (2006) Characterization of Streptococcus iniae isolated from ornamental cyprinid fishes and development of challenge models. Aquaculture 256:1-4, 105-110
CrossRef41
Susanna K.P. Lau, Patrick C.Y. Woo, Wei-kwang Luk, Ami M.Y. Fung, Wai-ting Hui, Angie H.C. Fong, Chi-wing Chow, Samson S.Y. Wong, Kwok-yung Yuen. (2006) Clinical isolates of Streptococcus iniae from Asia are more mucoid and β-hemolytic than those from North America. Diagnostic Microbiology and Infectious Disease 54:3, 177-181
CrossRef42
Patrick CY Woo, Susanna KP Lau, Jade LL Teng, Kwok-yung Yuen. (2005) Current status and future directions for Laribacter hongkongensis, a novel bacterium associated with gastroenteritis and travellerʼs diarrhoea. Current Opinion in Infectious Diseases 18:5, 413-419
CrossRef43
R WHITTINGTON, C LIM, P KLESIUS. (2005) Effect of dietary β-glucan levels on the growth response and efficacy of vaccine in Nile tilapia,. Aquaculture 248:1-4, 217-225
CrossRef44
A TORANZO, B MAGARINOS, J ROMALDE. (2005) A review of the main bacterial fish diseases in mariculture systems. Aquaculture 246:1-4, 37-61
CrossRef45
Jesse D Miller, Melody N Neely. (2004) Zebrafish as a model host for streptococcal pathogenesis. Acta Tropica 91:1, 53-68
CrossRef46
Ana I. Mata, M.Mar Blanco, Lucas Domı́nguez, José F. Fernández-Garayzábal, Alicia Gibello. (2004) Development of a PCR assay for Streptococcus iniae based on the lactate oxidase (lctO) gene with potential diagnostic value. Veterinary Microbiology 101:2, 109-116
CrossRef47
Andrew C Barnes, Michael T Horne, Anthony E Ellis. (2003) Streptococcus iniae expresses a cell surface non-immune trout immunoglobulin-binding factor when grown in normal trout serum. Fish & Shellfish Immunology 15:5, 425-431
CrossRef48
Ahmed Darwish, Adnan Ismaiel. (2003) Laboratory Efficacy of Amoxicillin for the Control of Streptococcus iniae Infection in Sunshine Bass. Journal of Aquatic Animal Health 15:3, 209-214
CrossRef49
Ta-Naska Trotter, Douglas L Marshall. (2003) Influence of pH and NaCl on monolaurin inactivation of Streptococcus iniae. Food Microbiology 20:2, 187-192
CrossRef50
Ahmed Darwish, Steven Rawles, Bill Griffin. (2002) Laboratory Efficacy of Oxytetracycline for the Control of Streptococcus iniae Infection in Blue Tilapia. Journal of Aquatic Animal Health 14:3, 184-190
CrossRef51
Ahmed Darwish, Steven Rawles, Bill Griffin. (2002) Laboratory Efficacy of Oxytetracycline for the Control of Streptococcus iniae Infection in Blue Tilapia. Journal of Aquatic Animal Health 14:3, 184-190
CrossRef52
David Schlossberg. (2001) Infections from leisure-time activities. Microbes and Infection 3:6, 509-514
CrossRef53
Craig A. Shoemaker, Phillip H. Klesius, Joyce J. Evans. (2001) Prevalence of Streptococcus iniae in tilapia, hybrid striped bass, and channel catfish on commercial fish farms in the United States. American Journal of Veterinary Research 62:2, 174-177
CrossRef54
D.L Evans, S.L Taylor, J.H Leary, G.R Bishop, A Eldar, L Jaso-Friedmann. (2000) In vivo activation of tilapia nonspecific cytotoxic cells by Streptococcus iniae and amplification with apoptosis regulatory factor(s). Fish & Shellfish Immunology 10:5, 419-434
CrossRef55
Larry M Baddour. (2000) Cellulitis syndromes: an update. International Journal of Antimicrobial Agents 14:2, 113-116
CrossRef56
Jiro ARATA. (2000) Nishi Nihon Hifuka 62:3, 357-360
CrossRef57
Naiel Bisharat, Vered Agmon, Renato Finkelstein, Raul Raz, Gad Ben-Dror, Larisa Lerner, Soboh Soboh, Raul Colodner, Daniel N Cameron, David L Wykstra, David L Swerdlow, JJ Farmer. (1999) Clinical, epidemiological, and microbiological features of Vibrio vulnificus biogroup 3 causing outbreaks of wound infection and bacteraemia in Israel. The Lancet 354:9188, 1421-1424
CrossRef58
S. V. Dodson, J. J. Maurer, E. B. Shotts. (1999) Biochemical and molecular typing of Streptococcus iniae isolated from fish and human cases. Journal of Fish Diseases 22:5, 331-336
CrossRef59
W.L. Chan, C.H.S. Chan, T.Y.K. Chan. (1999) Vibrio vulnificus septicaemia and necrotizing fasciitis after a prick from the dorsal fin of a tilapia. Transactions of the Royal Society of Tropical Medicine and Hygiene 93:2, 174
CrossRef60
Lúcia Martins Teixeira, Maria da Glória S. Carvalho, Richard R. Facklam. 1999. VAGOCOCCUS. , 2215-2220.
CrossRef61
A. Reilly, F. Käferstein. (1998) Food safety and products from aquaculture. Journal of Applied Microbiology 85:S1, 249S-257S
CrossRef62
P. R. Bowser, G. A. Wooster, R. G. Getchell, M. B. Timmons. (1998) Streptococcus iniae Infection of Tilapia Oreochromis niloticus in a Recirculation Production Facility. Journal of the World Aquaculture Society 29:3, 335-339
CrossRef
