ReviewStreptococcus iniae: An aquatic pathogen of global veterinary significance and a challenging candidate for reliable vaccination
Introduction
Streptococcus iniae has emerged as an important fish pathogen over the past few decades. Although originally isolated from freshwater dolphins (Pier and Madin, 1976), its major significance is as an aetiological agent of streptococcosis in farmed finfish. More recently, it has also been identified as a potential zoonotic pathogen, with at least 25 cases of human infection by S. iniae confirmed to date (Facklam et al., 2005, Lau et al., 2006, Lau et al., 2003). In 1997 the estimated annual impact of infection by this bacterium on the aquaculture industry in the USA alone was US$ 10 million and estimated globally to be US$ 100 million (Shoemaker et al., 2001).
The first confirmed streptococcal infection in cultured fish was reported in 1958 in rainbow trout (Oncorhynchus mykiss) in Japan (Hoshina et al., 1958). Over the next 2 decades, more streptococcal infections were identified as causes of mortality in farmed and wild species, the majority of which were reported from Japan and the USA (Kitao et al., 1981, Kusuda et al., 1979, Minami et al., 1979, Ohnishi and Jo, 1981, Robinson and Meyer, 1966). During this time, new species of streptococci were also being recognised. In 1976 a novel streptococcus was identified as the causative agent of “golf ball disease”, a disorder characterised by multiple subcutaneous abscesses in a captive Amazon freshwater dolphin (Inia geoffrensis) in San Francisco and was named Streptococcus iniae (Pier and Madin, 1976). A second isolate was obtained from skin lesions in another freshwater dolphin housed at the Niagara Falls Aquarium in New York in 1978 (Pier et al., 1978). A third dolphin isolate was also recovered in Ohio in 1987, although the findings were not published until 2003 (Bonar and Wagner, 2003).
The first descriptions of infection in fish by S. iniae occurred in the 1980s; epizootics were described in Japan in 1981 and 1983, and Singapore in 1985, although they were not recognised as S. iniae until years later (Foo et al., 1985, Inglis et al., 1993, Kitao et al., 1981, Nakatsugawa, 1983, Nguyen et al., 2002, Stoffregen et al., 1996). Infections also occurred in Israel and Taiwan in 1986, with the aetiological agent initially thought to be a new species and named Streptococcus shiloi (Eldar et al., 1994). Later analysis found the bacterial cause of the 1986 infections to be identical to the first S. iniae type strain (isolated from the San Francisco dolphin in 1976) and the name was later corrected to S. iniae (Eldar et al., 1994, Eldar et al., 1995b). In Israel, infection spread rapidly throughout the country, causing considerable mortalities to tilapia and rainbow trout stocks with significant economic effects (Eldar et al., 1994). To combat these losses, the first S. iniae vaccination program was initiated in Israel (Eldar et al., 1997a). Vaccination was successfully used in rainbow trout farms from 1995 to 1997, resulting in S. iniae-related mortalities decreasing from 50% to less than 5% (Bachrach et al., 2001). However, massive new outbreaks were recorded shortly thereafter, with isolates showing slight differences in biochemical properties, and new pathological changes in infected fish (Bachrach et al., 2001, Barnes et al., 2003b).
Confirmation of infections caused by S. iniae continued in various other locations around the world. Australia has suffered losses of cultured barramundi in marine cages every summer since 1992 (Bromage and Owens, 2002, Bromage et al., 1999). In the USA, infections in cultured fish were first reported in Texas in 1994 (Perera et al., 1994) and Massachusetts in 1996 (Stoffregen et al., 1996). S. iniae has also infected fish in other parts of Asia, the Middle East, and the Caribbean (Ferguson et al., 2000, Kitao et al., 1981, Nakatsugawa, 1983, Nguyen et al., 2002, Shen et al., 2005, Yuasa et al., 1999).
More recently, it has also been shown that S. iniae is able to infect and cause disease in humans. In the winter of 1995–1996 four cases of invasive S. iniae infection were documented in people in the Toronto area that had recently handled fresh, whole farmed fish from wholesale markets (Weinstein et al., 1996). Subsequent studies have identified at least 25 cases in Canada, the USA, Hong Kong and Singapore (Facklam et al., 2005, Koh et al., 2004, Lau et al., 2003, Weinstein et al., 1997).
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Distribution
To date, S. iniae has been identified in three main regions: North America (Canada, USA, and the Caribbean), Middle East (Bahrain and Israel), and Asia-Pacific (Australia, China, Japan, Singapore, and Taiwan) (Table 1).
It is currently unknown whether this bacterium could have originated from a single source and been distributed via ocean currents or movement of fish stocks. Eldar et al. (1994) postulated that since the pathogen was first identified in the USA nearly a decade earlier than the
Host range
At least 27 species of fish have been documented to have been infected by S. iniae (see Table 2). Freshwater, marine, and euryhaline species are represented, as well as both cultured and wild populations. There has also been documentation of species that have been resistant to infection in the face of challenge. These species include the common carp (Cyprinus carpus), when reared in community with infected tilapia (Eldar et al., 1995a), and market-sized channel catfish (Ictalurus punctatus)
Identification and typing
The initial morphological and biochemical characteristics of this species were based on the type strain isolated from the Amazon freshwater dolphin in 1976 which was deposited in the American Type Culture Collection under the Accession number 29178 (Pier and Madin, 1976). S. iniae is a Gram-positive, encapsulated coccus that most often occurs in long chains in broth culture. On solid blood agar media most strains form a small (up to 1 mm diameter) white, umbonate colony that is beta-haemolytic
Pathophysiology
S. iniae tends to cause different disease states depending on the type of hosts it infects. In dolphins it has only been shown to cause multifocal subcutaneous abscesses (Bonar and Wagner, 2003, Pier and Madin, 1976, Pier et al., 1978). Humans tend to develop a bacteraemic cellulitis, with occasional localisation in other organs or joints (Facklam et al., 2005, Lau et al., 2003, Weinstein et al., 1997). In fish, the disease state caused by infection with S. iniae generally results in a
Prevention and therapy
Dermal infections in freshwater dolphins have been successfully treated with antibiotics. The first animal responded to a 10-day course of penicillin and tylocin (Pier and Madin, 1976, Pier et al., 1978). The third was eventually successfully treated with carbenicillin followed by erythromycin, but the course was continued for 13 weeks and recovery took over 18 months (Bonar and Wagner, 2003).
All known human infections have also been treated successfully with antimicrobial therapy. Most were
Zoonotic potential
There is substantial evidence that S. iniae is able to be transferred to and infect humans. As of 2005, there have been at least 25 confirmed cases of S. iniae infections in humans reported in the literature (Facklam et al., 2005, Lau et al., 2006, Lau et al., 2003). The true number of human infections is likely to be much higher due to problems with identification. Its reported similarities to Streptococcus pyogenes and the viridans group of streptococci may lead to misidentification,
Conclusion
The list of susceptible species as well as the distribution of this bacterium highlight the importance of S. iniae not only as a pathogen to the aquaculture industry, but one which also has the potential to adversely affect human health. Although much work has been done on this species to date, more research is needed to further reduce the effects of this bacterium worldwide. Aquaculture is one of the fastest growing industries in the world. As global wild fish stocks continue to be depleted,
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