Bacterial and Viral Fish Diseases in Turkey

Yıl 2014, Cilt: 14 Sayı: 1, - , 07.07.2014

Rafet Çagrı Öztürk İlhan Altınok

https://doi.org/10.4194/1303-2712-v14_1_30

Öz

This review summarizes the state of knowledge about the major bacterial and viral pathogens of fish found in Turkey. It also considers diseases prevention and treatment. In this study, peer reviewed scientific articles, theses and dissertations, symposium proceedings, government records as well as recent books, which published between 1976 and 2013 were used as a source to compile dispersed literature. Bacterial and viral disease problems were investigated during this period in Turkey. Total of 48 pathogen bacteria and 5 virus species have been reported in Turkey. It does mean that all the bacteria and virus present in fish have been covered since every year new disease agents have been isolated. The highest outbreaks occurred in larval and juvenile stages of the fish. This article focused on geographical distribution, host range, and occurrence year of pathogenic bacteria and virus species. Vibriosis, Furunculosis, Motile Aeromonas Septicemia, Yersiniosis, Photobacteriosis and Flavobacteriosis are among the most frequently reported fish diseases. Meanwhile, Vagococcus salmoninarum, Renibacterium salmoninarum, Piscirickettsia salmonis and Pseudomonas luteola are rarely encountered pathogens and might be emerging disease problems. Finally, the current status in fish diseases prevention and their treatment strategies are also addressed.

Anahtar Kelimeler

Disease transfer, vaccines, disease treatment, disease prevention. Türkiye’de Görülen Bakteriyel ve Viral Balık Hastalıkları

Bacterial and Viral Fish Diseases in Turkey

Öz

Bu derlemede Türkiye'de bulunan başlıca bakteriyel ve viral balık patojenleri hakkında ki bilgi durumu özetlenmiştir. Bu bağlamda 1976 ve 2013 yılları arasında yayımlanan bilimsel makaleler, yüksek lisans ve doktora tezleri, sempozyum bildirileri, resmi kayıtlar ve kitaplarda dağınık olarak bulunan kayıtlar bir araya getirilmiştir. Türkiye'de bu dönemdeki bakteriyel ve viral hastalıkları incelenmiş ve toplam 48 patojenik bakteri ve 5 virüs türü rapor edilmiştir. Her yıl yeni hastalık etkenleri izole edilmesinden dolayı bu çalışmanın mevcut tüm bakteri ve virüsleri kapsadığı anlamı ortaya çıkmamalıdır. En yüksek salgınlar balıkların larval ve yavru dönemlerinde meydana gelmektedir. Bu makalede, patojenik bakteri ve virüs türlerinin coğrafik dağılımı, konakçı ve ortaya çıktıkları yıllara odaklanmıştır. Rapor edilen hastalıklar arasında en sık bildirilen balık hastalıkları Vibriosis, Furunkulosis, Hareketli Aeromonas Septisemi, Yersiniosis, Photobakteriosis ve Flavobakteriosis olarak yer almaktadır. Bu arada Vagococcus salmoninarum, Renibacterium salmoninarum, Piscirickettsia salmonis ve Pseudomonas luteola nadiren karşılaşılan patojenler olmasına rağmen balıklarda sorunlar oluşturabileceği düşünülmektedir. Son olarak, mevcut balık hastalıklarını önleme ve tedavi stratejileri de ele alınmıştır.

Anahtar Kelimeler

Hastalık transferi, aşılar, hastalıkların tedavisi, hastalıklardan korunma.

Kaynakça

• Red-pest, Vibriosis, Salt-water furunculosis, Boil disease Vibriosis Vibrio ordalii or until the harvest to sell. Sometimes, some farmer cannot sell their fish when water temperature increase in April or May; Therefore, they transfer their fish from sea cages to freshwater tank or raceways. Meanwhile, Vibrio species can also transferred from seawater to freshwater with the fish. Although Vibrio species cannot stay in freshwater for a long time, they can be isolated from fish since fish osmolality closed to 9‰ salinity. It does not mean that vibrio species can infect fresh water fish in fresh water. Furunculosis Aeromonas salmonicida subsp. salmonicida is known as an etiologic agent of furunculosis, one of the oldest known diseases and its origin is unclear and questionable. Etiological agent is also known as ‘‘typical A. salmonicida’’ and it should not be confused with ‘‘atypical A. salmonicida’’. The early isolation of the etiologic agent was made in 1930s
• (Mackie et al., 1930; Austin and Austin, 2012).
• Furunculosis is a prevalent disease of cultured salmonids, which causes serious economic crisis in the industry. Although salmonids seem to be most susceptible species, this particular disease has been reported more than 50 different fish species worldwide (McFadden, 1970; Bernoth, 1977; Barker and Kehoe, 1995; Kirkan et al., 2003). The pathogen bacterium was first isolated from rainbow trout fry in Marmara Region, Turkey (Timur et al., 1999). Following reports have been documented from different parts of Turkey (Table 2) but so far, only it has been observed in rainbow trout.
• The outbreaks generally occurred in hatcheries and ended up with high mortalities (Timur et al., 1999; Kirkan et al., 2003).
• Goldfish Ulcer Disease The causative agent of the disease is Aeromonas salmonicida subsp. achromogens, which is also known as atypical A. salmonicida. Ulcer disease was initially diagnosed in the early 1960s in trout in U.K.
• (Smith, 1963). Atypical A. salmonicida has become a major disease in cyprinids (Plumb and Hanson, 2011).
• The disease has been confirmed in many countries including European countries, USA and Australia (Plumb and Hanson, 2011).
• Few outbreaks of atypical A. salmonicida occurred in Turkey (Table 2). Korun and Timur (2001) were first reported the pathogen from rainbow trout in Balikesir. Subsequently, it was reported from sea bass and turbot in Black Sea region (Karatas et al., 2005; Savas and Ture, 2008).
• Motile Aeromonas Septicemia (MAS) MAS is associated with infections caused by Aeromonas hydrophila, A. sobria, A. veronii, and A. caviae. Aeromonas hydrophila is the predominant causative agent of MAS. These pathogens exist worldwide in fresh and brackish waters and occasionally in salt waters and they have a diverse host range. Motile Aeromonas spp. are considered as opportunistic pathogens and could easily found in organically rich waters. Thus, stress and poor water quality play a key role in occurrence. A. hydrophila has been recognized as a pathogen of fish since early 1960s in Europe (Levis and Bender, 1960) and in USA (Snieszko and Bullock, 1965). A. sobria has been recognized as a fish pathogen since 1987. Toranzo et al. (1989) was first reported it from wild gizzard shad (Dorosoma cepedianum) in USA.
• In Turkey, A. hydrophila was first isolated from rainbow trout in Eskisehir (Baran et al., 1980). The pathogen was subsequently isolated from other fish species such as sea bass, sea bream, eel, carp (Cyprinus carpio), sturgeon (Acipencer gueldenstaedtii), horse mackerel (T. mediterraneus) and from some ornamental fish species from different parts of Turkey (Table 3).
• The other etiological agent of the disease, A. sobria, was reported from Atlantic salmon (Salmo salar) in Black Sea (Karatas, 1996). It also has a wide host range such as rainbow trout, sea bass and sea bream. Initially, A. caviae was isolated from different fish species in Keban Dam (Muz et al., 1995). Afterwards, etiological agent was also isolated from rainbow trout, Atlantic salmon and some ornamental fish species (Candan et al., 1995; Timur et al., 2003; Korun and Toprak, 2010).
• The only incidence of mortality caused by A. Table Distribution and host range of A. salmonicida Common name of the disease Etiological agent Host Geographical distribution References Ulcerative Disease A. salmonicida subsp. achromogenes Oncorhynchus mykiss Balikesir Korun and Timur (2001)
• Dicentrarchus labrax Black Sea Karatas et al. (2005) Psetta maxima Eastern Black Sea Savas and Ture (2008) Furunculosis A. salmonicida subsp. salmonicida Oncorhynchus mykiss Marmara Region Timur et al. (1999) Aegean Region Kirkan et al. (2003) Ankara Ozkok (2005) Black sea Timur et al. (2008) Mugla, Aydin, Denizli Aksit and Kum (2008) Trabzon, Rize Kayis et al. (2009) schubertii was occurred in Mediterranean region and pathogen was isolated from rainbow trout (Akayli et al., 2011). This bacteria also belongs to motile
• Aeromonas species and might cause MAS. Yersiniosis It is one of the most important diseases in salmonids causing serious economic losses both in freshwater and marine salmonid aquaculture (Austin and Austin, 2012; Bullock and Snieszko, 1975;
• Toranzo, 2004). It also known as enteric red mouth disease (ERM), or yersiniosis. Causative agent of the disease is Yersinia ruckeri. It was first isolated from rainbow trout in Hagerman Valley, USA in 1950s
• (Ross et al., 1966). Yersiniosis is commonly observed from all over the world where salmonids are cultured (Plumb and Hanson, 2011). In Turkey, first outbreak of this disease occurred in one of the rainbow trout farm in southern Anatolia (Timur and Timur, 1991b). Disease agent came from Africa with imported rainbow trout summer eggs. After two decades, it became one of the widest distributed fish pathogen in Turkey (Table 4). Like the rest of the world, it was mostly seen in salmonids but it was also isolated from sea bass (Savaş et al., 2006)). Recently, number of Y. ruckeri isolation ware decreased may be due to vaccination of fish with Y. ruckeri bacterin. Photobacteriosis
• The disease is also known as pseudotuberculosis (formerly pasteurellosis) which is caused by Photobacterium damsela subsp. piscicida. The causative agent of the disease was first observed in white perch (Morone americanus) and striped bass (M. saxatilis) in Chesapeake Bay, USA (Snieszko and Enteric red mouth Yersiniosis Yersinia ruckeri Isparta, Bilecik, Denizli, Kirklareli Bolu, Tekirdag, Canakkale, Elazig Aydin, Bursa, Yalova, Trabzon, Rize Kutahya, Kayseri, Urfa, Ordu Manisa, Denizli Altun et al. (2010) Oncorhynchus mykiss Malatya and Elazig Seker et al. (2012)
• Table Distribution and host range of Ph. damsella subsp. P iscicida Common name of the disease Etiological agent Host Geographical distribution References Photobacteriosis Pseudotuberculosis Pasteurellosis cultivated fish, especially on rainbow trout in Europe and considered as a serious disease in farmed rainbow trout fry and fingerlings (Austin and Stobie, 1992;
• Bernardet et al., 1988; Santos et al., 1992; Toranzo and Barja, 1993). The pathogen was confirmed in most of the rainbow trout hatcheries in Turkey and caused heavy mortalities. First isolation of F. psychrophilum was from rainbow trout which sampled from different farms in 1990 (Balta and Cagirgan, 1998) (Table 6).
• Especially, when fish are small (0.1-4 g) and water temperature decrease to below 10 ⁰C, BCD or RTFS causes high mortality. Columnaris Disease Causative agent of the columnaris disease was described as Flavobacterium columnare (formerly Flexibacter columnaris, Cytophaga columnaris, Chondrococcus columnaris). It also referred to as cotton wool disease, saddleback disease, or mouth fungus. The disease was first reported from different fish species in Mississippi River and named Bacillus columnaris (Davis, 1922). After two decades, Ordal and Rucker (1944) isolated and described the causative agent. Unlike cold-water disease, columnaris disease generally occurs when the water temperature gets above 15 o C.
• Although F. columnare was isolated in Aegean, Mediterranean and Black Sea regions of Turkey, initial isolation of columnaris disease was from farmed rainbow trout in Mugla (Balta and Cagirgan, 1998) (Table 6).
• Bacterial Gill Disease Flavobacterium branchiophilum is the causative agent of the Bacterial Gill Disease (BGD). It was first described in 1926 (Davis, 1926). Afterwards, it was isolated from salmonids in USA (Kimura et al., 1978). Subsequently it was also isolated in Korea (Ko and Heo, 1997), Canada (Ostland et al., 1994) and Lactococcosis ''Warm-water'' Streptococcosis
• Pseudomonas sp. Stizostedion lucioperca Eğirdir Timur and Timur (1985) Haemorrhagic septicaemia, Fin Rot Pseudomonas fluorescens - Arcobacter cryaerophilus (Campylobacter cryearophila) Oncorhynchus mykiss Marmara Region Bulut and Aydin (2004) - Aerococcus viridans Oncorhynchus mykiss Mersin Ozet el al. (2008) - Burkholderia cepacia Oncorhynchus mykiss Trabzon, Rize Kayis et al. (2009) T. mediterraneus Trabzon Boran et al. (2013) Necrotic kidney, Hyperemia of the mouth Citrobacter braakii Oncorhynchus mykiss Bursa Altun et al. (2013c) Citrobacter freundii Oncorhynchus mykiss Erzurum Saglam et al. (2006) Oncorhynchus mykiss Trabzon, Rize Kayis et al. (2009) Enteric septicemia of catfish, hole in the head disease Edwardsiella ictaluri Oncorhynchus mykiss Ankara Keskin et al. (2004) Enterobacter cloacae Oncorhynchus mykiss Trabzon, Rize Kayis et al. (2009)
• Septicemia Escherichia vulneris Oncorhynchus mykiss, Carassius Carassius, Poecilia sp. Erzurum Aydin et al. (1997) Hemorrhagic septicemia Hafnia alvei Oncorhynchus mykiss Ankara Ozkok (2005) Oncorhynchus mykiss Trabzon, Rize Kayis et al. (2009)
• Vibriosis Photobacterium damselae subsp. damselae (Vibrio damselae) bacterium is not only a fish pathogen but also human pathogen. It effects variety of marine fish spp. Damsel fish seems to be most susceptible to this pathogen. It is one of the most important diseases in cultured European sea bass (Korun, 2004b). Initial isolation was fulfilled from sea bream in Mugla, Turkey (Akayli, 2001). In same region, it was also isolated from sea bass (Turk, 2002). Subsequently, the pathogen was reported from rainbow trout and horse mackerel in Black Sea (Timur et al., 2008; Kayis et al., 2009; Boran et al., 2013) (Table 9). It should be noted that only mixed bacteria colonies were isolated in all of these disease cases. Thus, pathogenicity of the bacterium is unclear in Turkey and the causative agent probably plays secondary pathogen role in most of the cases.
• Plesiomonas shigelloides Infection Plesiomonas shigelloides was first isolated from rainbow trout in Portugal in 1984 (Cruz et al., 1986).
• Subsequently, pathogen also isolated from catfish, sturgeon, rainbow trout, eel and gourami in Germany (Klein et al., 1993). Hemorrhages around the vent and protruded anus generally occur after infection (Austin and Austin, 2012). The pathogen is also the etiological agent of diarrhea in humans (Klein et al., 1993). Akayli and Zeybek (2005) was first reported the isolation of P. shigelloides from guppies (Poecilia reticulate) which were collected from different aquarium stores. After four years, the pathogen was reported from rainbow trout in Trabzon (Kayis et al., 2009) (Table 9).
• Serratia liquefeciens Infection Serratia liquefeciens is recognized as a potential fish pathogen belonging to Enterobacteriaceae family and it is the causative agent of bacterial septicemia (Woo and Bruno, 2011). The bacterium was isolated in different countries, for instance, from turbot in
• France (Vigneulle and Baudin, 1995), arctic char
• (Salvelinus alpinus) in U.S.A (Starliper, 2001) and from Atlantic salmon in Scotland (McIntosh and Austin, 1990). It was first isolated from rainbow trout in 2001 in Erzurum, Turkey (Aydin et al., 2001). Following isolation was reported in Trabzon from rainbow trout
• (Kayis et al., 2009). So far, the pathogen has never associated with serious outbreaks in Turkey (Table 9).
• Citrobacter Infection Citrobacter freundii was first reported as an emerging fish pathogen from sunfish (Mola mola) in Japan (Sato et al., 1982). After initial isolation, it was also isolated from Atlantic salmon in USA (Baya et al., 1990), rainbow trout in Spain which caused high mortalities with IPNV (Sanz, 1991) and from carp in
• India (Karunasagar et al., 1992). C. freundii is an opportunistic pathogen. Thus, stress, and pollution play a key role in infection occurrence (Sanz, 1991; Whalen et al., 2007).
• In Turkey, it was isolated from rainbow trout in Erzurum (Saglam et al., 2006) but there is no clear information about bacterial pathogenicity. After few years, it was also isolated from rainbow trout in Trabzon (Kayis et al., 2009). In both events, no heavy mortalities were observed. Besides that, another Citrobacter species, Citrobacter breakii was first reported as a fish pathogen in Bursa (Altun et al., 2013c) (Table 9).
• Arcobacter cryaerophilus Infection The bacterium is part of the normal micro flora of freshwater fish (Aydin et al., 2000b). Since the bacterium is ubiquitous in the environment and fish, it is not surprising that it might be opportunistic fish pathogen. It was first described as an emerging fish pathogen and isolated from rainbow trout in Balikesir and Canakkale (Aydin et al., 2000). After that, pathogenicity of the bacterium was confirmed by experimental infections which were performed on rainbow trout, and albino crosses (Bulut and Aydin, 2004) (Table 9). Infected fish showed pale gills, watery spleens, hemorrhages and bloody fluid in intestine.
• Shewanella putrefaciens Infection Disease caused by S. putrefaciens was first occurred in farmed rabbit fish (Siganus rivulatus) in Red Sea in 1985 and caused heavy mortalities (Saeed et al., 1987). After initial report, it was isolated from both common carp (Cyprinus carpio) and rainbow trout farms located in Poland (Kozinska and Pekala, 2004).
• Korun et al. (2009) was first reported the outbreak of a disease caused by S. putrefaciens from European sea bass in Aegean Region of Turkey. In the same year, the bacterium was also reported from rainbow trout in Trabzon (Kayis et al., 2009) (Table 9). Aerococcus viridans
• The bacterium was described as a pathogen and caused low mortalities in lobsters (Homarus gammarus L.) (Gjerde, 1984). Ozer et al. (2008) isolated A. viridans from cultured rainbow trout in Mersin (Table 9). Fish infected with A. viridans showed darkened skin, exophthalmia and hemorrhages in liver. Hafnia alvei
• Hafnia alvei is one of the causative agents of the hemorrhagic septicemia. It was first reported as a fish pathogen from rainbow trout in Bulgaria (Gelev and Gelev, 1988). Subsequent outbreak occurred in cherry salmon (O. masou) in Japan and confirmed its pathogenicity. If API Biochemical Test System is used for identification, the bacterium could be misidentified as Y. ruckeri or vice versa. The pathogen was isolated from rainbow trout in Ankara, Rize and Trabzon (Ozkok, 2005; Kayis et al., 2009) (Table 9).
• Enterobacter cloacae Enterobacter clocae was isolated from mullet (Mugil cephalus) in India. Bath challenge was performed and pathogenicity was determined (Sekar et al., 2008). In Turkey, Kayis et al. (2009) recovered the disease organism from rainbow trout in Trabzon and Rize (Table 9). Viral Fish Diseases
• IPNV The causative agent is Infectious pancreatic necrosis virus (IPNV) which belongs to Birnaviridae group. It is icosahedral in shape, unenveloped and has a double stranded RNA genome. IPN is an infectious systemic disease that has been recognized to have worldwide distribution in a wide range of fish. It causes high mortalities especially in fry and fingerling salmonids. The virus can be vertically and horizontally transmitted. Thus, the only way to get rid of the virus is the destruction of the stock (Olson and Thomas, 1994). Wood et al. (1955) was first described the IPNV. In Turkey, first IPNV particles were reported from rainbow trout organs after histopathological examination (Timur et al., 1993). After a decade, existence of IPNV was proved by RT-PCR (Candan, 2002). Subsequently, IPNV has been reported from different parts of Turkey and findings suggest wide distribution of the virus in Turkey (Table 10).
• VHSV Viral hemorrhagic septicemia (VHS) is a severe viral disease caused by VHS virus. The virus belongs to the family Rhabdoviridae, genus Novirhabdovirus. The disease was first occurred in rainbow trout in Germany (Schaperclaus, 1938). It is responsible for severe economic losses in rainbow trout farms in
• Europe (Woo and Bruno, 2011). VHSV was thought to have a predilection for salmonids, especially rainbow trout. Over the years, host range of the pathogen has expanded. For instance, Atlantic cod, pike, turbot, sea bass, Coho salmon, brown trout
• (Castric and Kinkelin, 1980; Jensen et al., 1979;
• Meier and Vestergard, 1980; Rasmussen, 1965;
• Winton et al., 1989). Unlike IPNV, there is no clear evidence about vertical transmission of the virus, but it is likely that, it can be transmitted horizontally and in many cases survivors become asymptomatic carriers. Salmonid fries are the most susceptible fish species to the virus. Mortality rates can reach up to 80-90%.
• VHSV was first isolated in Trabzon, Turkey from cultured turbot fry and brood stock in 2004 (Kalayci et al., 2006; Nishizawa et al., 2006). Subsequent isolations (Table 10) of VHSV in the Black Sea Region proved the existence of VHSV in Turkey (Altuntas and Ogut, 2010).
• Viral Erythrocytic Necrosis (VEN) The etiological agent of the disease is an iridovirus, named as erythrocytic necrosis virus (ENV). It was first reported in 1969 and identified as piscine erythrocytic necrosis (Laird and Bullock, 1969). Since its initial recognition, the virus has been recovered as a pathogen from a wide variety of fish species from different countries, for instance, sea bass in Spain (Pinto et al., 1989), coho salmon in Japan (Takahashi et al., 1982), pacific herring in Alaska (Meyers et al., 1986), coho salmon in Chile (Reyes and Campalans, 1987) and eel in Taiwan (Chen et al., 1985). Unlike VHSV and IPNV, VEN has not been recognized as a severe disease, it causes nominal mortalities in regard to other viral infections.
• In 2008, viral erythrocytic infection occurred in cultured Mediterranean sea bass in Black Sea (Timur et al., 2008). It is the only recorded report that has been made to date in Turkey (Table 10). Lymphocystis
• Lymphocystis is caused by a lymphocystis virus. It has been reported from wide variety of both freshwater and marine fish species from all over the world. It is one of the oldest and the best known fish virus. It has been known as a causative agent of a disease since 1874 (Plumb and Hanson, 2011). It was reported from ornamental fish in USA (Niggrelli and Ruggieri, 1965), Red Sea, Bering Sea, Mediterranean Sea (Anders, 1989) and Korea (Hossain et al., 2007).
• The causative agent of the virus was isolated from Sea Bream in Mugla, Turkey (Candan, 1991b). There is not any report of severe disease outbreak associated with Lymphocystis in Turkey (Table 10). Carp Pox
• It is also known as a fish pox or epithelioma papillosum, caused by a herpes virus. Like lymphocystis, it is one of oldest known fish disease. The virus was first recorded in 15th century (Hedrick and Sano, 1989). It was mainly reported from carp producer countries such as European countries, United States and Far East countries. Sano et al. (1985) was reported that, the most susceptible hosts of the virus are common carp and koi carp.
• Since it is restricted to cyprinids and carp production rates are low in Turkey, it is not considered as a serious disease problem in Turkey. It was first reported by Timur (1991a) from mirror carp in Antalya (Table 10).
• Prevention and Treatment The ideal way to control infectious fish diseases is to prevent exposure to pathogenic agents whenever possible, thus avoiding most devastating health problems through biosecurity (Plumb and Hanson, 2011). However, when dealing with the aquatic environment, it is virtually impossible to define all disease-causing agents and keep them isolated from the fish host. Water provides an excellent medium for transfer of many communicable agents from fish to fish or from locality to locality. Moreover, many disease-causing organisms are endemic to the aquatic environment and are opportunistic, facultative pathogens that remain viable under various conditions
• (Plumb and Hanson, 2011). Aquaculture is a vital source of food and still the fastest growing animal food producing sector. As a result of intensive fish farming and stressful conditions, infectious diseases, especially bacterial and viral origins, became one of the most important limiting factor in aquaculture facilities. Some diseases do not always reveal themselves in a clinical form. These types of diseases, e.g. BKD, furunculosis and ERM pose real risk of transferring the pathogen with fish movements (Hirvela et al., 2006). Therefore, it is obligatory to apply transportation restrictions. These may prevent the spread of the diseases or slow down the transmission. It may require efficient monitoring, dissuasive and financial sanctions. In some instances, it is really hard to get rid of the disease. Complete disposition of infected fish and disinfection of facilities, especially hatcheries, may be more economical than the losses associated with mortalities. The best practice for the elimination of IPNV, VHSV, BKD and furunculosis is prevention by the use of disease-free stocks if possible.
• Since fish are poikilothermic, they react more quickly to environmental change than homothermic terrestrial animals. Fish respond quickly any kind of environmental changes such as temperature change, excessive or insufficient dissolved gasses in the water, metabolites, or chemical additives, and so forth, to which they are unable to adapt. These factors increase fish susceptibility to infectious agents and compromise their immune response (Plumb and Hansen, 2011).
• In aquaculture, the usage of antimicrobial Adana, Adiyaman, Ankara, Antalya, Artvin, Aydin, Bilecik, Bolu, Burdur, Denizli, Duzce, Elazig, Eskisehir, Gumushane, Hatay, Izmir, Kahramanmaras, Kayseri, Mugla, Ordu, Sakarya, Samsun, Tokat, Trabzon, Usak, Zonguldak, Kalayci et al. (2012)
• Dicentrarchus labrax Antalya, Mugla, Ordu Kalayci et al. (2012) Oncorhynchus mykiss
• Elazig, Malatya, Sivas, Erzincan, Sanliurfa, Kahramanmaras, Erzurum Gurcay et al. (2013) Viral haemorrhagic septicemia virus VHSV ssRNA Rhabdoviridae, Novirhabdoviru s Psetta maxima Trabzon Nishizawa et al. (2006) Scopthalmus maximus Trabzon Kalayci et al. (2006)
• Merlangius merlangus Eastern Black Sea Altuntas and Ogut (2010) Oncorhynchus mykiss Bolu Kalayci et al. (2012) Sparus aurata Izmir Kalayci et al. (2012)
• Dicentrarchus labrax Antalya, Mugla, Izmir Kalayci et al. (2012) Psetta maxima Trabzon, Mugla Kalayci et al. (2012) Lymphocystis disease virus dsDNA Iridoviridae, Lymphocystis virus Sparus aurata Mugla Candan (1991b) Erythrocytic necrosis virus ENV dsDNA Iridoviridae
• Dicentrarchus labrax Black Sea Timur et al. (2008) Cyprinid herpes virus 1(Carp pox) CHV-1 ssRNA Rhabdoviridae Cyprinus carpio Timur (1991a)
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