Mousa et al. /Alexandria Journal of Veterinary Sciences 2015, 46: 110-116

Alexandria Journal of Veterinary Sciences 2015, 46: 110-116 ISSN 1110-2047, www.alexjvs.com DOI: 10.5455/ajvs.189505

Parasitic Hazard of Some Imported Frozen Fish

Mohamed M. Mousa1, Fatma A. Hiekal2, Samia M. EL-Hoshey3 and Mohamed A. Khamis 1 1Department of Food hygiene, Faculty of Veterinary Medicine, Alexandria University, Alexandria, . 2 Department of Parasitology, Faculty of Veterinary Medicine, Alexandria University, Alexandria, Egypt. 3 Department of Food hygiene, Alex Food Lab, Health Research Institute, Alexandria, Egypt. Key words ABSTRACT:

A total of 100 frozen fishes belonging to four different fish species were examined for presence of Frozen fish; Parasites, , different types of parasites during the period from April 2014 till the end of November 2014. Examination of the fish specimens revealed infestation with four different parasitic classes that included Nematoda, , Protozoa and Crustacea. When categorized according to species of fish, fish (Clupea harengus ) was the most susceptible to parasitic with a total infection rate of 96% for different types of parasites. This was followed by (Scomber scombrus ) with an infection rate of 92% , then the Horse mackerel (Trachurus mediterraneus) at the infection rate of 88%, and finally the Fish fillet (Pangasius hypophthalmus) was the least susceptible to parasites with the lowest infection rate of 16%.herring fish (Clupea harengus) was highly susceptible to Nematode infection at an infection rate of 92%, which was followed by infection with Protozoa (1.8%),Mackerel (Scomber scombrus) was susceptible to Nematode infection at the infection rate of 97.09% and to Protozoa with infection rate of 1.94%, while the infection rate with Crustacea was 0.97,Horse mackerel (Trachurus mediterraneus) was susceptible to Nematode infection at the infection rate of 97.8% and to Trematodes with 1.1% infection rate and to Crustacea with a rate of 1.1% and Fish fillet (Pangasius hypophthalmus) was susceptible to Trematodes with an infection rate of 16%. Corresponding Author: Mohamed A. Khamis: [email protected].

1. INTRODUCTION tract (Lopez Serrano et al., 2000, Chai et al., 2005 Nowadays, frozen fishes are considered as and Abd El-Ghany, 2007). one of the most important source of protein used in Moreover, and owing to the thermo stability of Egypt for its price and quality. Additionally, Anisakis simplex allergens, the ingestion of safely imported fish considered as one of the cheapest and cooked fish containing Anisakis simplex allergens promising source of protein that overcome the within dead parasites can also be potentially problem of shortage of animal source protein’s dangerous and can cause severe allergic reaction shortage due to limited animal production such as contact dermatitis and asthma (Audicana et capabilities (Norman, 1951). Regarding parasitic al., 2002 and EL-Daly et al., 2004). diseases of frozen fishes, about thirteen types of So the aim of the present study is to examine parasites were of concern to the food scientists in different fish types and species that were retailed at the United States (Jackson, 1990). Anisakid larvae Alexandria markets in order to detect different types are the most important group of nematode parasites of parasites. Also the second major aim is to survey that affect marine fishes. Anisakis or Anasikidiosis which type of fish is mostly infected with the referred to infection of people with larval stage of parasites, and to undertake a comparison between belonging to family . This male and female in relation to severity of infection disease is common and widely distributed in with different types of parasites. countries of far East and South East Asia where 2. MATERIAL AND METHODS: there is a habit of consuming raw, inadequately The duration of the work was extended from April cooked, pickled, semi-salted or smoked fishes 2014 till the end of November 2014, we worked on containing the third larval stages of Anisakis about ten fishes per month. The study was carried species. Larvae of Anisakid are found in the viscera out on 100 frozen fishes that belong to four different and muscle of wide range of fish and Cephalopod species as follow: twenty five herring fish, twenty mollusk species. Human are accidental in the five mackerel fish, twenty five horse mackerel fish; life cycle, nevertheless parasites almost never and twenty five fish fillet which was collected from developed further within the human gastrointestinal different retail markets at Alexandria. In order to

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Mousa et al. /Alexandria Journal of Veterinary Sciences 2015, 46: 110-116 examine for parasitic infection, the frozen fish was and to Protozoa with infection rate of 1.94%, while allowed to thaw at room temperature for 3-4 hours the infection rate with Crustacea was 0.97% and it under running tap water. In the laboratory, the fishes was free from Trematodes as recorded in Table (3). were autopsied separately in Petri dish according to Kabata (Kabata, 1985). Horse mackerel (Trachurus mediterraneus) was Autopsy was carried out as the following. Muscles, susceptible to Nematode infection at the infection body cavity, internal organs and gonads were rate of 97.8% and to Trematodes with 1.1% examined visually for the presence of larvae. To infection rate and to Crustacea with a rate of 1.1% examine further for parasites, the Compression and it was free from Protozoa Table (3). technique and the digestion method were used according to Jackson and Manfredi (Jackson et al., Fish fillet (Pangasius hypophthalmus) was 1981 and Manfredi et al., 2000). susceptible to Trematodes with an infection rate of Examination of muscle was done by the methods of 16%, while it was free from Nematodes, Protozoa compression and digestion using pepsin according and Crustacea Table (3). to FDA method and Bier (Bier et al., 1984). Fixation, staining and mounting of Trematodes were Nematodes recovered from examined fish included done as previously published (Carleton, 1957, Anisakis simplex that was recovered from Herring Lucky, 1977 and Beaver et al., 1984). On the other fish (Clupea harengus), Mackerel (Scomber hand, fixation and mounting of Nematodes , and scombrus) and Horse mackerel (Trachurus Crustacea were done according previously mediterraneus). The relative prevalence was 58.5%, published methods (Belding, 1965, Whitelock, 57.28% and 56.04%, respectively. Internal organs 1966, Lucky, 1977 and Kruse and Pritchard, 1982). that were mainly infected included intestine, liver, Finally, collection, fixation, staining and mounting air sac, and gonads Table 4. Also, muscle was of Coccidia were done according to Molnar reported to be infected as the case in the Horse (Molnar, 1989). mackerel and Mackerel fish Table (4).

3. RESULTS Contracaecum species were recovered from Herring The total number of infected fish with different fish (Clupea harengus), Mackerel (Scomber parasites was 73 (73%). When categorized, the scombrus) and Horse mackerel (Trachurus number of fish that was infected with Nematodes mediterraneus). The relative prevalence was was 69 (69%), that with Trematodes was 7 (7%), 17.12%, 24.27% and 19.78%, respectively. that with Crustacea was 2 (2%), and that infected Infection distribution in the internal organs included with Coccidia was 4 (4%), respectively Table (1). intestine, peritoneal cavity, intestine, liver surface and gonads Table (4). In regard to susceptibility of examined fish types to parasitic infection, Herring fish (Clupea harengus ) Pseudo terranova species was recovered from was the most susceptible to parasitic infection with a Herring fish (Clupea harengus), Mackerel (Scomber cumulative infection rate of 96% with different scombrus) and Horse mackerel (Trachurus species of parasites. This is followed by Mackerel mediterraneus) with a relative prevalence of 22.5%, (Scomber scombrus ) at an infection rate of 92% , 15.53% and 21.98%, in the infected fish types, then the Horse mackerel (Trachurus mediterraneus) respectively, and were mainly recovered from with 88% infection rate, while the Fish fillet intestine, peritoneal cavity, intestine, liver surface (Pangasius hypophthalmus) was the least and gonads Table (4). susceptible to parasitic infection with the lowest Concerning Trematodes recovered from fish, infection rate of 16%, respectively Table (2). Clinostomum species were recovered from Fish fillet (Pangasius hypophthalmus) and Horse In relation to the host-parasite specificity, herring mackerel (Trachurus mediterraneus), with a relative fish (Clupea harengus) was highly susceptible to prevalence of 16% and 1.1%, respectively. Nematode infection at an infection rate of 92%, Trematodes were infecting intestine of Horse which was followed by infection with Protozoa mackerel and muscle of Fillet. On the other hand, all (1.8%), while it was free from infection with examined fishes were free from Monogenean Trematodes and Crustacea as recorded in Table (3). Trematodes Table (4). In regard to Protozoa that were recovered from fish, Mackerel (Scomber scombrus) was susceptible to Coccidia species were recovered from intestine of Nematode infection at the infection rate of 97.09% Herring fish (Clupea harengus) and Mackerel

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(Scomber scombrus) with a relative prevalence of mackerel (Trachurus mediterraneus) and Mackerel 1.8% and 1.9%, respectively Table (4). (Scomber scombrus) with a relative abundance of Concerning Crustacea, Argulus species were 1.1% and 0.97 %, respectively Table (4). recovered externally from the skin of Horse

Table (1): Total percentage of infected fish with different types of parasites in examined fish (n=100).

Rate of infection* Type of parasite Number % Nematode 69 69 % 7 7 % Trematode Crustacea 2 2 % Coccidia 4 4 %

* There was a mixed infection. Table (2): Parasitic infection rate and fish susceptibility to different types of parasites (n=25). Species of Nematode Trematodes Protozoa Crustacea Frozen Fish Number % Number % Number % Number % Herring fish 24 96 - - 2 8 - - Horse 22 88 1 4 - - 1 4 mackerel Mackerel 23 92 - - 2 8 1 4 Fish fillet - - 4 16 - - - -

Table (3): Fish susceptibility to different types of parasite Fish susceptibility to different types of parasites Number Type of Nematode Trematode Protozoa Crustacea of fish parasite No % No % No % No % /fish Herring 111 109 98.2% - - 2 1.8% - - Mackerel 103 100 97,09% - - 2 1.9% 1 0,97% Horse 91 89 97.8% 1 1.1% - - 1 1.1% mackerel - Fish fillet* 25 - 4 16% - - - - * In fish fillet, the number of parasites refers to number of fish examined and the number of fish susceptible to Trematode refers to number of infected fish. Table (4): Parasitic infection rate and the prevalence of different parasite types. Nematodes Trematodes Protozoa Crustacea Number Fish Pseudo Of Anisakis Contracaecum Species terranova spp Parasite simplex spp. . Clinostomum Coccidea Argulus

No %* No % No % No % No % No % Frozen 111 65 58.5 19 17.12 25 22.5 - - 2 1.8 - - herring Horse 91 51 56.04 18 19.78 20 21,98 1 1.1 - - 1 1.1 mackerel Mackerel 103 59 57.28 25 24.27 16 15.53 - - 2 1.9 1 .97 Fish fillet 25 ------25 16 - - - - * The percentage of each parasite = Number of specific parasite recovered / total number of parasites recove

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4. DISCUSSION Nematodes of Pseudoterranova species were isolated The present study was carried out on 100 examined from Herring fish (Clupea harengus), Mackerel fish samples of imported frozen fish , 73 fish (73%) (Scomber scombrus), Horse mackerel (Trachurus harboured 6 species of parasites, 3 Nematodes (69%) mediterraneus) and the Fish fillet (Pangasius ,one Trematode (5%) ,one Protozoa (4%), and one hypophthalmus) with a moderate prevalence. A lower Crustacea (2%). prevalence of this parasite was recorded by Moller et The most important one is the Nematode as it al., (1991), Cremonte and Sardella (1997), Eissa et al. produce clinical symptomatology characterized by (1998), Herreras et al. (2000), Abdou ( 2005) and Al- serious gastrointestinal lesion (Eguia et al.,(2003)and Zubaidy et al. (2012). On the other hand, higher Montalto et al.,(2005) ), More ever ,owing to the prevalence of this parasite was recorded by thermo stability of Anisakis simplex allergens ,the Zdzitowiecki (1978) and Sey and Petter (1998). ingestion of safely cooked of Anisakis simplex In this study, examined fishes were free from allergens ,the ingestion of safely cooked fish Monogenean Trematodes, as the result disagree with containing dead parasites can also be potentially Price, ( 1967), Ozturk, and Altunel, ( 2006), Akhter et dangerous and can cause severe allergic reaction such al. (2007), Koyun and Altunel (2011), Koyun, (2011), as contact dermatitis and asthma (Audicana et al( Ramudu and Dash ( 2013) and Perveen, et al. (2013). 2002) and EL-Daly et al .,(2004) ). On the other hand, the result agrees with Ramudu and Dash (2013) as reported for infection with The present study revealed that Nematode of Anisakis Gyrodactylus species. simplex was isolated from Herring fish (Clupea harengus), Mackerel fish (Scomber scombrus), Horse Clinostomum species were recorded mainly in the mackerel (|Trachurus mediterraneus) and the Fish Fish fillet, and also in mainly the Horse mackerel, but fillet (Pangasius hypophthalmus) with a relatively with a slightly low infection rate. Higher prevalence high infection rates. Lower prevalence of this parasite of this parasite was recorded by Taber, (1972), was recorded by Hogans et al .(1983) , Mahmoud Newman, et al . (1976), Daly , et al. (2002) , (1986), Romuk –wodoracki (1988), Abd EL-maksoud McAllister ,et al. (2010) and Morais, et al. (2011). On (1992), Adroher et al .(1996), Cremonte and Sardella the other hand, lower prevalence of this parasite was (1997), Alves et al. (2003), Tolonen and Karlsbakk recorded by Thapa, et al. (2008). (2003), EL –Daly et al.(2004), EL-Gazzar et al. (2004), Abdou, ( 2005 ), Alves and Luque (2006), In this study we found fishes that were infected with Abd El-Ghany (2007), Abd Al-Aal et al. (2008), Protozoa that represented mainly by Coccidia, which Serracca et al. (2013) and Mohamed et al., (2013). recovered from Herring and Mackerel. The prevalence On the other hand, higher prevalence was reported by rate in the Herring and the Mackerel fish in this study Abd EL-maksoud (1992), Piccolo,et al. (1999), was lower than that reported by Baska, (1997), and, Manfredi et al., (2000), Aref (2006), Abd Al-Aal et al. Marty, et al. (1998). Parallel to this, percentages of (2008) and Nada et al. (2011). infected fishes with Crustacea which represented in Argulus species that were found in the Herring and Slightly low prevalence of Nematode was reported in Mackerel were lower than that reported by Jalali, et al. this study that included Contracaecum species which (2008), ALAŞ, et al. (2010), Raissy, et al (2010), were isolated from Herring fish (Clupea harengus), Notash, (2012), and Perveen, et al., (2013). mackerel fish (Scomber scombrus), Horse mackerel (Trachurus mediterraneus) and the Fish fillet 5. REFERENCES (Pangasius hypophthalmus). Lower prevalence of this Abd-Al-Aal, Z., Amer, O.H., El-Ashram, A.A., El-Ekiaby, parasite was recorded by Valter (1979), Fagerholm W.T., 2008. Light and electron microscopic studies on (1982), Valtonen et al. (1988), Shukhgalter and some larvae in marine fishes. Zag. Vet. J., 36: 110-118. Nigmatullin (2001), Al-Zubaidy A. B. (2009) and A Abd El-Ghany, A.M., 2007. Parasites of some imported del M. et al. (2013). On the other hand, higher fish. M.V.Sc. Thesis, (Parasitology), Fac. Vet. Med., Zag. Univ. prevalence of this parasite was recorded by Cremonte Abd El – Maksoud, S.A., 1992. Zoonotic agents in marine and Sardella (1997), Lymbery, et al. (2002), Luque et fish marketed in Dumyat. M.V.Sc. Thesis, (), al. (2003) and Barson, (2003). Fac. Vet. Med., Zag. Univ. 113

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