Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T03:19:42.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluation and Microanalysis of Parasitic and Bacterial Agents of Egyptian Fresh Sushi, Salmo salar

Part of: Micrographia Collection

Published online by Cambridge University Press:  13 November 2019

Sara S. Abdel-Hakeem Open the ORCID record for Sara S. Abdel-Hakeem [Opens in a new window] ,
Ghada Abd-Elmonsef Mahmoud Open the ORCID record for Ghada Abd-Elmonsef Mahmoud [Opens in a new window]  and
Hanan H. Abdel-Hafeez Open the ORCID record for Hanan H. Abdel-Hafeez [Opens in a new window]
Sara S. Abdel-Hakeem
Affiliation:
Parasitology Lab, Zoology Department, Faculty of Science, Assiut University, Assiut 71516, Egypt
Ghada Abd-Elmonsef Mahmoud
Affiliation:
Department of Botany and Microbiology, Faculty of Science, Assiut University, Assiut 71516, Egypt
Hanan H. Abdel-Hafeez*
Affiliation:
Department of Anatomy, Embryology and Histology, Faculty of Veterinary Medicine, Assiut University, Assiut 71516, Egypt (Previous PhD student) Department of Veterinary Sciences, Institute for Anatomy, Histology and Embryology, Ludwig Maximilian University, Veterinärstrasse 13, DE-80539 Munich, Germany
*
*Author for correspondence: Hanan H. Abdel-Hafeez, E-mail: [email protected]
Get access

Abstract

The present study aimed to evaluate the quality of fresh sushi in Egypt. Fifty samples of sushi (Salmo salar) were collected from restaurants in Alexandria, Egypt. Paraffin, semi-thin and ultra-thin sections were used for parasitological analysis by light and transmission electron microscopy. Bacteria were isolated by the dilution plate and direct plate methods and identified by a Vitek system. Twenty (40%) of the total examined samples showed microsporidia and helminth metacercariae infections. Histochemical stains showed distinct pinkish-red pyriform microspores embedded in muscular tissue stained with Gram, periodic acid-Schiff (PAS), and Ziehl–Neelsen (ZN) stains. Semi-thin sections showed double membrane xenoma-inducing granulomas containing spores at different developmental stages. Empty sporophorous vesicles and free spores were observed in the electron microscopic images. A bacteriological assay showed forty samples (80%) contaminated with human pathogenic bacteria with the average total bacterial counts ranging from 32 to 526 CFU/g. Four species of human pathogenic bacteria were identified in the examined samples, namely Klebsiella pneumoniae, Escherichia coli, Staphylococcus aureus, and Serratia plymuthica in 40, 38, 11, and 6 samples, respectively. These constitute the first record of fresh sushi product in Egypt and indicate the potential pathogenicity associated with raw seafood products.

Keywords

metacercariamicrosporepathogenic bacteriasushi
Type
Micrographia
Information
Microscopy and Microanalysis , Volume 25 , Issue 6 , December 2019 , pp. 1498 - 1508
Copyright
Copyright © Microscopy Society of America 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdel-Ghaffar, F, Bashtar, A, Mehlhorn, H, AL-Rasheid, K & Morsy, K (2011). Microsporidian parasites: A danger facing marine fishes of the Red Sea. Parasitol Res 108, 219–225. doi:10.1007/s00436-010-2061-1.Google Scholar
Abdel-Hafeez, HH & Soliman, SA (2016). Origin of rodlet cells and mapping their distribution in ruby-red-fin shark (rainbow shark) Epalzeorhynchos frenatum (Teleostei: Cyprinidae): Light, immunohistochemistry and ultrastructure study. J Cytol Histol 7. doi:10.4172/21577099.1000345.Google Scholar
Abdel-Hafeez, HH & Soliman, SA (2017). New description of telocyte sheaths in the bovine uterine tube: An immunohistochemical and scanning microscopic study. Cells Tissues Organs 203(5), 295–315.Google Scholar
Abdel-Hakeem, S, Soliman, SA, Abd-Elhafeez, HH, Abdel- Hafez, E & Zaki, RS (2019). Occurrence of metacercarial cyst of Ascocotyle (Ascocotyle sp.) in the gills of ruby-red-fin shark (rainbow shark) Epalzeorhynchos frenatum (Teleostei: Cyprinidae): Light microscopic study. EC Clin Exp Anat 2, 296–304.Google Scholar
Abd-Elkareem, M (2017). Cell-specific immuno-localization of progesterone receptor alpha in the rabbit ovary during pregnancy and after parturition. Anim Reprod Sci 180, 100–120. doi:10.1016/j.anireprosci.2017.03.007Google Scholar
Abdel-Maksoud, Fatma M, Abd-Elhafeez, Hanan H & Soliman, Soha A (2019). Morphological changes of telocytes in camel efferent ductules in response to seasonal variations during the reproductive cycle. Sci Rep 9(1), 4507. 10.1038/s41598-019-41143-y.Google Scholar
Adams, AM, Leja, LL, Jinneman, K, Beeh, J, Yuenz, GA & Wekelv, MM (1994). Anisakid parasites, Staphylococcus aureus and Bacillus cereus in sushi and sashimi from Seattle area restaurants. J Food Prot 57, 311–317.Google Scholar
Ahmed, L, El-Dib, NA & El-Boraey, Y (1999). Capillaria phillipinensis: An emerging parasite causing severe diarrhoea in Egypt. J Egypt Soc Parasitol 29, 483–493.Google Scholar
Arpenter, JL (1990). Klebsiella pulmonary infections: Occurrence at one medical center and review. Rev Infect Dis 12, 672–682.Google Scholar
Asai, Y, Murase, T, Osawa, R, Okitsu, T, Suzuki, R, Sata, S, Yamai, S, Terajima, J, Izumiya, H, Tamura, K & Watanabe, H (1999). Isolation of Shiga toxin-producing Escherichia coli O157:H7 from processed salmon roe associated with the outbreaks in Japan, 1998, and a molecular typing of the isolates by pulsed-field gel electrophoresis. Kansenshogaku Zasshi 73, 20–24.Google Scholar
Asaishi, K, Nishino, C & Hayasaka, H (1989). Geographical Distribution and Epidemiology. Tokyo: Springer-Verlag. pp. 31–36.Google Scholar
Atanassova, V, Reich, F & Klein, G (2008). Microbiological quality of sushi from Sushi bars and retailers. J Food Prot 71, 860–864.Google Scholar
Atlas, RM (1993). Handbook of Microbiological Media. Boca Raton, FL: CRC Press.Google Scholar
Austin, DN, Mikhail, MG & Chiodini, PL (1999). Intestinal capillariasis acquired in Egypt. Eur J Gastroenterol Hepatol 11, 935–936.Google Scholar
Ayulo, AM, Machado, RA & Scussel, VM (1994). Enterotoxigenic Escherichia coli and Staphylococcus aureus in fish and seafood from the southern region of Brazil. Int J Food Microbiol 24, 171–178.Google Scholar
Batista, CM, Ribeiro, ML, De Souza, MJ, Borges, LJ, Ferreira, TA & André, MC (2017). Microbiological and physicochemical qualities of sushi and sashimi from Japanese restaurants in Brazil. J Food Nutr Res 5, 729–735.Google Scholar
Bruno, DW, Nowak, B & Elliott, DG (2006). Review: Guide to the identification of fish protozoan and metazoan parasites in stained tissue sections. Dis Aquat Org 70, 1–36.Google Scholar
Canning, EU & Curry, A (2005). Microgemma vivaresi (Microsporidia: Tetramicridae): Host reaction to xenoma induced in sea scorpions, Taurulus bubalis (Osteichthyes: Cottidae). Folia Parasitol 52, 95–102.Google Scholar
Canning, EU & Lom, J (1986). The Microsporidia of Vertebrates. London: Academic Press.Google Scholar
Casal, G, Matos, E, Teles-Grilo, ML & Azevedo, C (2008). A new microsporidian parasite, Potaspora morhaphis n. gen., n.sp. (Microsporidia) infecting the teleostean fish, Potamorhaphis guianensis from the River Amazon. Morphological, ultrastructural and molecular characterization. Parsitology 135, 1053–1064.Google Scholar
Chattopadhyay, P & Adhikari, S (2014). Fish - Catching and Handling.Google Scholar
Costa, C, Melo-Moreira, E & Pinheiro de Carvalho, MA (2016). Occurrence of microsporidians Glugea hertwigi and Pleistophora ladogensis, in smelt Osmerus eperlanus from two German rivers, North Sea coast. Dis Aquat Organ 121, 49–57.Google Scholar
Egyptian Organization for Standards and Quality, EOSQ (2017). Managing Quality in Egypt: A directory of services for SMEs. In Food saftey (Geneva, Switzerland/Cairo, Egypt, International Trade Centre (ITC)).Google Scholar
Eklund, MW, Peterson, ME, Poysky, FT, Paranjpye, RN & Pelroy, GA (2004). Control of bacterial pathogens during processing of cold-smoked and dried salmon strips. J Food Prot 67, 347–351.Google Scholar
El-Deep, NM (2002). Parasites Infecting Some Fishes in Egypt. Egypt: Ain Shams University.Google Scholar
European Food Safety Authority (2010). Scientific Opinion on risk assessment of parasites in fishery products: EFSA Panel on Biological Hazards (BIOHAZ). In EFSA Journal (Parma, Italy, European Food Safety Authority (EFSA)), p. 1543.Google Scholar
Fierer, J (2012). Biofilm formation and Klebsiella pneumoniae liver abscess: True, true and unrelated? Virulence 3, 241–242.Google Scholar
Franzen, C & Müller, A (1999). Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clin Microbiol Rev 12, 243–285.Google Scholar
Freeman, MA, Turnbull, JF, Yeomans, WE & Bean, CW (2010). Prospects for management strategies of invasive crayfish populations with an emphasis on biological control. Aquat Conserv 20, 211–223.Google Scholar
Greenlees, KJ, Machado, J, Bell, T & Sundlof, SF (1998). Food borne microbial pathogens of cultured aquatic species. Vet Clin North Am: Large Anim Pract 14, 101–112.Google Scholar
Gross, CA, Reddy, CK & Dazzo, FB (2010). CMEIAS color segmentation: An improved computing technology to process color images for quantitative microbial ecology studies at single-cell resolution. Microb Ecol 59, 400–414.Google Scholar
Hanna, A, Koskinen, H, Valtonen, ET & Taskinen, J (2017). Spore-Forming Parasites Infecting Muscles of Freshwater Fishes: Ecology and Epidemiology. Finland: University of Jyvaskyla, Faculty of Mathematics and Science.Google Scholar
Hastein, T, Hjeltnes, B, Lillehaug, A, Utne Skåre, J, Berntssen, M & Lundebye, AK (2006). Food safety hazards that occur during the production stage: Challenges for fish farming and the fishing industry. Rev Sci Tech 25, 607–625.Google Scholar
Hicks, TD (2016). Seafood safety and quality: The consumer's role. Foods 5, 1–11.Google Scholar
Holt, JG, Krieg, PH, Sneath, JT & Staley Williams, ST (1994). Bergeys Manual of Determinative Bacteriology, 9th ed. Baltimore, MD: Williams & Wilkins Co.Google Scholar
Hwang, DF, Huang, YR, Lin, KP, Chen, TY, Lin, SJ, Chen, LH & Hsieh, HS (2004). Investigation of hygienic quality and freshness of marketed fresh seafood in Northern Taiwan. Shokuhin Eiseigaku Zasshi 45, 225–230.Google Scholar
Karnovsky, MJ (1965). A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27, 137A–138A.Google Scholar
Karthiga Rani, M, Chelladurai, G & Jayanthi, G (2016). Isolation and identification of bacteria from marine market fish Scomberomorus guttatus (Bloch and Schneider, 1801) from Madurai district, Tamil Nadu, India. J Parasit Dis 40, 1062–1065.Google Scholar
Kawai, T, Sekizuka, T, Yahata, Y, Kuroda, M, Kumeda, Y, Iijima, Y, Kamata, Y, Sugita-Konishi, Y & Ohnishi, T (2012). Identification of Kudoa septempunctata as the causative agent of novel food poisoning outbreaks in Japan by consumption of Paralichthys olivaceus in raw fish. Clin Infect Dis 54, 1046–1052.Google Scholar
Kent, ML (2000). Marine netpen farming leads to infections with some unusual parasites. Int J Parasitol 30, 321–326.Google Scholar
Kliks, MM (1986). Human anisakiasis: An update. J Am Med Assoc 255, 2605.Google Scholar
Kristmundssona, Á & Freeman, MA (2014). Negative effects of Kudoa islandica n. sp. (Myxosporea: Kudoidae) on aquaculture and wild fisheries in Iceland. Int J Parasitol Parasites Wildl 3, 135–146. doi: 10.1016/j.ijppaw.2014.06.001Google Scholar
Kure, K & Yokoi, M (1989). Safe sushi. N Engl J Med 321, 900–901.Google Scholar
Lemos, AC, Coelho, JC, Matos, ED, Monta, G, Aguiar, F & Badaró, R (2007). Paragonimiasis: First case reported in Brazil. Braz J Infect Dis 11, 153–156. doi:10.1590/S1413-86702007000100031.Google Scholar
Lom, J & Dykova, I (1992). Developments aquaculture and Fisheries Science, Edition. Amsterdam: Elsevier, repeated reference, please delete it.Google Scholar
Lom, J & Dyková, I (1992). Protozoan Parasites of Fishes (Developments in Aquaculture and Fisheries Science), vol. 26. Amsterdam: Elsevier. pp. 315.Google Scholar
Lom, J & Nilsen, F (2003). Fish microsporidian: Fine structural diversity and phylogeny. Int J Parasitol: Parasites Wildl 33, 107–127.Google Scholar
Macé, S, Cornet, J, Chevalier, F, Cardinal, M, Pilet, M, Dousseta, X & Joffraud, J (2012). Characterisation of the spoilage microbiota in raw salmon (Salmo salar) steaks stored under vacuum or modified atmosphere packaging combining conventional methods and PCR-TTGE. Food Microbiol 30, 164–172.Google Scholar
Matthews, CG, Richards, RH, Shinn, AP & Cox, DI (2013). Gill pathology in Scottish farmed Atlantic salmon, Salmo salar L., associated with the microsporidian Desmozoon lepeophtherii Freeman et Sommerville, 2009. J Fish Dis 36, 861–869.Google Scholar
Mladineo, I (2006). Microsporidia sp. in Atlantic bluefin tuna (Thunnus thynnus). Bull Eur Assoc Fish Pathol 26, 153–156.Google Scholar
Nawa, Y, Hatz, C & Blum, J (2005). Sushi delights and parasites: The risk of fishborne and foodborne parasitic zoonoses in Asia. Travel Med 41, 1297–1303.Google Scholar
Novotny, L, Dvorska, L, Lorencova, A, Beran, V & Pavlik, I (2004). Fish: A potential source of bacterial pathogens for human beings. Vet Med 49, 343–358.Google Scholar
Nylund, S, Andersen, L, Sævareid, I, Plarre, H, Watanabe, K, Arnesen, CE, Karlsbakk, E & Nylund, A (2011). Diseases of farmed Atlantic salmon Salmo salar associated with infections by the microsporidian Paranucleospora theridion. Dis Aquat Org 94, 41–57. doi:10.3354/dao02313.Google Scholar
Nylund, S, Nylund, A, Watanabe, K, Arnesen, CE & Karlsbakk, E (2010). Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the Salmon Louse (Lepeophtheirus salmonis, Copepoda) and Atlantic Salmon (Salmo salar). J Eukaryot Microbiol 57, 95–114.Google Scholar
Oshima, T (1987). Anisakiasis - is the sushi bar guilty? Parasitol Today 3, 44–48.Google Scholar
Palenzuela, O, Redondo, MJ, Cali, A, Takvorian, PM, Alonso-Naveiro, M, Alvarez-Pellitero, P & Sitjà-Bobadilla, A (2014). A new intranuclear microsporidium, Enterospora nucleophila n. sp., causing an emaciative syndrome in a piscine host (Sparus aurata), prompts the redescription of the family Enterocytozoonidae. Int J Parasitol 44, 189–203.Google Scholar
Praveena, PE, Bhuvaneswari, T, Krishnan, AN, Jagadeesan, V, Sahaya Rajan, JJ & Jithendran, KP (2018). An improved microscopic method for the rapid diagnosis of emerging microsporidian parasite, Enterocytozoon hepatopenaei in shrimp farms. Curr Sci 115(4), 00113891.Google Scholar
Ramanan, P & Prittb, BS (2014). Extraintestinal microsporidiosis. J Clin Microbiol 52, 3839–3844.Google Scholar
Reynods, ES (1963). The use of lead citrate at high pH as an electron-opaque stain for electron microscopy. J Cell Biol 17, 208–212.Google Scholar
Richardson, KC, Jarett, L & Finke, EH (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol 35, 313–323.Google Scholar
Shaw, RW & Kent, ML (1999). Fish Microsporidia. In The microsporidia and microsporidiosis. Washington, DC: American Society for Microbiology. pp. 418–446.Google Scholar
Soliman, SA & Abd-Elhafeez, HH (2016a). Are C-KIT, MMP-9 and Type II collagen positive undifferentiated cells involved in cartilage growth? A description of unusual interstitial type of cartilage growth. J Cytol Histol 7, 440.Google Scholar
Soliman, SA & Abd-Elhafeez, HH (2016b). Mesenchymal cells in cartilage growth and regeneration “an Immunohistochemical and electron microscopic study”. J Cytol Histol 7, 437. doi:10.4172/2157-7099.1000437.Google Scholar
Soliman, SA, Abd-Elhafeez, HH & Enas, A (2017). A new mechanism of cartilage growth in mammals “Involvement of CD117 Positive Undifferentiated Cells in Interstitial Growth”. J Cytol Histol 1(1001).Google Scholar
Soliman, SA, Kamal, BM & Abd-Elhafeez, HH (2019). Cellular invasion and matrix degradation, a different type of matrix-degrading cells in the cartilage of catfish (Clarias gariepinus) and Japanese quail embryos (Coturnix coturnix japonica). Microsc Microanal. doi:10.1017/S1431927619014892.Google Scholar
Sprague, V, Becnel, JJ & Edwin, IH (1992). Taxonomy of phylum Microspora. Crit Rev Microbiol 18, 285–395.Google Scholar
Suvarna, SK, Layton, C & Bancroft, JD (2013). Bancroft's Theory and Practice of Histological Techniques, 7th ed. Churchill Livingstone: Elsevier.Google Scholar
Vávra, J & Lukeš, J (2013). Microsporidia and 'the art of living together'. Adv Parasitol 82, 254–319.Google Scholar
Vieira, RHSF, Rodrigues, DP, Gocalves, FA, Menezes, FGR, Aragao, JS & Sousa, OV (2001). Microbicidal effect of medicinal plant extracts (Psidium guajava Linn. and Carica papaya Linn.) upon bacteria isolated from fish muscle and known to induce diarrhea in children. Rev Inst Med Trop São Paulo 43, 145–148.Google Scholar
Weber, R, Schwartz, DA & Deplazes, P (1999). Laboratory Diagnosis of Microsporidiosis. In The microsporidia and mirosporidiosis. Washington, DC: American Society for Microbiology. pp. 315–362.Google Scholar
Whipple, MJ & Rohovec, JS (1994). The effect of heat and low pH on selected viral and bacterial fish pathogens. Aquaculture 123, 179–189.Google Scholar
Whitaker, DJ & Kent, ML (1991). Kudoa thyrsites (Myxosporea): A cause of soft flesh in farm-reared Atlantic salmon (Salmo salar). J Aquat Anim Health 3, 291–294.Google Scholar
WHO, National Institute of Aging 2011. Global Health and Aging (NIH Publication 11-7737). National Institutes of Health and World Health Organization.Google Scholar
WHO, World Health Organisation (2009). Basic Food Safety for Health Workers. Geneva: World Health Organization.Google Scholar
Yokoyama, H, Lee, SJ & Bell, AS (2002). Occurrence of a new microsporidium in the skeletal muscle of the flying fish Cypselurus pinnatibarbatus japonicus (Exocoetidae) from Yakushima, Japan. Folia Parasitol 49, 9–15.Google Scholar
Young, CA & Jones, SRM (2005). Epitopes associated with mature spores not recognized on Kudoa thyrsites from recently infected Atlantic salmon smolts. Dis Aquat Org 63, 267–271.Google Scholar
Yousef, MS, Abd-Elhafeez, HH, Talukder, AK & Miyamoto, A (2019). Ovulatory follicular fluid induces sperm phagocytosis by neutrophils, but oviductal fluid around oestrus suppresses its inflammatory effect in the buffalo oviduct in vitro. Mol Reprod Dev 86, 835–846.Google Scholar
Supplementary material: File

Abdel-Hakeem et al. supplementary material

Abdel-Hakeem et al. supplementary material 1

Download Abdel-Hakeem et al. supplementary material(File)
File 15.7 KB
Supplementary material: Image

Abdel-Hakeem et al. supplementary material

Abdel-Hakeem et al. supplementary material 2

Download Abdel-Hakeem et al. supplementary material(Image)
Image 3.9 MB
Supplementary material: File

Abdel-Hakeem et al. supplementary material

Abdel-Hakeem et al. supplementary material 3

Download Abdel-Hakeem et al. supplementary material(File)
File 12.1 KB