Introduction

The Anisakis, a parasite of worldwide distribution, whose larva (L₃) of white-pinkish filiform appearance, approximately 2 to 3 cm long, can be detected with the naked eye forming tangles in the visceral bundle or encysted in the muscle closest to the abdominal cavity of many marine fish^1-2 and even freshwater fish³. Its definitive host is cetaceans and pinnipeds, with hake, cod, anchovy, mackerel, salmon, horse mackerel, and others as intermediate hosts. Humans become infected by consuming undercooked dishes such as sushi, ceviche, smoked foods, semi-preserved foods, etc., which contain the larva L₃^4-6.

The human is an accidental host, it does not develop, however, a single larva can generate intense abdominal pain, vomiting, diarrhea, fever, allergic diseases, perforating the gastrointestinal mucosa, and may invade other organs (lung, pancreas, liver), generating gastritis, enteritis, etc^1,4,7-9. Although the reported cases indicate that this is a rare disease, its true incidence could potentially be higher since this condition may go undiagnosed.

The consumption of raw or semi-cooked fish in a traditional dish called ceviche is widespread in Cajamarca and throughout Peru. In places far from fishing ports, due to a lack of knowledge, bromatological controls of seafood are not important for the responsible entities, so there is no real and reliable information on the public health risks posed by the consumption of semi-cooked fish meat with parasite larvae embedded in the muscles; for this reason, the objective of this study was to identify larvae (L₃) of Anisakis sp. in jack mackerel muscle marketed in the city of Cajamarca.

Materials and methods

The research was carried out between May and July 2016, in the city of Cajamarca. A total of 120 jack mackerel fish (T. s. murphyi) identified by their morphological characteristics (10 samples per week) of different sizes and weights were collected from the various stalls of the Modelo, San Sebastian, and Santa Rosa markets of this city, which vendors are supplied from the port of Santa Rosa - Chiclayo - Lambayeque - Peru. Once the samples were obtained, they were transported to the Laboratorio de Parasitología Veterinaria y Enfermedades Parasitarias (LPV-EP) of the Facultad de Ciencias Veterinarias from the Universidad Nacional de Cajamarca (FCV-UNC) for study. With the established biosecurity measures, each fish was eviscerated and carefully washed with clean water, proceeding with transverse cuts of the dorsal musculature (epaxial and hypaxial) using a scalpel and acute observation with the aid of a magnifying glass for the presence of parasite larvae.

The larvae were identified by microscopy (Leitz WETZLAR at 50 and 100 X) based on their morphological characteristics (color, shape, and size)^1,11-14.

Since this was a study that did not involve live animals, it was not necessary to obtain the approval of an ethics committee; however, the present research was approved by the Comité Científico of the FCV-UNC, Peru.

Results

Table 1
Morphological characteristics of the larvae found

n	Positive (%)	Variable	Characteristic
120	1 (0.83%)	Color	Off-white
		Form	Rounded and elongated body, with pointed ends.
		Size	2.5 cm length x 1.0 mm width

Figure 1
Photographs of the L₃ larvae found, shown coiled (a), without membrane (b), length (c) and width (d)

Figure 2
Photomicrographs of the structures of the L₃ larva found. Anterior end (a) viewed at 50X, and structures (b, c); posterior end (d), both views at 100X

Discussion

Positivity to Anisakis sp. larvae was extremely low (0.83 %), due to climatic conditions, so it does not yet represent a public health problem⁹. In addition, most of its commercialization comes from the main ports of the northern coast of the country (Peru), so the probability of containing parasites is very low, so the risk of infection is negligible; however, the results are not a reason for carelessness since in cases of anisakiasis there are no vaccines or effective pharmacotherapy, resorting to endoscopy, colonoscopy or surgical intervention as the effective methods¹⁰.

In several places, people have reported illnesses compatible with anisakiasis after consuming dishes based on insufficiently cooked fish^15,19, however, this should not be a limiting factor for the consumption of any kind of fish purchased with sanitary guarantees and cooked at the recommended temperature and time. On the other hand, it is necessary to take into account the risky dishes and avoid ingestion of those prepared with raw fish that was not previously frozen; in addition to having biosecurity measures in their preparation^1,4.

In contrast to our results, two studies have reported the presence of Anisakis sp. larvae such as A. pegreffii and A. physeteris in three types of fish from the Peruvian coast^20,21. Also in various regions around the world, prevalences much higher than those found have been reported in Australia²², Albania²³, Egypt²⁴, Chile²⁵, and many other countries, so it is recommended not to relax biosecurity measures throughout the process that culminates with the consumption of prepared fish.

The results suggest that, although it is true that Anisakis sp. is not a common parasite, if surveillance measures are not taken, it could constitute a public health problem in the fish-consuming population.

Cited Literature

1. Fiandor Román A, Audicana Berasategui MT. La alergia a pescados y mariscos y Anisakis simplex. En: Zubeldia JM, Baeza ML, Chivato T, Jáuregui I, Senen CJ, editores. Libro de las enfermedades alérgicas [Internet]. Bilbao: Fundación BBVA; 2012. p. 275-86. Recuperado a partir de: https://www.fbbva.es/wp-content/uploads/2021/10/Libro-enfermedades-alergicas_FBBVA.pdf

2. Ángeles-Hernández JC, Gómez-de Anda FR, Reyes-Rodríguez NE, Vega-Sánchez V, García-Reyna PB, Campos-Montiel RG, et al. Genera and species of the Anisakidae family and their geographical distribution. Animals (Basel) 2020;10 (12):2374. DOI: https://doi.org/10.3390/ani10122374

3. Airahuacho Bautista FE, Cuellar Reyes JC, Romero Bozzetta JL, Encarnación Valentín NF. Primer reporte de Anisakis spp. en peces de agua dulce en Huacho, Perú. Rev Investig Vet Perú 2019;30(4):1662-9. DOI: https://doi.org/10.15381/rivep.v30i4.17151

4. Vicente Pardo JM. El anisakis y sus enfermedades como enfermedad profesional. Med Segur Trab 2016;62(244):223-40.

5. Tokiwa T, Kobayashi Y, Ike K, Morishima Y, Sugiyama H. Detection of Anisakid larvae in marinated mackerel sushi in Tokyo, Japan. Jpn J Infect Dis 2018;71(1):88-9. DOI: https://doi.org/10.7883/yoken.JJID.2017.280

6. Grano-Maldonado MI, Medina-Vera RA. Parasitosis, gastronomic tourism and food identities: A public health problem in Mazatlán, Sinaloa, México. Neotrop Helminthol 2019;13(2):203-25. DOI: https://doi.org/10.24039/rnh2019132641

7. Pravettoni V, Primavesi L, Piantanida M. Anisakis simplex: current knowledge. Eur Ann Allergy Clin Immunol 2012;44(4):150-6.

8. Ahmed M, Ayoob F, Kesavan M, Gumaste V, Khalil A. Gastrointestinal anisakidosis - watch what you eat. Cureus 2016;8(11):e860. DOI: https://doi.org/10.7759/cureus.860

9. Maguiña Vargas C. Anisakiasis no es problema de salud pública. Rev Med Hered 2017;28(4):223-5. DOI: https://doi.org/10.20453/rmh.v28i4.3220

10. Shimamura Y, Muwanwella N, Chandran S, Kandel G, Marcon N. Common symptoms from an uncommon infection: gastrointestinal anisakiasis. Can J Gastroenterol Hepatol 2016;2016: 5176502. DOI: https://doi.org/10.1155/2016/5176502

11. Abou-Rahma Y, Abdel-Gaber R, Kamal Ahmed A. First record of Anisakis simplex third-stage larvae (Nematoda, Anisakidae) in European Hake Merluccius merluccius lessepsianus in Egyptian Water. J Parasitol Res 2016;2016:9609752. DOI: https://doi.org/10.1155/2016/9609752

12. Abdelsalam M, Attia MM, Mahmoud MA. Comparative morphomolecular identification and pathological changes associated with Anisakis simplex larvae (Nematoda: Anisakidae) infecting native and imported chub mackerel (Scomber japonicus) in Egypt. Reg Stud Mar Sci 2020;39: 101469. DOI: https://doi.org/10.1016/j.rsma.2020.101469

13. Simsek E, Pekmezci GZ, Yildirim A, Duzlu O, Onder Z, Ciloglu A, et al. Investigation of Anisakis larvae in different products of ready-to-eat fish meat and imported frozen fish in Turkey. Int J Food Microbiol 2020;333:108829. DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108829

14. Mattiucci S, Palomba M, Nascetti G. Anisakis. Encyclopedia of Infection and Immunity 2022;2: 408-23. DOI: https://doi.org/10.1016/B978-0-12-818731-9.00075-6

15. Bucci C, Gallotta S, Morra I, Fortunato A, Ciacci C, Iovino P. Anisakis, just think about it in an emergency! Int J Infect Dis 2013;17(11): e1071-2. DOI: https://doi.org/10.1016/j.ijid.2013.05.008

16. Fukita Y, Asaki T, Katakura Y. Some like it raw: An unwanted result of a sushi meal. Gastroenterology 2014;146(5):e8-e9. DOI: https://doi.org/10.1053/j.gastro.2013.12.040

17. Carmo J, Marques S, Bispo M, Serra D. Anisakiasis: a growing cause of abdominal pain!. BMJ Case Rep 2017;2017:bcr2016218857. DOI: https://doi.org/10.1136/bcr-2016-218857

18. Furuya K, Nakajima H, Sasaki Y, Urita Y. Anisakiasis: The risks of seafood consumption. Niger J Clin Pract 2018;21(11):1492-4. DOI: https://doi.org/10.4103/njcp.njcp_256_17

19. Aibinu IE, Smooker PM, Lopata AL. Anisakis nematodes in fish and shellfish- from infection to allergies. Int J Parasitol Parasites Wildl 2019;9: 384-93. DOI: https://doi.org/10.1016/j.ijppaw.2019.04.007

20. Aco Alburqueque R, Palomba M, Santoro M, Mattiucci S. Molecular Identification of zoonotic parasites of the Genus Anisakis (Nematoda: Anisakidae) from fish of the Southeastern Pacific Ocean (Off Peru Coast). Pathogens 2020;9(11): 910. DOI: https://doi.org/10.3390/pathogens9110910

21. Martínez-Rojas R, Mondragón-Martínez A, Rojas De-Los-Santos E, Cruz-Neyra L, García-Candela E, Delgado-Escalante A. Molecular identification and epidemiological data of Anisakis spp. (Nematoda: Anisakidae) larvae from Southeastern Pacific Ocean off Peru. Int J Parasitol Parasites Wildl 2021;16:138-44. DOI: https://doi.org/10.1016/j.ijppaw.2021.09.001

22. Shamsi S. The occurrence of Anisakis spp. in Australian waters: past, present, and future trends. Parasitol Res 2021;120(9):3007-33. DOI: https://doi.org/10.1007/s00436-021-07243-3

23. Ozuni E, Vodica A, Castrica M, Brecchia G, Curone G, Agradi S, et al. Prevalence of Anisakis Larvae in different fish species in Southern Albania: five-year monitoring (2016-2020). Appl Sci 2021;11(23):11528. DOI: https://doi.org/10.3390/app112311528

24. El Meghanawy RA, E.I ET, Salim Dalia A, Abdel Aziz AR. Epidemiological, morphological and molecular characterization of Anisakis simplex (sensu stricto) in Clupea harengus from Egypt. Vet Parasitol Reg Stud Reports 2021;24:100574. DOI: https://doi.org/10.1016/j.vprsr.2021.100574

25. Muñoz-Caro T, Machuca A, Morales P, Verdugo J, Reyes R, García M, et al. Prevalence and molecular identification of zoonotic Anisakis and Pseudoterranova species in fish destined to human consumption in Chile. Parasitol Res 2022;121(5): 1295-304. DOI: https://doi.org/10.1007/s00436-022-07459-x

Notes

Author notes

Alternative link

http://www.scielo.org.bo/scielo.php?script=sci_arttext&pid=S2311-25812022000200084&lng=es&nrm=iso&tlng=en (html)