Survival of Trichinella spiralis and T. pseudospiralis in Experimentally Infected Wild Boar Muscle Tissue under Freezing and Environmental Conditions
-
Clara Bessi
,
Mariano Emmanuel Ercole
,
Fernando Adrian Fariña
,
Francisco Montalvo
,
Valeria Fassa
,
Marcelo Acerbo
,
Miriam Mabel Ribicich
,
Mariana Inés Pasqualetti
Abstract
Background: The aim of this study was to investigate the survival of Trichinella spiralis and T. pseudospiralis in decaying wild boar tissue and assess their freezing tolerance in experimentally infected animals.
Methods: The present study was conducted in Buenos Aires City, Argentina during the 2018-2019 period. Two wild boars were used, one infected with 20,000 muscle larvae (ML) of T. spiralis and the other with T. pseudospiralis. Both animals were euthanized 19 weeks post-infection. Limbs from each boar were placed over soil in plastic containers to assess ML survival in decaying tissue, under natural temperature and humidity, shielded from rain. Weekly samples were taken for artificial digestion, and the ML were inoculated into mice to determine their reproductive capacity index (RCI). Additionally, to evaluate the freezing tolerance of the ML, muscle samples were stored at -18°C. Six samples were taken and digested after 2, 4, 7, 9, 11, and 14 days, with subsequent inoculation into mice to assess RCI.
Results: T. spiralis remained infective in decaying wild boar tissue for 11 weeks, while T. pseudospiralis remained infective for only 4 weeks. The freezing tolerance assay showed that T. spiralis ML remain infective for 9 days. However, T. pseudospiralis ML remain infective for only 2 days at -18°C.
Conclusion: The findings highlight the survival strategies of T. spiralis and T. pseudospiralis in different environmental conditions, which may have implications for understanding their transmission dynamics in wild animals.
1. Santrac V, Nedic DN, Maric J, et al. The first report of Trichinella pseudospiralis presence in domestic swine and T. britovi in wild boar in Bosnia and Herzegovina. Acta Parasitol. 2015; 60(3):471-475.
2. Owen IL, Reid SA. Survival of Trichinella papuae muscle larvae in a pig carcass maintained under simulated natural conditions in Papua New Guinea. J Helminthol. 2007; 81:429–432.
3. Pozio E, Darwin Murrell K. Systematics and Epidemiology of Trichinella. Adv Parasitol. 2006; 63:367–439.
4. Bilska-Zając E, Różycki M, Grądziel-Krukowska K, et al. Diversity of Trichinella species in relation to the host species and geographical location. Vet Parasitol. 2020; 279:109052.
5. Campbell WC. Trichinella and Trichinellosis. Plenum Press, New York, 1983. p. 581.
6. Stewart GL. Pathophysiology of the Muscle Phase, in: Campbell, W.C. (Ed.), Trichinella and Trichinosis. Springer US, Boston, MA. 1983. p. 241–264.
7. Von Köller J, Kapel CMO, Enemark HL, Hindsbo O. Infectivity of Trichinella spp. recovered from decaying mouse and fox muscle tissue. Parasite. 2001; 8(2 Suppl):S209-12.
8. Lacour SA, Heckmann A, Macé P, et al. Freeze-tolerance of Trichinella muscle larvae in experimentally infected wild boars. Vet Parasitol. 2013; 194:175–178.
9. Worley DE, Seesee FM, Espinosa RH, Sterner MC. Survival of sylvatic Trichinella spiralis isolates in frozen tissue and processed meat products. J Am Vet Med Assoc. 1986; 189:1047–1049.
10. Dick TA, Belosevic M. Observations on a Trichinella spiralis Isolate from a Polar Bear. J Parasitol. 1978; 64:1143–1145.
11. Pozio E, la Rosa G, Rossi P, Murrell KD. Biological Characterization of Trichinella Isolates from Various Host Species and Geographical Regions. J Parasitol. 1992; 78:647–653.
12. Malakauskas A, Kapel CMO. Tolerance to Low Temperatures of Domestic and Sylvatic Trichinella Spp. in Rat Muscle Tissue. J Parasitol. 2003; 89:744– 748.
13. Burke R, Masuoka P, Murrell KD. Swine Trichinella infection and geographic information system tools. Emerg Infect Dis. 2008; 14:1109–1111.
14. Murrell KD, Pozio E. Worldwide occurrence and impact of human trichinellosis, 1986-2009. Emerg Infect Dis. 2011, 17:2194-2202.
15. Franssen F, Swart A, vander Giessen J, Havelaar A, Takumi K. Parasite to patient: A quantitative risk model for Trichinella spp. in pork and wild boar meat. Int J Food Microbiol. 2017;241:262-275.
16. Gondek M, Grzelak S, Pyz-Łukasik R, Knysz P, Ziomek M, Bień-Kalinowska J. Insight into Trichinella britovi infection in pigs: Effect of various infectious doses on larvae density and spatial larvae distribution in carcasses and comparison of the detection of Anti-T. britovi IgG of Three Different Commercial ELISA Tests and Immunoblot Assay. Pathogens. 2022; 11(7):735.
17. Dupouy-Camet J. Trichinellosis: A worldwide zoonosis. Vet Parasitol. 2000; 93:191–200.
18. Ribicich M, Gamble HR, Bolpe J, et al. Trichinella infection in wild animals from endemic regions of Argentina. Parasitol Res. 2010; 107:377–380.
19. Fichi G, Stefanelli S, Pagani A, et al. Trichinellosis Outbreak Caused by Meat from a Wild Boar Hunted in an Italian Region Considered to be at Negligible Risk for Trichinella. Zoonoses Public Health. 2015; 62(4):285-291.
20. Kapel CMO, Pozio E, Sacchi L, Prestrud P. Freeze Tolerance, Morphology, and RAPD-PCR Identification of Trichinella nativa in Naturally Infected Arctic Foxes. J Parasitol. 1999; 85: 144-147.
21. Rostami A, Gamble HR, Dupouy-Camet J, Khazan H, Bruschi F. Meat sources of infection for outbreaks of human trichinellosis. Food Microbiol. 2017; 64:65-71.
22. Faber M, Schink S, Mayer-Scholl A, et al. Outbreak of trichinellosis due to wild boar meat and evaluation of the effectiveness of post exposure prophylaxis, Germany, 2013. Clin Infect Dis. 2015; 60(12):e98-e104.
23. Hill DE, Forbes L, Gajadhar AA, Gamble HR. Viability and infectivity of Trichinella spiralis muscle larvae in frozen horse tissue. Vet Parasitol. 2007; 146:102–106.
24. Bessi C, Ercole ME, Fariña FA, et al, Pasqualetti MI. Study of Trichinella patagoniensis in wild boars. Vet Parasitol. 2021; 297:109166.
25. Krivokapich SJ, Gonzalez-Prous CL, Gatti GM, Saldía L. First finding of Trichinella pseudospiralis in the Neotropical region. Vet Parasitol. 2015; 208:268– 271.
26. Gamble HR, Bessonov AS, Cuperlovic K, et al. International Commission on Trichinellosis: Recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Vet Parasitol. 2000; 93:393–408.
27. Anonymous. Servicio Meteorológico Nacional. Observatorio Buenos Aires. 2022. https://www.estadisticaciudad.gob.ar/eyc/?p=27702. Accesed 11 January 2022.
28. Kapel CMO, Gamble HR. Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. Int J Parasitol. 2000; 30:215–221.
29. Riva E, Steffan P, Guzmán M, Fiel C. Persistence of Trichinella spiralis muscle larvae in natural decaying mice. Parasitol Res. 2012; 111:249–255.
30. Stewart GL, Kennedy R., Larsen E. Infectivity of Trichinella pseudospiralis Isolated from Carrion, Source: J Parasitol. 1990; 76(5):750-751.
31. Kapel CMO. Host diversity and biological characteristics of the Trichinella genotypes and their effect on transmission. Vet Parasitol. 2000; 93:263–278.
32. Webster P, Malakauskas A, Kapel CMO. Infectivity of Trichinella papuae for experimentally infected red foxes (Vulpes vulpes). Vet Parasitol. 2002; 105:215–218.
33. Fariña F, Pasqualetti M, Ilgová J, Cardillo N, et al. Evaluation of the infectivity and the persistence of Trichinella patagoniensis in muscle tissue of decomposing guinea pig (Cavia porcellus). Parasitol Res. 2017; 116:371-375.
34. Pozio E. The impact of globalization and climate change on Trichinella spp. epidemiology. Food Waterborne Parasitol. 2022; 27:e00154.
35. Keppel G, Wardell‐Johnson GW. Refugia: keys to climate change management. Glob Chang Biology. 2012; 18(8):2389-2391.
36. Pozio E. Adaptation of Trichinella spp. for survival in cold climates. Food Waterborne Parasitol. 2016; 4:4–12.
37. Pozio E, La Rosa G, Amati M. Factors influencing the resistance of Trichinella muscle larvae to freezing. In: Trichinellosis. Proceedings of the 8th International Conference on Trichinellosis. Ed. Campbell CW, Pozio E, and Bruschi F. Rome: Instituto Superiore di Sanita Press, 1994. p:173–178.
38. Sacchi L, Corona S, Gajadhar AA, Pozio E. Ultrastructural characteristics of nurse cell-larva complex of four species of Trichinella in several hosts. Parasite. 2011; 8(2 Suppl):S54-8.
39. Kapel CMO, Webster P, Malakauskas A, Hurnikova Z, Gamble HR. Freeze tolerance of Trichinella genotypes in muscle tissue of experimentally infected pigs, horses, wild boars, mice, cats, and foxes. In: International Conference Trichinellosis, San Diego, 2004. p. 8-12.
40. Seymour J, Horstmann-Dehn L, Rosa C, Lopez JA. Occurrence and genotypic analysis of Trichinella species in Alaska marine-associated mammals of the Bering and Chukchi seas. Vet Parasitol. 2014; 200(1-2):153-164.
41. Rudneva OV, Аndreyanov ON, Sidor EA. Reprint of: The retention and concentration of glycogen in Trichinella nativа in the winter-spring period. Vet Parsitol. 2021; 297:109547.
42. Dick TA. Infectivity of isolates of Trichinella and the ability of an arctic isolate to survive freezing temperatures in the raccoon, Procyon lotor, under experimental conditions. J Wildl Dis. 1983; 19:333–336.
43. Raines KM, Stewart GL. Carbohydrate reserves and infectivity in Trichinella spiralis isolated from carrion. Parasitology. 1988; 96(Pt 3):533-41.
44. Davidson RK, Handeland K, Kapel CM. High tolerance to repeated cycles of freezing and thawing in different Trichinella nativa isolates. Parasitol Res. 2008; 103:1005-1010
45. Pauli JN, Zuckerberg B, Whiteman JP, Porter W. The subnivium: a deteriorating seasonal refugium. Front Ecol Environ. 2013; 11:260-267.
46. Theodoropoulos G, Kapel CMO, Webster P, Saravanos L, Zaki J, Koutsotolis K. Infectivity, predilection sites, and freeze tolerance of Trichinella spp. In experimentally infected sheep. Parasitol Res. 2000; 86:401–405.
47. Malakauskas A, Kapel CM., Webster P. Infectivity, persistence and serological response of nine trichinella genotypes in rats. Parasite. 2001; 8(2 Suppl):S216-22.
48. Pozio E. The broad spectrum of Trichinella hosts: From cold- to warm-blooded animals. Vet Parasitol. 2005; 132:3–11.
49. Gondek M, Knysz P, Pomorska-Mól M, Ziomek M, Bień-Kalinowska J. Acute phase protein pattern and antibody response in pigs experimentally infected with a moderate dose of Trichinella spiralis, T. britovi, and T. pseudospiralis. Vet Parasitol. 2020; 288:109277.
50. Pozio, E. Trichinella pseudospiralis an elusive nematode. Vet Parasitol. 2016; 231:97–101.
51. Gottstein B, Pozio E, Nöckler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev. 2009; 22(1):127-145.
52. Pozio E, Zarlenga DS. Recent advances on the taxonomy, systematics and epidemiology of Trichinella. Int J Parasitol. 2005; 35:1191–1204.
2. Owen IL, Reid SA. Survival of Trichinella papuae muscle larvae in a pig carcass maintained under simulated natural conditions in Papua New Guinea. J Helminthol. 2007; 81:429–432.
3. Pozio E, Darwin Murrell K. Systematics and Epidemiology of Trichinella. Adv Parasitol. 2006; 63:367–439.
4. Bilska-Zając E, Różycki M, Grądziel-Krukowska K, et al. Diversity of Trichinella species in relation to the host species and geographical location. Vet Parasitol. 2020; 279:109052.
5. Campbell WC. Trichinella and Trichinellosis. Plenum Press, New York, 1983. p. 581.
6. Stewart GL. Pathophysiology of the Muscle Phase, in: Campbell, W.C. (Ed.), Trichinella and Trichinosis. Springer US, Boston, MA. 1983. p. 241–264.
7. Von Köller J, Kapel CMO, Enemark HL, Hindsbo O. Infectivity of Trichinella spp. recovered from decaying mouse and fox muscle tissue. Parasite. 2001; 8(2 Suppl):S209-12.
8. Lacour SA, Heckmann A, Macé P, et al. Freeze-tolerance of Trichinella muscle larvae in experimentally infected wild boars. Vet Parasitol. 2013; 194:175–178.
9. Worley DE, Seesee FM, Espinosa RH, Sterner MC. Survival of sylvatic Trichinella spiralis isolates in frozen tissue and processed meat products. J Am Vet Med Assoc. 1986; 189:1047–1049.
10. Dick TA, Belosevic M. Observations on a Trichinella spiralis Isolate from a Polar Bear. J Parasitol. 1978; 64:1143–1145.
11. Pozio E, la Rosa G, Rossi P, Murrell KD. Biological Characterization of Trichinella Isolates from Various Host Species and Geographical Regions. J Parasitol. 1992; 78:647–653.
12. Malakauskas A, Kapel CMO. Tolerance to Low Temperatures of Domestic and Sylvatic Trichinella Spp. in Rat Muscle Tissue. J Parasitol. 2003; 89:744– 748.
13. Burke R, Masuoka P, Murrell KD. Swine Trichinella infection and geographic information system tools. Emerg Infect Dis. 2008; 14:1109–1111.
14. Murrell KD, Pozio E. Worldwide occurrence and impact of human trichinellosis, 1986-2009. Emerg Infect Dis. 2011, 17:2194-2202.
15. Franssen F, Swart A, vander Giessen J, Havelaar A, Takumi K. Parasite to patient: A quantitative risk model for Trichinella spp. in pork and wild boar meat. Int J Food Microbiol. 2017;241:262-275.
16. Gondek M, Grzelak S, Pyz-Łukasik R, Knysz P, Ziomek M, Bień-Kalinowska J. Insight into Trichinella britovi infection in pigs: Effect of various infectious doses on larvae density and spatial larvae distribution in carcasses and comparison of the detection of Anti-T. britovi IgG of Three Different Commercial ELISA Tests and Immunoblot Assay. Pathogens. 2022; 11(7):735.
17. Dupouy-Camet J. Trichinellosis: A worldwide zoonosis. Vet Parasitol. 2000; 93:191–200.
18. Ribicich M, Gamble HR, Bolpe J, et al. Trichinella infection in wild animals from endemic regions of Argentina. Parasitol Res. 2010; 107:377–380.
19. Fichi G, Stefanelli S, Pagani A, et al. Trichinellosis Outbreak Caused by Meat from a Wild Boar Hunted in an Italian Region Considered to be at Negligible Risk for Trichinella. Zoonoses Public Health. 2015; 62(4):285-291.
20. Kapel CMO, Pozio E, Sacchi L, Prestrud P. Freeze Tolerance, Morphology, and RAPD-PCR Identification of Trichinella nativa in Naturally Infected Arctic Foxes. J Parasitol. 1999; 85: 144-147.
21. Rostami A, Gamble HR, Dupouy-Camet J, Khazan H, Bruschi F. Meat sources of infection for outbreaks of human trichinellosis. Food Microbiol. 2017; 64:65-71.
22. Faber M, Schink S, Mayer-Scholl A, et al. Outbreak of trichinellosis due to wild boar meat and evaluation of the effectiveness of post exposure prophylaxis, Germany, 2013. Clin Infect Dis. 2015; 60(12):e98-e104.
23. Hill DE, Forbes L, Gajadhar AA, Gamble HR. Viability and infectivity of Trichinella spiralis muscle larvae in frozen horse tissue. Vet Parasitol. 2007; 146:102–106.
24. Bessi C, Ercole ME, Fariña FA, et al, Pasqualetti MI. Study of Trichinella patagoniensis in wild boars. Vet Parasitol. 2021; 297:109166.
25. Krivokapich SJ, Gonzalez-Prous CL, Gatti GM, Saldía L. First finding of Trichinella pseudospiralis in the Neotropical region. Vet Parasitol. 2015; 208:268– 271.
26. Gamble HR, Bessonov AS, Cuperlovic K, et al. International Commission on Trichinellosis: Recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Vet Parasitol. 2000; 93:393–408.
27. Anonymous. Servicio Meteorológico Nacional. Observatorio Buenos Aires. 2022. https://www.estadisticaciudad.gob.ar/eyc/?p=27702. Accesed 11 January 2022.
28. Kapel CMO, Gamble HR. Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. Int J Parasitol. 2000; 30:215–221.
29. Riva E, Steffan P, Guzmán M, Fiel C. Persistence of Trichinella spiralis muscle larvae in natural decaying mice. Parasitol Res. 2012; 111:249–255.
30. Stewart GL, Kennedy R., Larsen E. Infectivity of Trichinella pseudospiralis Isolated from Carrion, Source: J Parasitol. 1990; 76(5):750-751.
31. Kapel CMO. Host diversity and biological characteristics of the Trichinella genotypes and their effect on transmission. Vet Parasitol. 2000; 93:263–278.
32. Webster P, Malakauskas A, Kapel CMO. Infectivity of Trichinella papuae for experimentally infected red foxes (Vulpes vulpes). Vet Parasitol. 2002; 105:215–218.
33. Fariña F, Pasqualetti M, Ilgová J, Cardillo N, et al. Evaluation of the infectivity and the persistence of Trichinella patagoniensis in muscle tissue of decomposing guinea pig (Cavia porcellus). Parasitol Res. 2017; 116:371-375.
34. Pozio E. The impact of globalization and climate change on Trichinella spp. epidemiology. Food Waterborne Parasitol. 2022; 27:e00154.
35. Keppel G, Wardell‐Johnson GW. Refugia: keys to climate change management. Glob Chang Biology. 2012; 18(8):2389-2391.
36. Pozio E. Adaptation of Trichinella spp. for survival in cold climates. Food Waterborne Parasitol. 2016; 4:4–12.
37. Pozio E, La Rosa G, Amati M. Factors influencing the resistance of Trichinella muscle larvae to freezing. In: Trichinellosis. Proceedings of the 8th International Conference on Trichinellosis. Ed. Campbell CW, Pozio E, and Bruschi F. Rome: Instituto Superiore di Sanita Press, 1994. p:173–178.
38. Sacchi L, Corona S, Gajadhar AA, Pozio E. Ultrastructural characteristics of nurse cell-larva complex of four species of Trichinella in several hosts. Parasite. 2011; 8(2 Suppl):S54-8.
39. Kapel CMO, Webster P, Malakauskas A, Hurnikova Z, Gamble HR. Freeze tolerance of Trichinella genotypes in muscle tissue of experimentally infected pigs, horses, wild boars, mice, cats, and foxes. In: International Conference Trichinellosis, San Diego, 2004. p. 8-12.
40. Seymour J, Horstmann-Dehn L, Rosa C, Lopez JA. Occurrence and genotypic analysis of Trichinella species in Alaska marine-associated mammals of the Bering and Chukchi seas. Vet Parasitol. 2014; 200(1-2):153-164.
41. Rudneva OV, Аndreyanov ON, Sidor EA. Reprint of: The retention and concentration of glycogen in Trichinella nativа in the winter-spring period. Vet Parsitol. 2021; 297:109547.
42. Dick TA. Infectivity of isolates of Trichinella and the ability of an arctic isolate to survive freezing temperatures in the raccoon, Procyon lotor, under experimental conditions. J Wildl Dis. 1983; 19:333–336.
43. Raines KM, Stewart GL. Carbohydrate reserves and infectivity in Trichinella spiralis isolated from carrion. Parasitology. 1988; 96(Pt 3):533-41.
44. Davidson RK, Handeland K, Kapel CM. High tolerance to repeated cycles of freezing and thawing in different Trichinella nativa isolates. Parasitol Res. 2008; 103:1005-1010
45. Pauli JN, Zuckerberg B, Whiteman JP, Porter W. The subnivium: a deteriorating seasonal refugium. Front Ecol Environ. 2013; 11:260-267.
46. Theodoropoulos G, Kapel CMO, Webster P, Saravanos L, Zaki J, Koutsotolis K. Infectivity, predilection sites, and freeze tolerance of Trichinella spp. In experimentally infected sheep. Parasitol Res. 2000; 86:401–405.
47. Malakauskas A, Kapel CM., Webster P. Infectivity, persistence and serological response of nine trichinella genotypes in rats. Parasite. 2001; 8(2 Suppl):S216-22.
48. Pozio E. The broad spectrum of Trichinella hosts: From cold- to warm-blooded animals. Vet Parasitol. 2005; 132:3–11.
49. Gondek M, Knysz P, Pomorska-Mól M, Ziomek M, Bień-Kalinowska J. Acute phase protein pattern and antibody response in pigs experimentally infected with a moderate dose of Trichinella spiralis, T. britovi, and T. pseudospiralis. Vet Parasitol. 2020; 288:109277.
50. Pozio, E. Trichinella pseudospiralis an elusive nematode. Vet Parasitol. 2016; 231:97–101.
51. Gottstein B, Pozio E, Nöckler K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin Microbiol Rev. 2009; 22(1):127-145.
52. Pozio E, Zarlenga DS. Recent advances on the taxonomy, systematics and epidemiology of Trichinella. Int J Parasitol. 2005; 35:1191–1204.
| Files | ||
| Issue | Vol 19 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v19i4.17166 | |
| Keywords | ||
| Freezing tolerance Infectivity Persistence study Trichinella Wild boars | ||
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How to Cite
1.
Bessi C, Ercole ME, Fariña FA, Montalvo F, Fassa V, Acerbo M, Ribicich MM, Pasqualetti MI. Survival of Trichinella spiralis and T. pseudospiralis in Experimentally Infected Wild Boar Muscle Tissue under Freezing and Environmental Conditions. Iran J Parasitol. 2024;19(4):457-464.
