EDP Sciences logo
Submit your paper
Search
Menu
All issues Volume 29 (2022) Parasite, 29 (2022) 11 Full HTML
Open Access
Research Article
Issue
Parasite
Volume 29, 2022
Article Number 11
Number of page(s) 6
DOI https://doi.org/10.1051/parasite/2022011
Published online 28 February 2022

© G. Khalil et al., published by EDP Sciences, 2022

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Trichinellosis has been described many times in Lebanon, ranging from outbreaks to small series in the 20th century [2, 9, 11, 13–15, 17, 18, 20, 24, 27, 31]. Outbreaks were also reported in other Mediterranean countries, such as Greece, Italy, and Spain, during the past few years [1, 3, 7, 23, 26, 28].

In recent years, wild boar (Sus scrofa) hunting and wild boar meat consumption was the most described source of outbreaks. Bear and walrus meat consumption was also associated with confirmed trichinellosis in North America, Asia, and Europe [19, 25]. Wild boar meat consumption is associated with Trichinella spiralis infection as well as other species (T. britovi, T. pseudospiralis, and T. papuae) [25]. Undercooked meat and meat-derived products, as well as parasite load are among the most common described risk factors. Clinical signs and symptoms are mainly due to an intestinal phase consisting of diarrhea, abdominal pain, nausea and vomiting, and a larval invasive phase mainly causing fever, facial and/or orbital edema, cutaneous allergy, and myalgia [4]. Trichinellosis is a typical febrile helminthiasis.

During the past two decades, we have observed a drastic decrease in trichinellosis in Lebanon for many reasons, such as the prohibition by the state of an old practice of mixed butcheries (pork vs. other livestock). Moreover, pork meat consumption is limited to some areas in Lebanon as a result of confessional disparity, as well as the small number of pork farms due to more rigid health regulations recently imposed by the state. In contrast, the risk of trichinellosis has been increasing of late because wild boar hunting is becoming more popular in Lebanon. This hunting practice mainly takes place near the southern border of Lebanon, a zone that constitutes a true natural reserve sheltering wild boars, and that is yet to be regulated by the state. Other areas of Lebanon are also involved (Metn, Kesrouan, Chouf, and Bekaa valley). The recent financial crisis in Lebanon has caused basic needs shortages [30]. As a consequence, wild boar hunting has become a source of cheap protein-rich food.

The aim of this paper is to report a recent outbreak of trichinellosis due to wild boar meat consumption in Lebanon, in the context of renewed interest in wild boar hunting due to the recent economic crisis, and integrating it with historical epidemiologic data of trichinellosis in this country.

Materials and methods

Cases and definition of cases

Diagnostic criteria for trichinellosis were based on clinical symptoms and biological test results.

A confirmed case of trichinellosis was defined when a patient had consumed infested meat and had clinical signs and symptoms suggestive of trichinellosis, in addition to a positive muscle (deltoid) biopsy [4] or positive serology or seroconversion: considered negative if less than 11 NTU, or less than doubling value after 2 weeks [5].

A probable case of trichinellosis was defined when a patient had consumed infested meat followed by signs and symptoms such as intestinal phase symptoms (diarrhea, abdominal pain), as well as larval migration phase symptoms/signs (fever, myalgia, facial or periorbital edema, urticarial rash, and conjunctival or sub-nail hemorrhage). In addition, biological workup of the patient revealing any of the following biologic abnormalities suggestive of the disease resulted in a probable case: eosinophilia > 500 cells/μL (norm: 0–450 cells/μL), elevated creatinine phosphokinase (CPK, norm: 10–200 IU/L), or elevated lactate dehydrogenase (LDH, norm: 140–280 IU/L).

Complete blood count (CBC), CPK, and LDH testing was performed on all symptomatic individuals, while serological testing was done only for hospitalized patients.

Serum samples were tested using a commercial qualitative enzyme-linked immuno-sorbent assay (ELISA) for the detection of IgG class antibodies against Trichinella spp. (NovaTec Immun-diagnostica GmbH, Germany), according to the manufacturer’s recommendations. The manufacturer claims that the test has a diagnostic sensitivity and specificity of 100% and 94.81%, respectively and the testing kit was additionally validated in the laboratory (based on excretory/secretory Trichinella antigens) [5].

The index case allowed us to track and identify all other concomitant and/or consecutive cases by providing a list of people who consumed the wild boar meat.

Literature review and inquiry with Lebanese wild boar hunters and the head of the Animal Health Laboratory, Lebanese Agricultural Research Institute (LARI)

In order to obtain information about previous trichinellosis outbreaks in Lebanon, general surveillance data were consulted on the official website of the Ministry of Public Health (MOPH). Furthermore, additional research was conducted on PubMed using the keywords “Lebanon” and “Trichinosis” or “Trichinellosis”. There were no restrictions on article time period.

In order to obtain information about the current status of trichinellosis in Lebanon, we interviewed the head of the Animal Health Laboratory at the Lebanese Agricultural Research Institute (LARI) and five private hunters from different regions of the country. LARI is a governmental institute under the supervision of the Ministry of Agriculture, responsible for all animal-derived products on the market. A particular research station located in Fanar, Lebanon (Mount Lebanon) has recently been established for animal health and zoonosis control.

Results

Case report in January 2019

The index case was a hunter hospitalized in January 2019 for low grade fever, eyelid and facial edema, myalgia, and diarrhea, with diffuse pruriginous maculo-papular rash (patient 1). His blood tests revealed hypereosinophilia, elevated CPK and LDH, and positive serology for trichinellosis. An investigation was then undertaken, upon which we discovered that fifteen people were present at a barbecue party and consumed hunted boar meat grilled over a wood fire. His hunting partner (patient 2) was simultaneously hospitalized for urticaria and fever in a different ward at the same hospital. His physician was notified about the high suspicion for trichinellosis in patient 1, and Trichinella serology testing confirmed the diagnosis. Three other probable cases were subsequently identified and treated as outpatients for similar but less intense symptoms (Table 1). They received symptomatic treatment for viral gastroenteritis. They were subjected to an oriented questionnaire and targeted blood tests were also performed that revealed hypereosinophilia and elevated CPK and LDH levels. The 10 remaining individuals were contacted for follow-up and serological testing, but refused to seek medical care since they were totally asymptomatic.

Table 1

Characteristics and symptoms described by patients.

Literature review and data collection in Lebanon

History of trichinellosis outbreaks in Lebanon from data of the MOPH

In Lebanon, trichinellosis is a reportable disease to the MOPH. Surveillance data that go back to 2002 on the MOPH website were checked for positive trichinellosis cases. There were only three reported cases from 01/01/2002 to 27/05/2020: one case in January 2016 in Beirut and our two cases reported in January 2019 (our confirmed cases). The trichinellosis cases reported to the MOPH and the cases from the literature in Lebanon are summarized in Table 2.

Table 2

Trichinellosis outbreaks in Lebanon.

Data collection gathered from Lebanese wild boar hunters and the Head of the Animal Health Laboratory, LARI

There are two subspecies of wild boar in Lebanon. The first, Sus scrofa libycus, also known as the Anatolian boar, is mainly found along the southern border of the country. The second, the Central European boar (Sus scrofa scrofa), was imported in the late 20th century. The initial population of this subspecies, originally imported for leisure and hunting by private individuals, later on mated and became established in the northern regions of Lebanon.

In Lebanon, the state does not currently regulate wild boar hunting. The most recent legislation regarding this issue dates from 05 April 2017, when a law (Law 580/04) was passed to require physical, mental, and reading (or oral) examinations before obtaining a hunting license.

Based on our interview with the Head of Animal Health laboratory, Trichinella larvae detection has been done on pork and wild boar meat cuts. However, no data are available from before 2006. Unlike pork cuts, which are received from the private and public sectors, wild boar meat is tested on demand by private hunters. The samples were mainly received from the Metn and Aaley regions. Paraspinal muscles undergo trichinoscopy and pepsin and HCl digestion [16] for larva detection. An average of four wild boar samples per year are tested at this institute, with no positive tests for Trichinella larvae since 2006.

There is no official hunting season in Lebanon. Even though the regulations are scarce, there is a consensus between hunters. First, female wild boars are only hunted starting November until September of the following year, in order to allow time for the piglets to mature and be independent of their mother. Male wild boars are hunted independently of the season. Second, three hunting techniques are agreed upon and used: long distance sniping with thermal scopes, and short distance hunting with shotguns by baiting them either with food or hunting dogs. Third, hunters must aim for critical body parts (brain, heart, lungs, or spine) knowing that any non-fatal or non-debilitating shot would enrage the boar, leading to possible physical harm to the hunters or damage to the environment.

Discussion

Although trichinellosis is a notifiable disease, the actual prevalence and incidence are unknown because the disease is difficult to identify due to a nonspecific picture or due to the absence of a pathognomonic clinical picture. Moreover, the disease could be self-limited without medical care seeking. Some outbreaks were not even published, such the one that occurred in East Beirut (Achrafieh) during the 1990–1991 war period. The estimated number of infected persons was around 200. At that time, the livestock was imported from Eastern Europe via Cyprus and the meat (beef, sheep, and pork) was delivered by the same butcher. Trichinella larvae were suspected to have been transmitted from one livestock to another by cross-contamination. Cross-contamination occurred because the same knives, cutting boards, and other utensils were used by the butcher to cut meat of different pieces of infected pork and those of sheep and beef meat. In the food traditions of the Lebanese people, eating raw sheep meat is common. Consuming rare sheep or beef meat is also usual. During this outbreak, the group that consumed the meat of pork or wild boar ate it well cooked. Data collected for 40 patients at this time by the corresponding author, for oral presentation, during his internship in the university hospital located in the epidemic area of trichinellosis, revealed that patients eating raw sheep meat were mainly those who subsequently developed the disease, knowing that raw sheep meat should be consumed within 6–8 h after preparation and delivery by the butcher, for a matter of taste. Only seven patients ate pork meat, and three ate rare beef meat.

There is a general misconception among hunters and consumers that freezing the meat kills larval worms. Studies, however, have shown that not all species of Trichinella are sensitive to cold temperatures. In fact, T. spiralis larval worms are neutralized by freezing the pork either 20 days at −15 °C or 3 days at −20 °C [10, 12, 29]. In contrast, other species found in wild boars, such as T. britovi and T. nativa, are able to resist cold temperatures [10, 12, 21, 29]. To kill the encysted larvae, internal meat temperatures must reach 62 °C or more, taking into consideration the variability in heat distribution and cooking techniques [6]. Using wood fire cooking, such as in our case has shown that heat distribution might not be optimal in the core of the meat to kill encysted larvae. In our reported outbreak, the most likely cause was that the meat was not successfully grilled, hence, a part was served rare. As a result, wild boar cuts should be handled with precaution when using wood fire cooking.

Furthermore, international veterinary societies recommend that hunters should refrain from killing ill-looking boars, as well as avoid leaving behind animal remains and waste after discarding unwanted meat, to avoid the spread of Trichinella in the wildlife [8, 22]. On the other hand, meat handlers (butchers and consumers) should follow certain hygiene rules (hand, utensil, and surface washing, with boiling water and diluted sodium hypochlorite solutions) [10, 12, 29].

As of 2020, Lebanon ranked as having the fourth highest inflation rate globally at 85.45%. This rapid hyperinflation has severely affected the purchasing power of the Lebanese people, especially in impoverished communities. As a result, prices of imports, particularly food and livestock have inflated by more than 441% since 2019. The most recent inflation rate stood at 144.1% during the month of October 2021. Meat prices have sky-rocketed and meat is no longer accessible to the lower- to average-income consumer. Consequently, other means of securing sufficient animal protein intake have been contemplated. One of these means is wild boar hunting for several reasons. First, pork meat consumption is not banned at the national level. Second, wild boars are abundant, as previously mentioned, and their hunting is unregulated. This creates a perfect recipe for gun-owning Lebanese who are looking for leisure or to provide food for their families.

In addition, the lack of veterinarian control increases the risk of unfortunate events. This is illustrated by the scarce amount of testing being done at the reference center for animal health control (LARI).

Our study was limited by the lack of further investigations to detect the species of Trichinella that was implicated in this case. It was not performed for financial reasons and futility regarding the management of the patients involved.

However, this is the first paper since the late 19th century that sheds light on trichinellosis outbreaks in Lebanon originating from wild boar meat consumption.

Conclusion

Trichinellosis, a zoonosis typically unrecognized or undeclared, still represents a risk linked to the consumption of meat from wild animals, especially wild boar.

Given the looming risk of witnessing other trichinellosis outbreaks, the general population, and specifically veterinarians, hunters, and butchers, should be targeted by awareness campaigns regarding the disease and the risk of eating undercooked meat. They should also be instructed on how to properly prepare the meat in a risk-free manner. In addition, regulations should be implemented on this practice to avoid other outbreaks.

Acknowledgments

We thank the Lebanese Agricultural Research Institute and Lebanese hunters for their collaboration. No grants were received for this study. The authors report that they have no conflicts of interest.

References

  1. Arévalo Velasco A, Bringas MJ, Rodríguez R, Menor A. 2009. Description of a trichinosis outbreak in the province of Salamanca. Revista Espanola De Quimioterapia, 22, 115–116. [PubMed] [Google Scholar]
  2. Blondheim DS, Klein R, Ben-Dror G, Schick G. 1984. Trichinosis in southern Lebanon. Israel Journal of Medical Sciences, 20, 141–144. [PubMed] [Google Scholar]
  3. Boutsini S, Papatsiros VG, Stougiou D, Marucci G, Liandris E, Athanasiou LV, Papadoudis A, Karagiozopoulos E, Bisias A, Pozio E. 2014. Emerging Trichinella britovi infections in free ranging pigs of Greece. Veterinary Parasitology, 199, 278–282. [CrossRef] [PubMed] [Google Scholar]
  4. Diaz JH, Warren RJ, Oster MJ. 2020. The disease ecology, epidemiology, clinical manifestations, and management of trichinellosis linked to consumption of wild animal Meat. Wilderness & Environmental Medicine, 31, 235–244. [CrossRef] [PubMed] [Google Scholar]
  5. Djurković-Djaković O, Bobić B, Nikolić A, Klun I, Dupouy-Camet J. 2013. Pork as a source of human parasitic infection. Clinical Microbiology and Infection, 19, 586–594. [CrossRef] [PubMed] [Google Scholar]
  6. Food Safety and Inspection Service. 2018. FSIS compliance guideline for the prevention and control of Trichinella and other parasitic hazards in pork products, Guideline ID FSIS-GD-2016-0002. [Google Scholar]
  7. Gallardo MT, Mateos L, Artieda J, Wesslen L, Ruiz C, García MA, Galmés-Truyols A, Martin A, Hernández-Pezzi G, Andersson Y, Gárate T, Christensson D. 2007. Outbreak of trichinellosis in Spain and Sweden due to consumption of wild boar meat contaminated with Trichinella britovi. Euro Surveillance, 12, E070315.1. [PubMed] [Google Scholar]
  8. Gottstein B, Pozio E, Nöckler K. 2009. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical Microbiology Reviews, 22, 127–145. [CrossRef] [PubMed] [Google Scholar]
  9. Haim M, Efrat M, Wilson M, Schantz PM, Cohen D, Shemer J. 1997. An outbreak of Trichinella spiralis infection in southern Lebanon. Epidemiology and Infection, 119, 357–362. [CrossRef] [PubMed] [Google Scholar]
  10. Heaton D, Huang S, Shiau R, Casillas S, Straily A, Kong LK, Ng V, Petru V. 2018. Trichinellosis outbreak linked to consumption of privately raised raw boar meat – California, 2017. Morbidity and Mortality Weekly Report, 67, 247–249. [CrossRef] [PubMed] [Google Scholar]
  11. Kanán S, Saliba Y, Benoist G. 1980. Trichinosis in Lebanon. A survey on the 1978–1979 outbreak of trichinosis in Lebanon. Lebanese Medical Journal, 31, 339–348. [Google Scholar]
  12. Larter NC, Forbes LB, Elkin BT, Allaire DG. 2011. Prevalence of Trichinella spp. in black bears, grizzly bears, and wolves in the Dehcho Region, Northwest Territories, Canada, including the first report of T. nativa in a grizzly bear from Canada. Journal of Wildlife Diseases, 47, 745–749. [CrossRef] [PubMed] [Google Scholar]
  13. Matossian RM, Ibrahim J. 1974. Rats, flies and mosquitos of Lebanon: pests, reservoirs and vectors of disease. Le Journal Médical Libanais. The Lebanese Medical Journal, 27, 375–381. [Google Scholar]
  14. Matossian RM, Rebeiz J, Stephan E. 1974. Outbreak of trichinosis in Lebanon, 1970. A clinical and epidemiological study. Le Journal Médical Libanais. The Lebanese Medical Journal, 27, 267–273. [Google Scholar]
  15. Matossian RM, Rebeiz J, Stephan E. 1975. Serodiagnosis by fluorescent antibody staining of an outbreak of trichinosis in Lebanon. Annals of Tropical Medicine and Parasitology, 69, 387–392. [CrossRef] [PubMed] [Google Scholar]
  16. Mayer-Scholl A, Pozio E, Gayda J, Thaben N, Bahn P, Nöckler K. 2017. Magnetic stirrer method for the detection of Trichinella larvae in muscle samples. Journal of Visualized Experiments: JoVE, 121, e55354. [Google Scholar]
  17. Merab A, Melki L, Brounst G, Sioufi H. 1952. On a recent epidemic of trichinosis in North Lebanon. La Presse Médicale, 60, 1131–1132. [Google Scholar]
  18. Millischer P, Dubarry J. 1942. Remarques à l’occasion d’une épidémie de trichinose sur la clinique, la thérapeutique et l’hygiène de cette affection. Biologie Médicale, 23, 23–48.. [Google Scholar]
  19. Murrell KD, Pozio E. 2011. Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases, 17, 2194–2202. [CrossRef] [PubMed] [Google Scholar]
  20. Olaison L, Ljungström I. 1992. An outbreak of trichinosis in Lebanon. Transactions of the Royal Society of Tropical Medicine and Hygiene, 86, 658–660. [CrossRef] [PubMed] [Google Scholar]
  21. Pozio E, La Rosa G, Rossi P, Fico R. 1989. Survival of Trichinella muscle larvae in frozen wolf tissue in Italy. Journal of Parasitology, 75, 472–473. [CrossRef] [Google Scholar]
  22. Pozio E, Casulli A, Bologov VV, Marucci G, La Rosa G. 2001. Hunting practices increase the prevalence of Trichinella infection in wolves from European Russia. Journal of Parasitology, 87, 1498–1501. [CrossRef] [PubMed] [Google Scholar]
  23. Pozio E, La Rosa G, Gomez Morales MA. 2001. Epidemiology of human and animal trichinellosis in Italy since its discovery in 1887. Parasite, 8, S106–S108. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  24. Rizk E, Berberian D. 1945. La trichinose au Liban. Revue Médicale Française du Moyen Orient, 4, 609. [Google Scholar]
  25. Rostami A, Gamble HR, Dupouy-Camet J, Khazan H, Bruschi F. 2017. Meat sources of infection for outbreaks of human trichinellosis. Food Microbiology, 64, 65–71. [CrossRef] [PubMed] [Google Scholar]
  26. Sotiraki ST, Athanasiou LV, Himonas CA, Kontos VJ, Kyriopoulos I. 2001. Trichinellosis in Greece: a review. Parasite, 8, S83–S85. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  27. Stephan E, Mamo A. 1952. New cases of trichinosis in Lebanon; grave neurologic involvement in one of the cases; value of muscular biopsy; treatment with ACTH. Le Journal Médical Libanais [The Lebanese Medical Journal], 5, 236–248. [Google Scholar]
  28. Turiac IA, Cappelli MG, Olivieri R, Angelillis R, Martinelli D, Prato R, Fortunato F. 2017. Trichinellosis outbreak due to wild boar meat consumption in southern Italy. Parasites & Vectors, 10, 107. [CrossRef] [PubMed] [Google Scholar]
  29. Wilson NO, Hall RL, Montgomery SP, Jones JL. 2002. Trichinellosis surveillance–United States, 2008-2012. Morbidity and Mortality Weekly Report. Washington, D.C: Surveillance Summaries, Vol. 64. p. 1–8. [Google Scholar]
  30. World Bank. 2021. Lebanon economic monitor, in Spring 2021. Washington, DC: World Bank. [Google Scholar]
  31. Wortabet J. 1881. An outbreak of trichinosis (?) from eating the flesh of a wild boar. Lancet, 117, 454–455. [CrossRef] [Google Scholar]

Cite this article as: Khalil G, Marty P, Hage K, Sfeir S, El Hage J, Bou Assi T, Rassam M, Pomares C & Mikhael E. 2022. Could the re-emerging practice of wild boar hunting linked to the recent economic crisis lead to new outbreaks of trichinellosis in Lebanon?. Parasite 29, 6.

All Tables

Table 1

Characteristics and symptoms described by patients.

In the text
Table 2

Trichinellosis outbreaks in Lebanon.

In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.