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 Table of Contents  
REVIEW ARTICLE
Year : 2014  |  Volume : 7  |  Issue : 2  |  Page : 86-92

Travels and tourism are drivers for trichinellosis


Department of Parasitology, Paris Descartes University, Assistance Publique, Hôpitaux de Paris, Paris, France

Date of Submission06-Jun-2014
Date of Acceptance01-Jul-2014
Date of Web Publication19-Jan-2015

Correspondence Address:
Jean Dupouy-Camet
Department of Parasitology, Paris Descartes University, Assistance Publique, Hôpitaux de Paris, 27 rue du Faubourg Saint Jacques, 75014 Paris
France
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1687-7942.149555

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  Abstract 

Background
Acquiring trichinellosis while traveling abroad is not a new phenomenon and imported cases are regularly reported worldwide. Cases contracted abroad and reported by the French National Reference Centre for Trichinella (NRCT) are analyzed here.
Results
Since 1998, 28 imported cases, representing 37% of all cases, were reported to the NRCT, with a mean annual incidence of two cases. Between 1975 and 1998, 40 imported cases represented only 1.5% of all identified cases, but with a comparable mean annual incidence of 1.6 cases. The incidence of imported cases could even have decreased since 1998 as the number of international travelers increased during that period. Since 1998, most cases were acquired in Canada from bear meat (hunters). Some cases were acquired in West Africa from warthog meat, in Laos from pork, and one case, in Algeria, was because of the consumption of jackal meat.
Discussion
These imported cases are most likely to occur in countries where the habit of eating raw meat is common and may show a high transmission in some regions where the disease is or had become unknown (e.g. Senegal, Laos, etc.). Backpackers, adventure travelers, or hunters will certainly be at a higher risk and should be informed about the risks of eating raw meat (pork, game, or reptile meat) and should be discouraged from illegally importing potentially infected meat that could introduce the parasite in Trichinella-free areas.
Conclusion
Travelers can be good indicators of the emergence of the parasitosis in a given country. Imported cases are good indicators of the epidemiology of the disease in countries where the original infection occurred.

Keywords: epidemiology, travel, Trichinella


How to cite this article:
Dupouy-Camet J. Travels and tourism are drivers for trichinellosis. Parasitol United J 2014;7:86-92

How to cite this URL:
Dupouy-Camet J. Travels and tourism are drivers for trichinellosis. Parasitol United J [serial online] 2014 [cited 2017 Jun 26];7:86-92. Available from: http://www.new.puj.eg.net/text.asp?2014/7/2/86/149555


  Introduction Top


Trichinellosis is a worlwide zoonosis caused by parasitic nematodes of the genus Trichinella. It can be a serious disease, particularly for elderly individuals, in whom severe complications such as myocarditis or encephalitis can lead to death. Recently, several publications reported cases acquired during travel mainly for touristic reasons (holidays or hunting tours) or after consumption of meat imported from countries where trichinellosis is endemic. The French National Reference Center for Trichinella (NRCT) was created in 2001 and one of its objectives was to analyze all cases of trichinellosis reported in France. Interestingly, the analysis of these reports showed that the infection was quite often observed in travelers or in participants of hunting tours. Some of these reports will be discussed below.


  Trichinella , a multispecies genus with a worldwide distribution Top


Trichinella spp. are widespread in wildlife on all continents (except probably Antarctica) and in domestic pigs of many countries [1] . Infections occur in populations used to eating raw or undercooked meat and meat products of different animal origins (e.g. pork, horse, game). Nowadays, nine species and three genotypes are recognized in the genus Trichinella, namely, Trichinella spiralis, Trichinella nativa, and its related genotype Trichinella T6, Trichinella britovi, and its related genotype Trichinella T8, Trichinella pseudospiralis, Trichinella murrelli, and its related genotype Trichinella T9, Trichinella nelsoni, Trichinella papuae, Trichinella zimbabwensis, and Trichinella patagoniensis ([Table 1]). The parasites are perpetuated in lifecycles by carnivorous and omnivorous animals, representing the most important reservoir. All species can develop in mammals, but T. pseudospiralis can also develop in birds, and T. papuae and T. zimbabwensis also occur in some reptile species. A zoonotic parasite found in mammals, birds, and reptiles is quite unique in medical parasitology. No morphological differences exist between species and genotypes, and they are most reliably distinguished by biochemical or molecular analyses.
Table 1 Trichinella spp. and genotypes and human infections

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  Trichinellosis can be a severe disease in humans Top


Contamination occurs after consumption of raw meat containing coiled larvae of 0.5 mm long. The parasitic cycle can be divided into two phases: an intestinal (or enteral) phase and a systemic and muscular phase, which can coexist for a period lasting from a few days to several weeks. After the gastric digestion of the infected meat, the larvae are released into the stomach, take on a snake-like appearance, penetrate the mucosa of the small intestine, and mature into adult worms. After mating in the intestine, adult females shed 100-μm long newborn larvae into the blood and lymphatic vessels. Then, these larvae migrate in the general circulation to find their definitive niche: the musculoskeletal fiber. The circulating larvae induce in their host a parasitic vasculitis. After penetrating the muscular fiber, the larvae take control of it and for most Trichinella spp., induce the constitution of a collagen capsule. The larvae will stay alive in the modified muscle cell (called 'nurse cell') for months or years. Mature females release newborn larvae for 3-4 weeks as confirmed by the observation of a Trichinella spp. female containing embryos on a duodenal section of an individual infected 3-4 weeks earlier [2] . The females then die or are expelled by smooth muscle hyper contractility elicited by the immune response. The clinical signs are directly related to the parasitic cycle [1] . They consist of diarrhea and abdominal pain during the intestinal phase lasting for 3-7 days, facial edema, fever, cardiac and neurological complications during the dissemination phase, and muscular pain when larvae penetrate and develop into the muscle cell [2] . Cutaneous rash and subconjunctival hemorrhages may occur. This phase will last for 1 week, but muscular pain will persist for several weeks. Severe, life-threatening complications (such as encephalitis and myocarditis, which are often simultaneously present) may occur during the invasive phase and lead to death. The diagnosis is suspected if grouped cases of patients with fever, facial edema, and muscular pain are observed. High eosinophil counts associated with high levels of muscular enzymes (CPK, aldolase) are highly suggestive of the diagnosis. At disease onset, antibody detection (ELISA, indirect fluorescence) can be negative and should be repeated after several days. Specific antibodies can be detected earlier by western blot analysis. Antibodies will be detectable in the serum months or years after acute disease. The sooner specific treatment is introduced, the fewer cardiovascular and neurological complications occur. Drug treatment is based on albendazole (15 mg twice daily during a fatty meal) for 10-15 days, associated, in serious forms, with prednisolone to alleviate symptoms and prevent complications [2] .


  Trichinellosis has a global incidence Top


Trichinellosis certainly remains an important zoonotic disease on a global basis. In an extensive review of published cases, Murrell and Pozio [3] analyzed outbreak report data for 1986-2009. Searches of six international databases yielded 494 reports. After applying strict criteria for relevance and reliability, they selected 261 reports for data extraction. From 1986 through 2009, 65 818 cases and 42 deaths were reported from 41 countries. The WHO European Region accounted for 87% of these cases and 50% of those occurred in Romania, mainly during 1990-1999. The incidence in the region ranged from 1.1 to 8.5 cases/100 000 populations. Trichinellosis affected primarily adults (median age 33.1 years) and about equally affected men (51%) and women. Pork was the major source of infection; wild game sources were also reported frequently. Bruschi and Dupouy-Camet [4] analyzed all reports made on the ProMED-mail (www.promedmail.org) organization from 1998 to 2013 and identified 58 outbreaks involving more than 2400 cases and 15 deaths from 23 countries. Pork was the source of the infection in 64% of cases, horsemeat of 16%, wild boars of 12%, and wild carnivores of 8%. However, these reports are not fully analyzed; early warnings, reporting unusual vectors, imported cases or severe and lethal outbreaks, and data from several countries (such as China) are not reported through this media. The usual sources of infection for humans are detailed in [Table 1], the most frequent source being pork from domestic or wild pigs harboring T. spiralis, T. britovi, and sometimes T. pseudospiralis. Meats from wild carnivores (bears, dogs, badgers, etc.) are a source of small outbreaks among hunters and their associated social groups (friends, relatives, etc.), and horsemeat has been implicated in a number of larger outbreaks in France and Italy, where this meat is consumed raw or rare. Indeed, in France, since 1975, 68 cases were contracted abroad, whereas 2497 cases were contracted in the country and were mostly related to eight outbreaks because of horsemeat consumption (each involving from seven to 642 cases). Nevertheless, implementation of radical preventive measures in 1998 (education of technicians, quality control, and lab accreditation) has prevented the occurrence of new horsemeat-related outbreaks [5]


  Examples of imported cases that occurred recently in France Top


Cases in tourists after a travel to Laos

In March 2005, two patients were hospitalized in the Rouen University hospital a few days after returning from a tour of 'ethnic minorities of Northern Laos' (communicated by Loic Favennec). These two patients presented with high fever, myalgia, and facial edema, and were part of a 10-person group including a Lao guide and a local driver. Antibody testing performed on the blood of the eight tourists allowed the identification of a third case. The infection source was not clearly identified, but free-ranging pigs are a common situation in Laos ([Figure 1]) and the tourists ate local specialties such as 'lap mou' (a traditional preparation made of spiced and chopped raw pork). A few weeks later, a large outbreak of at least 650 estimated patients was reported in Udomxay (northern Laos), a place in which the tourists stayed [6] . In this region, larvae of T. spiralis were found and genotyped in one of 11 local pigs (not involved in this outbreak).
Figure 1 Laos (and Northern Thailand) are hot spots of trichinellosis as local people are fond of raw pork preparation such as 'lap mou' or 'som mou' [6]. Free-ranging pigs are very frequent in the villages of these regions. Picture: Jean Dupouy-Camet, reserved rights.

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Cases after a hunting tour in George River region (Northern Quebec) [7]

At the end of September 2005, the NRCT was informed that five patients had presented with fever, myalgia, and eosinophilia and had been admitted to Orleans hospital. Two weeks previously, the five patients had shared a meal of bear meat brought back by one of them from a hunting trip in Canada. This patient was one of a group of 10 hunters who had all eaten bear meat in Canada; some of them had subsequently brought more of this meat back to France ([Figure 2]). The meat was obtained from an American black bear shot on 26 August 2005 near the George River (northern Quebec). The meat was eaten by the hunters during several meals between 28 and 30 August as undercooked or even eaten completely as raw steaks. Exposed individuals were identified from a list obtained from the leader of the hunt and by interviewing each of those who had eaten meat brought back to France. The NRCT contacted each of these individuals to advise them on a systematic medical check-up and recommend appropriate preventive treatment. The exposed population comprised 25 individuals. By 4 October, 17 cases of trichinellosis had been identified: eight in the group of hunters and nine in the group of exposed consumers in France. Two muscle biopsies (one from a hunter and one from an individual who had shared a meal in France) showed a parasitic burden of at least two larvae per gram of muscle and DNA typing identified T. nativa. Although bear meat is a frequent source of Trichinella spp. outbreaks in northern Canada [9] , Canadian health authorities did not identify other contemporaneous outbreaks in the region.
Figure 2 The bear, responsible for the outbreak, was an American black bear (Ursus americanus) aged about 4– 5 years and weighing ∼150 kg. In western Canada, Trichinella spp. larvae were found in 65.9% of polar bears (Ursus maritimus), in 29.4% of grizzly bears (Ursus arctos), and in 7.3% of black bears, but the highest larval burden was observed in black bears, explaining why most Canadian outbreaks are related to this species [8]. Picture: Thierry Ancelle, reserved rights.

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Cases in tourists after a stay in a hotel in Northern Senegal [10]

In early May 2009, the NRCT was informed about three patients returning from Senegal who had high titers of specific anti-Trichinella antibodies. These patients were confirmed cases according to the case definition criteria for trichinellosis defined elsewhere [2] . The three patients, living in different regions of France, became infected after consuming smoked warthog (Phacochoerus africanus) ham around mid-February 2009, in the same hotel in Saint Louis (Ndar) in Senegal ([Figure 3]). Trichinellosis was suspected in three additional individuals. Two of the suspected cases were the wife and the husband of two of the confirmed cases; they felt sick and tired, but without typical signs. The third suspected case was a colleague of one confirmed case who presented with suggestive signs (fever and diarrhea). All three stayed in the same hotel and shared meals with the confirmed cases. According to the hotel director, no other cases of trichinellosis were reported among the guests or staff and their families, although they had also consumed warthog ham. He stated that the warthog meat was usually deep-frozen for several weeks before being processed as ham. The suspected warthog ham was not available for parasitological examination. Human trichinellosis was first reported in Senegal in the 1960s, when an outbreak involving nine French expatriates occurred after the consumption of warthog meat coming from the Senegal delta region (Boundoum) [11] . At that time, veterinary studies reported a 4% prevalence of Trichinella spp. infection in 450 Senegalese warthogs [12] . Pozio et al. [13] identified isolates from carnivore mammals of neighboring Guinea as belonging to the species T. britovi, but could not find Trichinella spp. in any of the 10 warthogs examined.
Figure 3 In Senegal, warthog meat has been incriminated in at least two outbreaks: the present one and another reported in the 1960s and involving French expats [11]. In the 1970s, a 4% prevalence of Trichinella infection was reported in Senegalese warthogs [12]. Picture: Denys Piningre, reserved rights.

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Cases in navigators sailing through the North-West Passage [14]

On 5 October 2009, the NRCT was informed about a possible case of trichinellosis in an individual returning from Nunavut, Canada. This asthenic patient had high eosinophil counts and elevated plasma levels for muscle enzymes. Specific antibodies were detected by ELISA and western blot. The patient was part of a group of five marine navigators who had traveled from the Aleutian Islands to Greenland and crossed the North-West Passage in northern Canada. The NRCT identified four more cases among these navigators. Considering the occurrence, onset, and duration of signs and symptoms, the source of infection was attributed to grizzly (Ursus arctos) steaks that were consumed in the Cambridge Bay area (Iqaluktuuttiaq), Victoria Island, Nunavut, Canada, between the 19th and 22nd August 2009. The grizzly bear was shot at Elu Inlet Lodge, at the beginning of August, and transported fresh to Cambridge Bay, where it was frozen for about a week. All five members of the crew consumed this meat, barbecued or panfried, on several occasions after 19th August. All the remaining meat from the bear was consumed locally in Cambridge Bay, but it was well cooked and no suspected cases were reported. For some time, the boat of the five travelers sailed together with another one with four individuals on board and members of both crews ate at the same places. The second boat was on its way to Halifax, Canada, in mid-October and according to the board blog, one of the crew members was affected by a persistent flu. The crew was contacted by email and alerted on the possibility of trichinellosis infection and on specific treatment measures that might be necessary. The diagnosis was confirmed in these sailors after they arrived at their final port. An extensive survey conducted recently on wildlife across northern Canada, Gajadhar, and Forbes [8] found that 29.4% of grizzly bears examined harbored T. nativa (or T6) larvae [8] . Approximately 18 cases of human trichinellosis are reported each year in Canada and are generally attributed to the consumption of infected meat from wildlife [15] .

Travel and trichinellosis

Acquiring trichinellosis while traveling abroad is not a new phenomenon, as McAuley et al. [16] , reviewing 'Trichinella spp. infection in travelers' in the USA from 1975 to 1989, reported 26 cases after pork consumption after stays in Central America. In France, between 1975 and 1998, 40 imported cases represented only 1.5% of all identified cases, with a mean annual incidence of 1.6 cases (unpublished data). Since 1998, 28 imported cases represented 37% of all cases reported to the NRCT, but with a comparable mean annual incidence of two cases ([Figure 4]). The incidence of imported cases could have even decreased since 1998 as the number of international travelers increased during that period. Most imported cases diagnosed in France in the period 75-98 were acquired in Egypt from pork [17] , in Algeria from wild boar meat [18] , or even from arctic bear meat [19] ; since 1998, most cases were acquired in Canada from bear meat [7],[14] , in West Africa from warthog meat [10] , and in Laos from pork ([Figure 5]). One case acquired in Algeria was because of the consumption of jackal meat [20] and other single cases were acquired from pork (Croatia, Spain) or warthog (Cameroon). Curiously, although the native population of bears is nearly extinct, bear meat has been the main source for human trichinellosis in France during the past 10 years.
Figure 4 Imported and autochtonous cases of trichinellosis at the French NRC on Trichinella. In 2005, nine of the autochtonous cases were because of the consumption of illegally imported black bear meat by two of the eight hunters contaminated in Quebec [7]. In 2009, four cases, not included in the figure, because of consumption of the same bear [14] were identifi ed in Belgium, Germany, Canada, and Honk Kong.

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Figure 5 Sources of the 25 imported cases of trichinellosis reported to the French NRC on Trichinella (2000– 2011).

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Travel is a driver for trichinellosis, but importation of pork delicacies from countries where the disease is prevalent is also a frequent cause of the disease. During the past 15 years, occasional cases or small outbreaks were imported in European countries from East European countries (Poland, Romania, former Yugoslavia), where trichinellosis re-emerged after the social upheavals of the 1990s [21] . For example, an outbreak of nine cases was reported in 2001 among Yugoslavian immigrants in west London and in the county of Hertfordshire after eating infected salami made from pork, a regional delicacy from Sombor in northern Serbia, that was brought into the UK in November 1999 and given to four households [22] . During the 2007 summer, an outbreak of trichinellosis affecting over 200 individuals was described in Poland, and related cases were observed in Germany [23] , Ireland [24] , and Denmark [25] . In mid-January 2007, three family members from Bavaria came down with typical symptoms for trichinellosis after visiting relatives in Romania (Arad district) during the Christmas holidays [26] . Again in 2007, 21 individuals became ill with trichinellosis in both Spain and Sweden. This was traced to the consumption of homemade wild boar sausage from an original source in Spain [27] . In January 2008, a Romanian family living in Italy (two adults and one child) and a friend of the family were admitted in hospitals in Verona (Italy). During a visit to relatives and friends in Romania, they had all consumed ham produced from a pig slaughtered without any veterinary control. Two more individuals in Romania developed trichinellosis from the same source [28] . In Asia, imported cases because of T. papuae were observed in Japan and Thailand after the consumption of soft-shelled turtle meat in Korea and in Malaysia [29],[30] . An outbreak was also observed in tourists from Singapore after traveling to a seaside resort in a neighboring island [31] .

The steady increase of international travel explains the acquisition of the disease as exemplified above by individual or small groups of travelers or hunters. These imported cases are most likely to occur in developed countries and may indicate a high transmission in some countries where the disease is or had become unknown (e.g. Senegal, Laos, etc.). In addition, consumers from countries where the habit of eating raw meat is common will certainly be at a higher risk and particularly if they are backpackers, adventure travelers, or hunters of exotic animals. Therefore, they should be informed about the risks of eating raw meat (pork and pork products, game, or reptile meat) and should be discouraged from illegally importing potentially infected meat that could introduce the parasite in Trichinella-free areas. Finally, health professionals should be aware of the possible occurrence of the disease after the consumption of unusual meats different from the usual pork. Curiously, no imported cases have been reported to the French NRCT since 2009. This could well be related to an increased awareness of the disease among travelers. The 'Lonely Planet' guidebooks recommend for some destination to 'avoid eating raw food, especially fish, pork and vegetables,' but this recommendation is not specified for Laos or Canada (where bear meat should be mentioned). In conclusion, travelers, particularly from countries where raw meat is consumed, could be indicators of the emergence of trichinellosis in a given country.


  Acknowledgements Top


All this work would have been impossible without the financial help of the National Reference Center on Trichinellosis ( http://cnrdestrichinella.monsite-orange.fr/ ) headed by Jean Dupouy-Camet and Thierry Ancelle (2002-2011). Many thanks to Gordon Langsley for language revision and to Philippine Sabarros for critical revision of the manuscript.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Pozio E. Taxonomy, biology and epidemiology of Trichinella parasites In: Dupouy-Camet J, Murrell D eds. FAO/WHO/OIE Guidelines for the Surveillance, Management, Prevention and Control of Trichinellosis. Paris: World Organisation for Animal Health (OIE) 2007; 1-35. Available at: ftp://ftp.fao.org/docrep/fao/011/a0227e/a0227e.pdf.  Back to cited text no. 1
    
2.
Dupouy-Camet J, Bruschi F Management and diagnosis of human trichinellosis In: Dupouy-Camet J, Murrell D eds. FAO/WHO/OIE Guidelines for the Surveillance, Management, Prevention and Control of Trichinellosis. Paris: World Organisation for Animal Health (OIE) 2007; 37-68 Available at: ftp://ftp.fao.org/docrep/fao/011/a0227e/a0227e.pdf.  Back to cited text no. 2
    
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Murrell KD, Pozio E. Worldwide occurrence and impact of human trichinellosis, 1986-2009. Emerg Infect Dis 2011; 17:2194-2202.  Back to cited text no. 3
    
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Schellenberg RS, Tan BJ, Irvine JD, et al. An outbreak of trichinellosis due to consumption of bear meat infected with Trichinella nativa, in 2 northern Saskatchewan communities. J Infect Dis 2003; 188:835-843.  Back to cited text no. 9
    
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Dupouy-Camet J, Lecam S, Talabani H, Ancelle T. Trichinellosis acquired in Senegal from warthog ham, March 2009. Euro Surveill 2009; 14. pii: 19220.  Back to cited text no. 10
    
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Pozio E, Pagani P, Marucci G, et al. Trichinella britovi etiological agent of sylvatic trichinellosis in the Republic of Guinea (West Africa) and a re-evaluation of geographical distribution for encapsulated species in Africa. Int J Parasitol 2005; 35:955-960.  Back to cited text no. 13
    
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Houzé S, Ancelle T, Matra R, et al. Trichinellosis acquired in Nunavut, Canada in September 2009: meat from grizzly bear suspected. Euro Surveill 2009; 14. pii: 19383.   Back to cited text no. 14
    
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