Review

Trichinellosis, a Romanian Never-Ending Story.An Overview of Traditions, Culinary Customs,

and Public Health Conditions

Raul Neghina

Abstract

Over the years, pork was the most frequent source of human trichinellosis in Romania. Cases generally occurredin foci, family, and group clusters and were rarely aggregated in extensive outbreaks. A study regarding thesocial consequences of trichinellosis in humans concluded that 84.8% of the patients diagnosed with the con-dition required an average of 53 days of sick leave. Cardiac complications are the most frequent causes ofsignificant health status impairment. ‘‘Pig’s alms,’’ a specific custom representing the thanksgiving meal offeredto relatives, friends, or neighbors who participated in the slaughtering process may be a very good source ofinfection with Trichinella parasites, leading to unfortunate consequences, especially when animals are not vet-erinary tested. Beside pork, other concerns for acquiring the disease are represented by game meat and horse-meat, the latter was introduced in public consumption in 2001. Although in Romania Trichinella sp. infection wasdocumented for the first time in horses in 1993, no consequent human cases were detected at that time. Numeroustrichinellosis outbreaks involve individuals from the gipsy community, most of whom are very poor, illiterate,unemployed, and live in unsanitary conditions raising backyard pigs without any compliance with hygienic rules.Measures aimed at limiting the spread of the infection in humans and animals should be widely available to beknown, understood, and adequately applied by the great mass of pig breeders, hunters, and consumers.

Background: The Story Begins with a Dream

The literary story of Trichinella parasites began hallu-cinatory in 1866 when Raskolnikov, Dostoevsky’s char-

acter from his well-known novel Crime and Punishment, ‘‘haddreamed that the whole world was doomed to fall victimto some terrible, as yet unknown and unseen pestilencespreading to Europe from the depths of Asia. Everyone was toperish, except for certain, very few, chosen ones. Some newtrichinae had appeared, microscopic creatures that lodgedthemselves in men’s bodies. But these creatures were spirits,endowed with reason and will. Those who received them intothemselves immediately became possessed and mad’’ (Dos-toevsky, 1993). In Romania, a southeastern European countrywith a population of about 22 million inhabitants, the storybegan in October 4, 1868 when the parasite was first found inhuman remains during a necroscopic examination (Lupascuet al., 1970; Cristea, 1998; Olteanu et al., 1999).

Since then, trichinellosis has been detected in all Romaniancounties. The first significant outbreak was described in 1957in the town of Orsova involving 124 individuals of whommore than a half consumed raw=smoked pork products

originated from unverified meat. Between 1963 and 1968, anumber of 72 human foci occurred in 25 counties including478 clinical cases of whom 8% were hospitalized and 0.7%died (Lupascu et al., 1970; Ionescu, 1995; Cristea, 1998; Ciro-neanu and Ispas, 2002). Following the dramatic outbreak thatinvolved 757 clinical cases in Arad County in 1973, the Ro-manian authorities declared trichinelloscopic examinationmandatory for all sacrificed pigs (Cironeanu and Ispas, 2002).

Trichinellosis incidence followed an ascending pattern overthe years. Between 1979 and 2007, the mean annual incidenceof human trichinellosis was 4.5 cases per 100,000 inhabitants.The figures were significantly increased (6.2 cases per 100,000inhabitants) during the postcommunist period (1990–2007)when compared with the late communist period (1979–1989)(1.8 cases per 100,000 inhabitants) (Neghina et al., 2009a).

‘‘Pig’s Alms’’: Between Old-Fashioned Ritesand Unsafe Habits

Over the years, pork was the most frequent source of in-fection in humans (95%), and cases generally occurred in foci,family, and group clusters and, more rarely, aggregated in

Department of Parasitology, Victor Babes University of Medicine and Pharmacy, Timisoara, Romania.

FOODBORNE PATHOGENS AND DISEASEVolume 7, Number 9, 2010ª Mary Ann Liebert, Inc.DOI: 10.1089=fpd.2010.0546

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extensive outbreaks. Family and group episodes were usuallyassociated with the consumption of raw, salted, smoked porkand different culinary products in cafeteria, in army, atweddings, or during the traditional ‘‘pig’s alms’’ (Cironeanuand Ispas, 2002).

In private households from the countryside, massive pigslaughtering usually begins in October, reaches a peak inDecember—the month of winter celebrations—and continuesin January and February. A Romanian specific custom isthe ‘‘pig’s alms,’’ representing the thanksgiving meal offeredto relatives, friends, or neighbors who participated in theslaughtering process. According to ancient traditions, eachfamily should slaughter a pig with the occasion of winterholidays. Actually the event welcomes the Holy Christmas.This ritual transmitted from generation to generation origi-nates from the archaic communities for whom pork re-presented the main food source during the cold seasons.People from ancestral communities celebrated the event ofpig’s sacrifice by sharing a small part of the animal’s meat as asign of trust, understanding, and cohabitation. At the end ofthe slaughtering process, those who are actively involveddrink a special boiled plum brandy or wine and have a mealwhile standing. They taste the fresh pork and finally make thewish to have a bigger pig next year. The traditional meal isprepared by frying different types of meat (muscles, liver,bacon, ribs, and jaw) in fats. These pieces are intended torepresent all the parts of the sacrificed animal. The meal isserved only when the entire process of preparing the productsis finished, including cleaning and total removal of theslaughtering remains. Nowadays, only the practical part ofthis custom has been maintained (CrestinOrtodox.Ro, 2010).The products prepared with this occasion include sausagesthat are later consumed raw, fried, or smoked, traditionalsalami, blood pudding salami, mosaic salami, bacon, ham(later consumed as salted fillet), greaves, and pig trotter’s jelly(Fig. 1, Supplemental Figs. S1–S7, available online at www.liebertonline.com). All these tasty culinary products are ex-tensively consumed during the winter season and particularly

during the Christmas and New Year celebrations (Neghinaet al., 2009a, 2009b).

The practice of the above described custom may be a verygood source of infection with Trichinella sp. parasites, leadingto unfortunate consequences. This happens especially whenpigs are not veterinary tested after slaughtering (Neghinaet al., 2009a, 2009b). On such occasions, besides consumptionof pork and its products by humans, domestic animals mayalso acquire the infection. Meat scraps are frequently thrownto cats and dogs from the household and, at the same time,may be ingested by rats, mice, or other pigs, thus contributingto the spread of the disease (Cironeanu and Ispas, 2002).

The Trojan Horse

In the recent years, cases of exported trichinellosis havebeen described when homemade Romanian pork productswere offered as gifts to relatives or friends in different Euro-pean countries and caused infections in those countries. Or,in other cases, products were consumed in Romania duringa visit, and the diagnosis was established later in the visitors’home country. Thus, an outbreak that involved seven patientsfrom Denmark who consumed a smoked sausage originatedfrom Romania was reported in 2004 (Hansen et al., 2004). InJanuary 2007, in Arad, a hyperendemic Romanian county(Neghina et al., 2009b), three family members from Germanyacquired trichinellosis after consumption of minced meat,cured sausage, and bacon proceeded from meat that was notproperly heated. Moreover, they continued to consume in-fected sausages and bacon after their return to Germany(Nockler et al., 2007). The most recent example ( January 2008)is the case of a Romanian family and their friend from Verona,Italy, who contracted the infection during a visit in Romaniato relatives, where they had consumed ham from a pigslaughtered without veterinary inspection (Angheben et al.,2008).

The Delicious Taste of Game Meatand Its Dramatic Outcomes

Beside pork, another concern for acquiring trichinellosis isrepresented by game meat, especially wild boar and bearmeat. In 1993, verified pork was mixed with unverified andinfected wild boar meat, leading to an extensive outbreakwith dramatic consequences. The practice of mixing differentassortments of meat (especially pork and wild boar meat) isvery frequent and led to many outbreaks (Cironeanu andIspas, 2002). A more recent example is the outbreak reportedin January 2007 in the city of Timisoara, when 21 individualsconsumed sausages prepared from wild boar meat mixedwith pork. Five of them acquired the infection and presentedbenign and moderately severe clinical courses of disease.The disease began with flu-like symptoms, and therefore,patients received only antibiotics and symptomatic drugs forthe first 5 days. Afterward, digestive symptoms occurred andthey were addressed to hospital with the assumed diagnosisof foodborne toxi-infection. Following medical evaluationof the patients, including a detailed and carefully takenanamnesis, trichinellosis came into physicians’ attention. Ve-terinary authorities were immediately alerted and they tookfood samples consisting of 1 kg of mixed sausages and 180 g offrozen wild boar meat. The trichinelloscopic examination waspositive for Trichinella sp., although the former examination,

FIG. 1. A traditional Romanian meal including the fol-lowing pork products: 1, mosaic salami; 2, Oltenian sau-sages; 3, raw-smoked sausages; 4, greaves; 5, pig trotter’sjelly; 6, salted ham (fillet); 7, traditional salami; 8, bloodpudding salami.

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undertaken in a veterinary laboratory from the market, wasnegative. The female-to-male sex ratio was 1.5:1 and all thepatients originated from urban regions. Professionally, threeof them were retired and two were medical assistants. Eosi-nophil counts ranged between 24.3% and 74.2% (mean,39.02%). Specific therapy with albendazole was administeredin all cases. The hospitalization period ranged between 10and 15 days and the outcome was favorable in all patients. Theother 16 persons who consumed infected meat did not presentclinical symptoms. Nevertheless, they were consulted in spe-cialized ambulatory units and received prophylactic antipara-sitic chemotherapy (Neghina, unpublished data). Further, avery recent examination of 160 wild boars that were killed in anextensive hunting for pleasure campaign organized by a Ro-manian business man in January 2010 indicated that five ani-mals (3.1%) were infected with Trichinella sp. (Gandul, 2010).

They Shoot Horses, Don’t They?

Another potential risk of infections in humans is re-presented by nutria and horse meat. The latter was introducedin public consumption in 2001 when the first butcher’s shopopened in the city of Bacau. Nevertheless, no human infec-tions have been detected following the consumption of theaforementioned types of meat (Cironeanu and Ispas, 2002).Trichinellosis episodes due to consumption of raw horsemeatwere brought into attention, especially in France and Italy(Pozio, 2001; Pozio et al., 2001; Cironeanu and Ispas, 2002;Blaga et al., 2009). Horses began to be incriminated more andmore frequently as Trichinella sp. bearers. Surprisingly, for thefirst time in Romania, 4 of 11 examined horses were found tobe infected with Trichinella sp. in 1993 (Olteanu et al., 1999;Cironeanu and Ispas, 2002). From then on, trichinelloscopicexamination has become mandatory even in these animals.Because horsemeat is increasingly requested, especially byconsumers from western Europe, numerous horse farms andbutchers’ shops appeared and continued to open in Romaniamainly for export purposes (Cironeanu and Ispas, 2002).However, recent investigations showed very low prevalenceof infection in Romanian horses (Olteanu et al., 1999; Blagaet al., 2009).

Exotic Gypsies, Bad Habits, and Poverty

Numerous trichinellosis outbreaks involve individualsfrom the gipsy community. These people represent an ethnicminority with roots in medieval India who are spread now-adays in European countries such as Romania, Bulgaria,Serbia, Macedonia, Hungary, Czech Republic, Slovakia,Spain, and Greece. In Romania, they account for 2.5% of thepopulation and are the second largest ethnic minority. Amajor part of this community includes individuals who arevery poor (about 80% are living on less than $4.30 per day),illiterate, and unemployed and who live in unsanitary con-ditions (Fig. 2) (Ringold et al., 2003). To assure their daily food,they raise backyard pigs without any compliance with hy-gienic rules (Fig. 3). Sometimes they even consume corpsesof pigs that died in uncertain circumstances. It is widelyknown in rural communities that gypsies are the first whofind out and come to take the dead body of any diseasedanimal whose meat is edible. Therefore, it is unsurprising thatthese people are usually involved in trichinellosis outbreaks.In some situations they might behave very violently, as it

happened in 1996 when a gipsy woman died of trichinellosisin a hospital from Bucharest and more than 20 gypsies rushedinto hospital, took her dead body, devastated the building,and injured the physicians (Olteanu et al., 1999).

The Socialist Legacy Is Falling Apart

Romania was the country with the highest density of ani-mals in huge industrial holdings for many decades of socialisteconomy. Such structures conferred certain favorable con-ditions for parasitic zoonoses. Nevertheless, the number ofhuman cases was kept under control at that time by the rig-orous policies of animal disease control. In the early post-communist period (1990s), the huge abattoirs closed downand young swine, most of them infected with Trichinella sp.,were transferred to small farms and private holdings wherethe veterinary control was less strict than the exhaustive ex-amination performed in the huge industrial holdings. Thus,the incidence of human and animal trichinellosis increasedin those years as a result of Trichinella imminent invasion inthe aforementioned holdings (Olteanu et al., 1999; Cuperlovic

FIG. 2. A gipsy community living in very poor and un-healthy conditions (February 2010). Reproduced courtesy ofAdevarul Holding, Bucharest, Romania.

FIG. 3. Backyard pig raised in unsanitary conditions. Atypical scene of the poor communities living in the Romaniancountryside.

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et al., 2005). In 1993 the incidence of trichinellosis in humans(15.9 cases per 100,000 inhabitants per year) was the highestever registered in Romania (Neghina et al., 2009a).

The Porcine Pathway

Trichinella sp. infections occurred especially in pigs thatlived in farms invaded by infected rats or in those that wanderfreely through urban waste on the outskirts of cities andtowns. In farms with fodder deficiencies, trichinellosis spreadthrough cannibalism (nibbling of the tails or ears) or acci-dental ingestion of corpses (Cironeanu and Ispas, 2002; Cu-perlovic et al., 2005). The sources of infection were alsoconstituted by corpses of dogs, cats, and rats, fortuitouslythrown on free areas, in ditches or garbages that were acces-sible to pigs. Pig’s preference for consuming different kinds ofdead bodies or animal remains is well known. Pregnant andnursing sows require increased quantities of proteins. Con-sequently, massive infections with hundreds and even thou-sands of Trichinella larvae per gram of meat were foundparticularly in sows. Less frequently, the infection has beentransmitted by pigs through consumption of wild animals’bodies (wolves, foxes, martens, wild cats, ferret, badger) thatwere brought in the households by hunters or forest em-ployees or spread by dogs. Another route of infection wasrepresented by the meat removed from the market or confis-cated from the slaughterhouses or farms that had pigs in-fected with Trichinella sp. Instead of being destroyed the meatwas disposed improperly and ingested by other receptiveanimals such as rats, mice, cats, and dogs, thus causing newinfections (Cironeanu and Ispas, 2002).

Romania’s ecological conditions as well natural and socialfactors in which humans were strongly involved have largelycontributed to the occurrence and evolution of numeroustrichinellosis foci (Cironeanu and Ispas, 2002). The maincauses that led to transmission and spread of the infections inpigs were the following: construction of farms for pig breed-ing and fattening in the immediate proximity of the slaugh-terhouses, thus favoring the spread of infection from theslaughterhouses to farms through rats; lack of adequatefencing of pig farms located in open fields; deficiencies in thefeeding of pigs that lead to metabolic disturbances and sub-sequent cannibalism, necrophagia, and coprophagia, fol-lowed by horizontal transmission of the parasites; advancedwear of shelters and lack of normal hygiene conditions;transfer of pigs from one farm to another without rigorouscompliance with veterinary and sanitary measures; trading ofpigs with trichinellosis from large holdings to small privatefarms and households; and lack of crematories and deficienteducation of the population regarding the destruction of an-imal corpses (Cironeanu and Ispas, 2002; Cuperlovic et al.,2005). Stray dogs and cats that consumed food scraps, animalremains from garbage, or infected rats also constituted goodhosts for parasites. At the same time, these animals representeda valuable indicator of the presence of Trichinella sp. because theentire parasitic load acquired through repeated infections wasdeposited in their muscles (Cironeanu and Ispas, 2002).

Economic and Social Implications. What Would BeExpected from Us to Do?

Economic implications may be either direct, by significanteconomic losses due to destruction of massive infected ani-

mals’ carcasses and internal organs, or indirect, by animals’fail in attaining the adequate weight, decreased resistance todifferent diseases, and prohibition of trading meat from farmswith sick animals. A survey of 17 farms with pigs infectedwith Trichinella showed that 183.4 tonnes of carcasses wereconfiscated from slaughterhouses in 1988, and 3011 pig car-casses (155.5 tonnes) were destroyed in 1989 (Enache, 2005).

Regarding the social consequences of trichinellosis inhumans, a study showed that 84.8% of the patients diagnosedwith the condition required an average of 53 days of sick leave(Olteanu et al., 1999; Enache, 2005). Another survey of 123complicated cases of trichinellosis admitted to Victor BabesHospital of Infectious and Tropical Diseases in Bucharest in-dicated that a total of 1962 days of hospitalization (5.3 years)with an average of 15.9 days per person and a maximum of 45days were required. Short-time hospitalizations were generallydue to improvement in the evolution of disease in some pa-tients who subsequently asked for discharge from the hospital.Of these patients, 34.14% benefited by a total of 501 days (1.3years) of sick leave. The remaining patients did not require sickleave because they had one of the following status: housewives,unemployed, retired, or pupils (Enache, 2005). In a study onhuman corpses exhumed 2 months after burial, the necropsyreports revealed that the former diagnosis of myocardialinfarction was wrongly established. The real diagnosis wastrichinellosis (Cristea, 1997; Olteanu et al., 1999). Cardiac com-plications are the most frequent causes of significant healthstatus impairment. As reported previously, between 30% and50% of patients infected with Trichinella sp. had acute myocar-ditis (Olteanu et al., 1999). Accordingly, a recent published casestudy described a 42-year-old woman from Romania affectedby cardiac complications of this severe malady (Tint et al., 2009).

Therefore, no matter how numerous and rationale wouldbe the measures expected to limit the spread of the infectionin humans and animals, they must be first known and un-derstood to be adequately applied by the great mass of pigbreeders, hunters, and consumers. The informative activitiesshould focus on the following aspects: morphology andbiology of Trichinella sp. parasites, routes of infections inhumans and animals, symptomatology of human disease andits multiple consequences, the importance of the veterinaryinspection of the meat, and the major risk incurred by eatingunverified meat and meat products from different animalsas well as the economic loss due to trichinellosis. All the in-formation aforementioned may reach wide audience throughthe following actions: brief and explicit articles publishedperiodically in local and national gazettes; special broadcastsfocused on trichinellosis; documentary film screenings inschools and community centers; organization of rural meet-ings focused on practical approaches; joint actions of phy-sicians and veterinary practitioners in designing specificposters based on suggestive drawings and photos regardingthe illness, and subsequent display in public places under thedirect supervision of the mayoralties; practical applications oftrichinelloscopy in schools and communities; publishing anddissemination of informative brochures for animal breedersand consumers; a strong collaboration between human andveterinary doctors in running the epidemiological and epi-zootological investigations on Trichinella infections; and theinclusion of basic knowledge about trichinellosis and otherfoodborne infections in school textbooks to increase theawareness from a young age (Cironeanu and Ispas, 2002).

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Disclosure Statement

No competing financial interests exist.

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Address correspondence to:Raul Neghina, M.D.

Department of ParasitologyVictor Babes University of Medicine and Pharmacy

5 Vasile Lucaciu St.Bl. B4, Sc.A, Ap.16

300051 TimisoaraRomania

E-mail: raul.neghina@gmail.com

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