Human Taeniasis in Western Romania and Its Relationship to Multicultural Food Habits and Influences

Introduction

T aeniasis represents an intestinal infection produced by adult tapeworms of the genus Taenia. It is acquired by the consumption of raw or undercooked meat containing the infective cysticerci. Ingestion of measly beef is responsible for infection with Taenia saginata and ingestion of measly pork may lead to infection with Taenia solium. Only humans are susceptible to be the final host for both Taenia species. About 50 million people are infected with T. saginata and 5 million with T. solium worldwide (Schantz, 1996). The prevalence of human taeniasis with T. saginata in Europe varied between 0.01% and 10% during the period 1973–2000 (Cabaret et al., 2002). Symptomatology of intestinal taeniasis is generally mild including abdominal pain, nausea, dizziness, headache, weight loss, anorexia, and allergic syndromes (Schantz, 1996; Willms and Sotelo, 2001). The most important complication of T. solium infection is neurocysticercosis caused by the ingestion of the eggs (especially by autoinfection) (Schantz, 1996; Jeri et al., 2004; Willingham and Engels, 2006). Diagnosis of the disease uses one of the following methods: questioning and self-detection, stool microscopy (detection of the eggs or gravid proglottids), perianal egg detection (Graham's test), coproantigen detection ELISA, copro-DNA assays, and serology (Schantz, 1996; Willms and Sotelo, 2001; Rajshekhar, 2004; Willingham and Engels, 2006). Infection can often be recognized by the patients themselves when individual/short chains of proglottids are eliminated in the stool (Schantz, 1996; Willms and Sotelo, 2001; Willingham and Engels, 2006). Species are differentiated by counting the primary uterine branches in gravid proglottids: 12 or more are characteristic for T. saginata and 10 or less for T. solium (Schantz, 1996; Willms and Sotelo, 2001). Treatment is based on the following specific antihelminthic drugs: Praziquantel, Albendazole, and Niclosamide (Willms and Sotelo, 2001; Rajshekhar, 2004; Montresor and Palmer, 2006; Willingham and Engels, 2006).

Romania, the largest southeast European country (approximately 23 million human inhabitants), is made up of nine regions. Banat region is situated in the western part and includes the largest Romanian county, Timis County, which lies across the border with Serbia and Hungary.

The purpose of this study was to overview the epidemiological, clinical, and therapeutic characteristics of taeniasis cases diagnosed in Timis County, Romania, during a 37-year period. The particular public health conditions and possibilities for prevention of the disease have been addressed.

Materials and Methods

Victor Babes Clinical Hospital in Timisoara is the reference hospital for infectious diseases in southwestern Romania and, particularly, in Timis County.

The medical charts of the patients diagnosed with taeniasis at the above mentioned hospital were descriptively analyzed, and the following data were retrospectively collected: registration number, age, sex, address, date and length of hospitalization period, profession, clinical symptomatology, eosinophil count, stool examination, and specific therapy. The elimination of the proglottids established the final diagnosis in all cases. The period of the study covered 37 years (1971–2007). Medical documentation before 1971 was not available in the archive of the hospital.

Results

Twenty-six patients were hospitalized for taeniasis at Victor Babes Hospital of Infectious Diseases in Timisoara, Romania, during the period 1971–2007. They were admitted to the hospital for clinical symptoms and/or elimination of helminthes proglottids. During hospitalization, the correct diagnosis allowed prompt institution of appropriate therapy.

Eighteen of the hospitalized patients (69.3%) originated from Timis County. The age of the study group ranged largely from 19 to 73 years with a mean of 38.3 years (Table 1). All cases were adults (over 18 years old), and 20 patients (77.0%) were females. Most patients (65.4%, n = 17) were inhabitants of urban areas. Laborers (46.2%, n = 12) and unemployed people (30.8%, n = 8) were predominantly affected (Table 2). Cases were classified according to the year of hospitalization and political regime that held power at that time (Table 3). A distribution in relation to the seasons has also been evaluated: five cases (19.2%) hospitalized in winter (December to February), nine cases (34.6%) in spring (March to May), four cases (15.4%) in summer (June to August), and eight cases (30.8%) in autumn (September to November).

Abdominal pain, asthenia, and loss of appetite were the most frequent clinical symptoms (Table 4). No cases of neurocysticercosis were detected within the study group. Most of the patients (80.8%, n = 21) were hospitalized for 1 to 7 days. The length of hospital stay ranged between 8 and 14 days in four patients (15.4%), and one patient (3.8%) was hospitalized for 16 days.

Eosinophilia of 5% to 40% was evidenced in 10 cases (38.5%). The patient who required the longest hospitalization period (16 days) had the highest peripheral eosinophil percentage 40%. The precise diagnosis at the species level showed T. saginata in four cases (15.4%) and T. solium in one case (3.8%). In the medical charts of the remaining 21 patients, the diagnosis of taeniasis was registered without any other specifications. Beside the elimination of the proglottids in all cases, Taenia eggs were also found in seven patients by stool examination, and a Taenia scolex was observed in one case. Coinfection with Giardia lamblia was diagnosed in one patient.

All cases underwent specific antihelminthic therapy as follows: Niclosamide (61.5%, n = 16), Praziquantel (19.2%, n = 5), Albendazole (11.5%, n = 3), Mebendazole (3.9%, n = 1), and Piperazine (3.9%, n = 1). The outcome was favorable, and all patients showed complete recovery. None of the patients required further hospitalization.

Discussion

The incidence of taeniasis varies largely among the different regions of Romania (Radulescu, 2000). The morbidity of taeniasis on the entire territory ranges between 0.4% and 0.75%, with higher values in Banat region and southcentral Moldavian region (Radulescu, 2000). The rates are unsurprisingly high in these two regions as a consequence of the gastronomic customs. In Moldavia, pig slaughtering especially during the cold season is followed by an old-fashioned rite in which the housewife prepares a lot of pork dishes varying from sausages to pig trotters jelly. Other specialties include force-meat rolls in cabbage and the Moldavian minced meat. On the other hand, Banat's cuisine comprising numerous fried pork or beef specialties was mainly influenced by the Serbian and Austro-Hungarian ones and partly by the Italian, French, and Greek ones. Appetizers including traditional pork products are widely consumed in this region (Travel Guide Romania, 2009).

Generally, people of all ages are susceptible to taeniid infections, and the age of exposure is determined by the age at which raw meat consumption begins (Schantz, 1996). Although no children were diagnosed with taeniasis in this study, the age of the patients ranged largely. Epidemiological data showing that females are predominantly affected (Radulescu, 2000) were confirmed by our study. The explanation is related to the culinary customs of the housewives, who taste continuously the meal while preparing it, and not to increased receptivity (Zanc, 2001).

Usually people living in cities and towns use to consume meat prepared in rural settings, especially by relatives or friends raising and slaughtering animals in improper sanitary conditions. This practice was especially frequent in the late communist period (before 1989) when commercial meat was not available. Thus, although most of the patients lived in urban areas, the source of infection was in the countryside.

The distribution of cases according to their professions confirmed the hypothesis that Taenia tapeworm diseases are usually associated with limited formal education and poverty (Willms and Sotelo, 2001). The highest rates of poverty (35.4%) and unemployment were registered in Moldavia (Report of the Commission against Poverty and Promoting of the Social Inclusion and World Bank 2003), which counted for more than one-third of the Romania's unemployed people and 18% of its employees at the end of 1995. On the contrary, Banat region and especially Timis County registered at the end of the same year one of the lowest rate of unemployment (4%) (Badulescu, 2006). Surprisingly, the incidence of taeniasis is high in both the regions; this demonstrates the importance of food habits in the pathogenesis of the disease.

The socioeconomic particularities of the political regimen, either communism or democracy, had no impact on human taeniasis as the mean number of cases were much similar: 1.8 and 1.5, respectively.

Niclosamide, an extremely cheap drug, considered as the most promising for large-scale use (Montresor and Palmer, 2006), was administered in most of the cases as a result of its wide availability in the hospital. It was followed by Praziquantel and Albendazole, both with evidence of high cure rates (Willms and Sotelo, 2001). Advanced methods for the diagnosis of the disease were not available due to the strictly limited financial resources of the hospital.

The disease might be more frequently diagnosed in patients with mild symptomatology or asymptomatic ones who are usually cared by general practitioners, thus explaining the low number of cases treated in hospitals. Taeniasis is not a notifiable disease in Romania, and therefore no supplementary data on infected individuals treated by their physicians without referral to the index hospital are available.

Conclusions

Human taeniasis remains a worrisome issue for public health and food safety authorities as well as a continuing threat to animal production (Hoberg, 2002). Several prophylactic measures must be considered for the eradication of the disease. Among them, the most important is the sanitary education of the masses dealing with the following aspects: implementation of routine freezing and proper cooking of pork/beef, interdiction of raw sausages consumption, adequate control and inspection of the meat, proper disposal of human feces, irrigation of vegetables with uncontaminated water, and animal vaccination (Willms and Sotelo, 2001; Willingham and Engels, 2006; Dorny and Praet, 2007).

Although our study had several limitations (low number of patients, retrospective nature), it showed the impact of a zoonotic disease on human health with the intention to increase the awareness of the authorities for the implementation of national campaigns envisaged to improve the situation. The general practitioners may successfully facilitate the access of their patients to informational and educational brochures during their regular visits, thus contributing to the prevention and early diagnosis of zoonotic diseases. The individual perceptions of the infective risk are very low especially in rural regions, thus the implementation of efficient communication strategies between individuals and healthcare professionals is mandatory. A strong collaboration must also be established between family physicians and veterinary doctors especially in the countryside regions where humans live in close proximity to animals on which they rely mostly for their food resources.