New trends and clinical patterns of human trichinellosis in Russia at the beginning of the XXI century

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1 Veterinary Parasitology 132 (2005) New trends and clinical patterns of human trichinellosis in Russia at the beginning of the XXI century N.N. Ozeretskovskaya a, *, L.G. Mikhailova b, T.P. Sabgaida a, A.S. Dovgalev c a E.I. Martsinovsky Institute of Medical Parasitology and Tropical Medicine, Mal, Pyrogovskaya 20, Moscow , Russian Federation b Department of the State Epidemic Surveillance, Ministry of Health of the Russian Federation, GSP-4, Rahmanovsky 3, Moscow, Russian Federation c Centre of Epidemic Surveillance of the Moscow Region, Mitischi, P.O. Box 68, Russian Federation Abstract Official national statistics show a gradual decline in the incidence of trichinellosis in Russia from 971 cases in 1996 to 527 cases in Of the total 864 cases involved in 47 trichinellosis outbreaks during , only 35.8% were due to infected pork compared to 80% in Other important sources were wild animals, such as bear (Ursus arctos) (39.5%), badger (Meles meles) (10.6%), and dog meat (11.9%). Children composed 15.9% of all cases. Overall, 81.0% of pork-cases occurred in the European part of the country, and 89.4% of bear-meat cases were from the Asian region where most of the badger and dogmeat cases also originated. The percent of clinically severe cases of disease derived from pork and from bear meat was 7.7% and 7.9%, respectively; the frequency of moderate cases from pork was significantly higher than from bear meat. Clinically severe cases from badger and dog meat were 1.1% and 1.9%, respectively, where the number of clinically moderate cases from badger meat was significantly larger than that from dog meat. A disturbing trend is the 52.3% of trichinellosis cases during in Russia that were derived from wild animal meat, especially the clinically severe cases occurring among the aboriginal Siberian population. The contributing factors to the slow decline in trichinellosis incidence in Russia and to the increase in percentage of cases originating from wild animal meat are the distribution and consumption of veterinary-uncontrolled pork, poaching and distribution of wild animal meat, and the neglect of medical and civil regulations. These trends should be seriously evaluated by the institutions of health, education, and by the veterinary service. # 2005 Elsevier B.V. All rights reserved. Keywords: Trichinellosis; Spread; Sources; Sylvatic trend; Clinical patterns 1. Introduction In the 1930s, Belorussia, Ukraine, and the Central European and Far East regions of the USSR * Corresponding author. address: kdmurrell@comcast.net (N.N. Ozeretskovskaya). were endemic for trichinellosis (Merkushev and Ozer- etskovskaya, 1968). By the end of the 1960s, the incidence of trichinellosis had dropped to almost zero due to obligate pork inspection (trichinelloscopy) practised in Russia since 1923 (Boev, 1978). However, the new economic development of the Russian North and Northeast in the 1970s caused a /$ see front matter # 2005 Elsevier B.V. All rights reserved. doi: /j.vetpar

2 168 N.N. Ozeretskovskaya et al. / Veterinary Parasitology 132 (2005) mass migration of people from regions of the country free of zoonotic helminthi infections (Ozerets-kovskaya, 1979). The incidence of trichi- nellosisinrussiafrom1971to1975increased16- fold; in 96% of patients the source of infection was wild animal meat, demonstrating a relationship between the emergence of this source of infection and social and economic changes of the times (Murrell, 2001). These changes are implicated in 80% of 1383 cases registered in outbreaks of trichinellosis in Russia during (Ozeretskovskaya, 1997). We present here an analysis of the main trends in trichinellosis epidemiology in adults and children since 1996, including the patterns of outbreak distribution, principal sources of the infection, clinical features of infection in Russia, and the measures taken to control trichinellosis. 2. Materials and methods The official national statistics on the incidence of trichinellosis in Russia are based on reports from the territorial Epidemic Surveillance Centres (TESCs) on single cases submitted to the Federal Centre of Epidemic Surveillance (FCES), and on reports on the trichinellosis outbreaks submitted to the Department of the State Epidemic Surveillance of the Ministry of Health of Russian Federation. The data on the incidence of human trichinellosis in Russia are published in the Information Bulletin of Statistic and Analitic Materials (IBSAM) of the Ministry of Health. IBSAM data (2001) on trichinellosis incidence during , FCES data on trichinellosis incidence in 2001 and 2002, and 47 TESCs reports on trichinellosis outbreaks during (864 cases), were collected. Data were analysed for 4 main aspects: (1) incidence of the infection in adults and children; (2) the geographical distribution of trichinellosis outbreaks; (3) the main sources of infection; and (4) the clinical features of disease from the different sources of infection. Associations were analysed for statistical significance by two-by-two table analysis using Epi-Info version 3, CDC Epidemiological Program Office software. Table 1 National incidence of trichinellosis in Russia in Incidence Years Total number Children number Children (%) Results and discussion 3.1. The incidence of trichinellosis in Russia between The incidence of trichinellosis in Russia has declined gradually from 971 cases in 1996 to 527 in 2002 (Table 1). The number and the percent of children affected (Table 1) declined from 1996 to 2000 (odds ratio (or) = 0.68, x 2 = 5.97, p = 0.015). The rise in the incidence of infection in 2001 (Table 1) is related to the large outbreak in the Krasnodar region when 119 cases including 25 children were registered. The increase in the percent of infected children in 2002 is due to their high involvement (19.3%) in 2 large bear-meat outbreaks The geographical distribution of trichinellosis outbreaks in Russia In the North-European part of the country, 4 outbreaks of trichinellosis from infected pork were registered in the Kaliningrad and the Vologda region (48 cases), and 2 cases in the Sankt-Petersburg in 1998 (Table 2). In the Central European part, 4 pork outbreaks (44 cases) occurred during in the Moscow and the Tula regions. Two outbreaks due to infected badger (Meles meles) meat (26 cases) were registered in 1998 and in 2002, and the outbreak from dog meat (10 cases) occurred in 2001 in the Volgograd region (Table 2). The South-European part of the country was one of the most affected by trichinellosis, with 81.2% of the cases resulting from the consumption of infected pork (Table 2). The largest outbreak (119 cases) in the Krasnodar region took place in An outbreak from infected bear (Ursus arctos) meat (36 cases) occurred in the mountain region of the territory in Two outbreaks that are not included in Table 2 were an outbreak from jackal meat (10 cases), which

3 N.N. Ozeretskovskaya et al. / Veterinary Parasitology 132 (2005) Table 2 The geographical distribution of trichinellosis outbreaks cases in Russia in Territory Pork Bear meat Badger meat Dog meat Total Number % Number % Number % Number % Number % North European Central European South European West Siberia East Siberia Northeast/East took place along the shore of the Black Sea in 2001, and an outbreak from wild boar meat (9 cases), registered in the mountain part of the territory in In West Siberia, the main sources of infection were pork (38.7%), bear meat (U. arctos) (36.6%), and badger meat (M. meles) (37.3%, Table 2). The number of cases from pork and from badger meat was higher than bear meat (or = 0.50, x 2 = 7.50, p = and or = 1.58, x 2 = 3.47, p = 0.006, respectively). Two outbreaks (22 cases) in Cheliabinsk City (the South Ural territory) in were also included. Two outbreaks from infected bear (U. arctos) meat occurred in the Yamal-Nenezk Autonomous District (AD) (26 cases) in 1999, and 1 outbreak (10 cases) in One single lethal case from bear meat was registered in 2001 in the Hanti-Manssi AD where trichinellosis in was detected only by seroepidemiological research (Sergiev and Ozeretskovskaya, 2003). In East Siberia, the second highest risk territory for trichinellosis, 60.2% of outbreak s cases were traced to U. arctos meat (Table 2). In the Krasnoyarsk region, 2 outbreaks (46 cases) with 1 mortality and 4 single lethal cases were registered in One outbreak in the Republic of Tuva and 2 outbreaks in the Republic of Hakassia (87 cases) occurred in 1999 and in , respectively. In the Northeast East territory of the country, including the Primorsky region, infected bear (U. arctos) meat was responsible for 90.2% of the cases (Table 2). The outbreaks were registered in the Republic of Sakha (80 cases) in 1999, and in the Primorsky region (56 cases) in An outbreak due to dog meat occurred in the Kamchatka region (15 cases) in 1998 (Table 2) The pattern of trichinellosis outbreaks during according to the source of infection The main causes of trichinellosis outbreaks in were consumption of infected swine or bear meat where the proportion of each source was often inversely correlated. That reflected the occurrence of extra large outbreaks, such as the pork outbreak in the Krasnodar region in 2001 or the bear meat outbreaks in the Republic of Sakha and the Primorsky region in 2002 (Table 3). Overall, during , pork accounted for 35.8% and bear meat Table 3 The pattern of trichinellosis outbreaks cases in Russia in according to the meat-source of infection Year Pork Bear meat Badger meat Dog meat Total number Number % Number % Number % Number % /14 a / / / / / / / / / / / / / / / / / / Total 309/ / / / Children (%) a The number of cases in the table is given as total/children.

4 170 N.N. Ozeretskovskaya et al. / Veterinary Parasitology 132 (2005) for 39.5% of outbreak s cases (Table 3). Bear meat was a more frequent source of infection than pork only among adults (or = 1.47, x 2 = 11.64, p = ). Pork as a source of infection was significantly more frequent than badger and dog meat among adults (or = 0.21, x 2 = , p =10 9 and or = 0.30, x 2 = 78.68, p =10 9, respectively) and among children (or = 0.40, x 2 = 12.62, p = and or = 0.18, x 2 = 31.91, p = , respectively, Table 3). Two minor but consistent sources of infection were badger and dog meat. Only 2 outbreaks from badger meat were registered in the European part of Russia, 5 outbreaks occurred in West and in East Siberia (Table 3). Children constituted 31.5% in these outbreaks, much more than in the outbreaks from bear meat. Badger meat in 6 out of 7 outbreaks was eaten as shashlik (small bits of meat roasted on the metal sticks on the open fire), a favorite dish for children and teenagers. Among 103 cases due to dog shashlik, 27 (26.2%) were children and teenagers. Five outbreaks from game or meat from stray dogs were registered in East Siberia and one outbreak in the Kamchatka region. Only 1 outbreak occurred in the Central European area from the meat of a dog from a private swine-breeding farm. The number of children, that had eaten badger meat, was significantly larger than those infected from dog meat (or = 0.47, x 2 = 5.19, p = 0.023, Table 3) The severeity of the clinical course of trichinellosis according to the source of infection In 18.7% of cases, pork had been purchased at the town markets, in all other cases pork was produced in house or obtained from private sources, and used without veterinary control. In the remnants of implicated pork available for trichinelloscopy, 3 5 larvae per microscopic field were revealed. The incubation period in pork-outbreaks differed from 5 8 to days. Trichinelloscopy of implicated bear meat revealed 3 5 to larvae per 28 cuts. The incubation period in bear meat outbreaks, regardless of geographical region, was days which corresponded with data obtained earlier (Ozeretskovskaya and Pereverzeva, 1976). The remnants of badger or dog meat were not available for examination. In contrast to superficial examination of implicated meat, the clinical survey of patients has been more thorough where 71.3% of patients were surveyed in the regional hospitals with clinical, biochemical, serological laboratory analyses and ECG, and if necessary, X-ray examination. The severe courses of trichinellosis from contaminated pork were revealed in 7.7% of cases, moderately severe in 74.6%, and mild courses in 17.6% of the total infections (Table 4). One single lethal case from infected pork was registered in the Stavropol region. In outbreaks from infected bear meat clinically severe disease was reported in 7.9%, moderately severe in 51.0% and mild symptoms in 41.1% of cases (Table 4). One fatal outcome in the outbreak and 4 single lethal cases from infected bear meat were registered in the Krasnoyarsk region. The number of patients with moderately severe disease in the pork-cases was larger than in bear-meat cases (or = 0.30, x 2 = 45.12, p =10 9, Table 4). The number of mild pork-cases was lower than in bear and in badger meat cases (or = 3.12, x 2 = 37.02, p =10 9 or = 2.75, x 2 = 15.14, p = , respectively, Table 4). The incubation period for trichinellosis obtained from dog meat in outbreaks in East Siberia and in the Kamchatka region was days. In the dog meat outbreak in the Volgograd region a boy age 15 suffered from severe disease after 17 days of incubation. The severe course of disease from dog meat occurred in 1.9% of cases, moderately severe in 40.8%, and a mild course in 57.3% (Table 4). A mild course of disease Table 4 The severity of the clinical course of trichinellosis in Russia in the period according to the source of infection The source of infection Severe Moderately severe Mild Total number of patients Number % Number % Number % Pork Bear meat Badger meat Dog meat

5 N.N. Ozeretskovskaya et al. / Veterinary Parasitology 132 (2005) was more frequent in patients infected with dog meat than in those infected with badger meat (or = 2.18, x 2 = 7.20, p = 0.007, Table 4) Prophylactic measures Every trichinellosis outbreak is followed by an epidemiological investigation that established the source of infection, the amount of consumed infected meat, the results of trichinelloscopy, and a possible further distribution of meat. People who consumed the infected meat would be actively sought after for their preventive chemotherapy. Sanitary propaganda and administrative measures for prosecuting in the distribution of uncontrolled infected meat are organised. Analysis of the reports on the outbreaks in demonstrated an activity of TESCs in the restriction of outbreaks. In 1998, mebendazole was administered to 237 patients and, preventively, to 158 persons that had consumed infected meat but were not ill (so-called contact persons ). In 2001, mebendazole was administered preventively to 506 contact persons. 4. Conclusion In spite of a decline in the incidence of trichinellosis in Russia over a 7-year period ( ), the situation in Russia is far from satisfactory. The main risk factors responsible for outbreaks of trichinellosis are (1) the distribution and purchasing of veterinary-uncontrolled pork from private sources; (2) the poaching and the distribution of uninspected meat from bear and other wild animals; and (3) ignorance or avoidance of food safety rules by rural populations, especially children. The 52.3% cases of trichinellosis originating from game and other animal meat in Russia in is a dangerous trend, especially with respect to the bear meat outbreaks in the aboriginal populations of the Russian North. Although only 35.8% of cases were due to infected pork, it continues to be an important source of trichinellosis in Russia. The situation should be evaluated seriously by the institutions of health and education and by the Veterinary service. Acknowledgements The authors wish to thank Professor K.D. Murrell of the Royal Veterinary and Agricultural University, Copenhagen, Denmark for the lively interest in their work, helpful criticism and for the unfailing editorial help in preparing the manuscript. References Boev, S.N., Historical review on trichinellae and trichinellosis. In: Boev, S.N. (Ed.), Trichinella and Trichinellosis. Nauka of Kazakh, SSR, Alma-Ata, pp (in Russian). Information Bulletin of Statistic and Analytic Materials, Part 3.2, 2001, pp (in Russian). Merkushev, A.V., Ozeretskovskaya, N.N., Trichinellosis. In: Manual on Microbiology, Clinic and Epidemiology of Infectious Diseases, Medgiz, Moscow, pp (in Russian). Murrell, K.D., Trichinellosis: now and forevermore? Parasite 8, Ozeretskovskaya, N.N., Zoonotic helminthiases of the Northeast and Far-East of the USSR. Peculiarities of their clinical pattern in migrants and the prevention of the development of new anthropogenic foci. Vestnik Med. Acad. Nauk 12, (in Russian, English summary). Ozeretskovskaya, N.N., Incidence of Trichinellosis and Characteristic of Outbreaks in the Russian Federation in (June). ICT Country Status Reports, Beltsville, MD, USA. Ozeretskovskaya, N.N., Pereverzeva, E.V., Clinical, epidemiological and parasitological features of the Arctic Trichinella strain (ATS). In: Proceedings of the Third International Conference on Bears Their Biology and Management, Switzerland, Morges, pp Sergiev, V.P., Ozeretskovskaya, N.N., Prevalence of human parasitic infections in Russia: epidemiology past and present. In: Akuffo, A., Linder, E., Ljungstrom, I., Wahlgren, M. (Eds.), Parasites of the Colder Climates. Taylor & Francis, London and New York, pp