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Epidemiological Features of Yersinia Infection in a Territory with Developed Agricultural Production

 Rediger
 1 Published: 23.11.04 Updated: 02.05.2005 14:08:36

Y.Y. Smirnova 1, A. B. Tebekin 2, G. Y. Tseneva 3, N. A. Rybakova 4, D. A. Rybakov 4. 1Centre for Diagnostics", Vologda, 2 State Agricultural Academy, Nizhnyi Novgorod, 3 L. Pasteur Scientific and Research Institute, Saint-Petersburg and 4 Vologda Regional Center for State Sanitary and Epidemiological Control, Russia

In the Vologda region of Russian Federation yersiniosis and pseudotuberculosis cases predominated in urban and specially in children population. Transmission was related to consumption of milk and dairy products (14%), meat (7%), water (1,5%), fruit and vegetables (74%) and contact with synantropic rodents (2%). Among different professional groups 4,0 0,6% were positive to Yersinia pseudotuberculosis serotypes I and III and 47,8 1,6% were positive to Yersinia entrocolitica serotypes 0:3, 0:4.33, 0:5.27, 0:6.30, 0:7.8 and 0:9. The most common Yersinia entrocolitica serotypes to cause human disease were 0:5.27, 0:3, 0:6.30 and 0:7.8 and professional groups at highest risk were animal and cattle breeders, staff of companies processing raw materials of animal origin, staff of vegetable stores and people in catering and sale.

Introduction

The prevalence of Yersinia infection is increasing among people all over the world. As reported in the proceedings of the International Symposium on Food-Borne Zoonosis, among zoonotic diseases yersiniosis is as important as salmonellosis in Russia (3).

During the last few years Yersinia infection has been defined as food-borne zoonosis with animals (wild, synanthropic, stock-bred) as the source and agricultural products including dairy, meat products, vegetables, fruit and fodder as transmission factors. Human and animal health care systems are of equally great importance when dealing with measures to prevent zoonosis. Both epizootic and epidemiological surveillance systems must receive equal attention (2).

The Vologda region is situated in the middle of North-Western Russia, covers 8.8% of the total territory and includes 12% of the total population. The region is quite favourable for intensive development of agricultural works and farming.

Infections caused by Yersinia enterocolitica and by Yersinia pseudotuberculosis have been reported in the region since 1988 and 1991, respectively. Since 1992, when separate notification was regulated in 13 region districts as well as in the cities of Vologda and Cherepovets, 107 pseudo-tuberculosis cases have been registered. A total of 504 yersiniosis cases in 21 region administrative districts have been registered during the same time. The average annual incidence rate increased up to 0.7 and 3.4 per 100,000 of population for pseudo-tuberculosis and yersiniosis, respectively.

During the period of observation sporadic cases were typical. Twice during the study period (in 1992 and 1998) the average yersiniosis prevalence rate in the region exceeded that in the whole country (1.7 and 2.9 times, respectively). The pseudotuberculosis prevalence rate in the region was considerably less than that in Russia during the study period.
Thirty percent of the total pseudo-tuberculosis cases were registered during outbreaks. Four outbreaks (in 1991, 1992, 1993 and 1995) were registered in neighbouring communities during which 52 persons, 41 children and 11 service staff adults, contracted pseudo-tuberculosis. All outbreak cases were defined as food-borne diseases with fresh cabbage and carrot salads given as transmission factors.

The morbidity rate exceeds the number of officially reported cases because laboratory and clinical diagnostics need improvement. Among samples screened from 18,000 patients suffering from different acute and chronic intestine dysbiotic disorders and allergies, 2.4% of the cases were culture positive for Yersinia. This rate is comparable to that for Salmonella and indicates the epidemiological significance of Yersinia as an etiological agent of intestinal infections in general.

Materials and Methods

From 1990 to 2002 serum samples from 15,448 humans, 3,201 small mammals and 772 farm animals were examined for Yersinia antibodies using commercially available diagnostic assays manufactured by the Scientific Research Institute for Vaccines and Sera (SRIVS) and Pasteur Institute of Saint-Petersburg. Bacteriological methods were used to test 51,002 human samples, whole cell organ homogenates of 5,085 wild and synanthropic small mammals, 1,197 samples from farm animals and 20,817 samples of food products and environmental objects. Cultures were performed with cold selection media. Phenotypic characterisation of Yersinia isolates was performed according to guidelines issued by Pasteur Institute of Saint-Petersburg (1).

Results and Discussions

Yersiniosis and pseudotuberculosis cases were registered primarily in urban populations (88% and 68%, respectively) and children predominated in both groups. The incidence ratio in adult population and children up to 14 years was 1 to 1.5. While analysing age and social standards of patients with yersiniosis and pseudotuberculosis it was ascertained that children from 3 to 14 years were predominate (85% and 97%, respectively) and that 95% of all cases were among children attending pre-school institutions and schools. This may indicate that public institutions play a major role in the dissemination of Yersinia infection.

Incidence of both infections had similar dynamics with peaks in May and June for pseudo-tuberculosis and in April for yersiniosis. Secondary peaks of yersiniosis came in October/November and pseudo-tuberculosis in December/January.

Epidemiological investigation of disease foci revealed that in 14% of cases caused by Yersinia enterocolitica patients indicated the consumption of milk and dairy products consumption as the transmission route, 7% by meat consumption and contact with animals, 2% by contact with synantropic rodents, 1.5% by unpurified water and 74% by fruit and vegetable consumption. A similar ratio was revealed for cases caused by Yersinia pseudotuberculosis.

To study the prevalence rate of infection, the main reservoirs in natural and household foci were defined. The circulation of Yersinia pseudotuberculosis was ascertained in 11 species of small mammals and of Yersinia enterocolitica in 13 species including grey rats, house mice, common field-voles, common shrews, red field-voles, water voles and field mice.
Different Yersinia enterocolitica serotypes were found in serum samples from 51.91.8% of examined farm animals (sheep18.03.0%, cows 49.42.7% and pigs 76.72.6%) and Yersinia pseudotuberculosis serotypes in samples from 14.21.3% of animals (in sheep 6.71.9%, cows 6.91.4% and pigs 28.62.8%). 

Among human sera examined (different professional groups) 4.00.6% were positive for antibodies to Yersinia pseudotuberculosis serotypes I and III and 47.81.6% were positive for Yersinia enterocolitica (serotypes O:3, O:4.33, O:5.27, O:6.30, O:7.8 and O:9). The percentage of seropositive samples in live-farmers, staff involved in animal-breeding and sale was 6.51.3, 2.20.6 and 4.21.6% for pseudo-tuberculosis pathogens and 58.02.6, 47.12.6 and 44.33.8% yersiniosis pathogens, respectively. In the control population not professionally at risk of infection pseudo-tuberculosis antibodies were found in 1.10.5% and yersiniosis antibodies in 17.63.9 % of cases. A significant difference for antibodies to Yersinia enterocolitica was observed between all professional groups and the control population. In contrast, only animal farmers showed a significant increase (P< 0.05) in pseudotuberculosis antibodies as compared to the control group.

Yersinia positive cultures indicate a wide spread of the pathogen. The percentage of Yersinia isolation varies between pigs (18.01.3%), synantropic rodents (5.80.5%), in small wild mammals (1.70.3%), human pathological material (2.10.06%), meat and dairy products (22.60.5%) and fruit and vegetables (6.50.3%). Yersinia enterocolitica was most frequently isolated from pig samples, products of animal origin and vegetables while Yersinia pseudotuberculosis was most commonly isolated from small mammals.

Table 1. Serotypes of Yersinia enterocolitica isolated from people who developed yersiniosis, from haematherm animals and foodstuff samples (%)

Examined objects

Serotypes of Y.enterocolitica

O:3

O:4.33

O:5.27

O:6.30

O:7.8

O:9

Not classified

Human material

13.7

5.3

18.5

17.1

14.9

2.9

27.6

Synantropic rodents

11.1

10.1

3.3

18.8

10.0

-

46.7

Wild small mammals

13.3

-

66.7

16.7

-

-

3.3

Pigs

6.5

10.5

10.5

21.0

6.5

4.0

41.1

Vegetables

2.6

8.2

5.6

15.7

3.2

-

64.7

Meat and dairy products

9.1

12.0

16.2

15.4

6.8

4.3

36.2

To define the epidemiological significance of environmental objects and haematherm animals as Yersinia infection reservoirs a comparative evaluation of the antigenic spectrum of Yersinia enterocolitica strains isolated from different sources was performed (Table 1). The analysis indicates that the most common serotypes of Yersinia enterocolitica to cause human diseases are O:5.27, O:3, O:6.30 and O:7.8. The particularity of human intestinal disease caused by all serotypes of Yersinia enterocolitica have zoonotic infection features.
The dynamics of annual yersiniosis morbidity rate in humans correlates with the monthly defined contamination of vegetable foodstuffs and the percentage of synantropic rodents infected (r = 0.549; r = 0.557, respectively).

Yersinia enterocolitica was most frequently isolated from carrots, cabbage, potatoes, beetroots and onions. The seasonal morbidity peak of Yersinia infection observed in the region can be explained by the availability of products such as early greenhouse-grown vegetables in addition to stored products.

The high percentage of rodents infected and trapped in stores as well as culture positive samples at any season (with the maximum from March to June and from September to November) indicates that stored and seasonal vegetables may be contaminated. The similarity between Yersinia enterocolitica strains isolated from synantropic rodents and vegetables and strains isolated from patients, as well as the identification of virulent Yersinia enterocolitica strains, confirms the role of vegetable stores as reservoirs of Yersinia infection. As indicated in Table 1, foodstuffs of animal origin are also of epidemiological significance for the dissemination of Yersinia infection.

The results of this study indicate that the following professional groups are at risk: animal and cattle breeders, staff at companies processing raw materials of animal origin, staff at vegetable stores and people in catering and sale. Significant differences in immunological status were found among these professionals as compared to the control population indicate the epidemiological importance of farm products and animals as reservoirs for human Yersinia infection.

References

1. Tseneva G.Y. Laboratory diagnostics of pseudo-tuberculosis and yersiniosis. St. Petersburg, 1997, 61.
2. Cherkassky B.L. Theoretical aspects of problems of food related zoonosis file://Materials of the international Symposium Food-related zoonosis (March 1-3, 1995, Moscow). Moscow,1995, 16-17.
3. Cherkassky B.L., Podounova L.G., Akoulova N.K. Food-related zoonosis in people of Russia file://Ditto,18-19.


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