Eurosurveillance

ECDC

Wild Small Mammals and Domestic Dogs Infected with Zoonotic Agents in Saint Petersburg and its Suburbs

 Rediger
 1 Published: 17.11.04 Updated: 17.11.2004 14:26:54
N. Tokarevich1, N .Stoyanova1, E. Kozhukhova 1,G. Makarova2, G. Volkova2, A. Khnykin2
1 Pasteur Institute, 2 City Center for Epidemiological Surveillance, Saint-Petersburg, Russia
In the Saint Petersburg area 2,5% of the wild small mammals were infected with Hantavirus, 2,6% with Coxiella burnetii and 2,9-5,5% with Leptospira. Zoonotic agents promote through synantropic animals and dogs the forming of infection foci within the city area

Introduction

In the territories of European North and North-Western Russia there are foci of certain zoonoses including leptospirosis, Q-fever, and Hantavirus infection  [1-3]. The largest city in the area is Saint-Petersburg. It is city with population of more than 4 million inhabitants and has a territory that covers more than 600 square kilometers, with numerous woodlands and parks in its periphery. Residents visit these areas quite extensively for agricultural, recreation, and ritual activities. Wild and synantropic mammals live in these territories, as well as large numbers of Ixodes ticks. In the city itself there are hundreds of thousands of domestic dogs. All factors mentioned can promote the existence of some zoonotic foci.
The objective of the present study was to investigate the proportion of small mammals (SM) and domestic dogs infected with Hantavirus, Q-fever, and leptospirosis and to reveal the role of different animals in human morbidity. We also wanted to determine high-risk city regions for these infections.

Methods

Lung tissue from 4.669 SM was examined with enzyme-immunoassay to detect Hantavirus and Coxiella burnetii.  The SMs belonged to 14 species, and were trapped during 1990-1999 at more than 90 locations in the city and its suburbs. Leptospira were examined in 1,500 SM including 300 Rattus norvegicus (gray rats) by culture and serology (micro-agglutination). In addition, sera from 139 domestic dogs with unknown diseases were examined. The sera were examined for Leptospira antibodies (micro-agglutination), Hantavirus (ELISA), and C. burnetii (indirect immunofluorescent reaction).

An epizootologic potential index was calculated according to the formula:

I= K1 * K 2,  where

I = the epizootologic  potential index of definite SM species

K1 = the detection rate of particular SM species in the study areas (number
of animals trapped per 100 traps per day)

K2 = the percentage of animals infected with the zoonotic agents

Results

Of the wild SM, 2.5% were infected with Hantavirus and 2.6% with C. burnetii (table 1). A majority of some species – Clethrionomys glareolus (bank vole), Apodemus agrarius (striped field mouse), and Sorex araneus (common shrew) – and the minority of some others– Microtus arvalis (field vole), Micromys minutus (harvest mouse), and Sorex minutus (Eurasian pygmy shrew) were infected with both of these agents.

Table 1.  Percentage of small mammals (SM) trapped in Saint-Petersburg from 1990-1999, and the distribution of Coxiella burnetii and Hantavirus by SM species

 
SM species
Average number of SM trapped (per 100 traps per day)
Coxiella burnetii
Hantavirus
Infected animals (%)
EPI*
Infected animals (%)
EPI*
Clethrionomys glareolus
(bank vole)
3.4
3.2
10.9
4.7
16.0
Apodemus agrarius
(striped field mouse)
2.6
1.5
3.9
2.2
5.7
Sorex araneus
(common shrew)
2.2
3.0
6.6
1.4
3.1
Microtus arvalis
(field vole)
1.7
1.2
2.0
0.8
1.4
Micromys minutus
(harvest mouse)
0.3
4.5
1.4
0.6
0.2
Sorex minutus
(Eurasian pygmy shrew)
0.3
2.0
0.6
0.4
0.1
Others
0.3
0.5
0.2
0.2
0.1

* EPI = epizootologic potential index

The carriage rates of Leptospira in the wild SM were: 5.5% (Clethrionomys glareolus), 4.3% (Microtus arvalis), 3.1% ( Apodemus agrarius), and 2.9% (Sorex araneus). The dominant serogroups of Leptospira were L. pomona (41.3 %) and L. grippotyphosa (28.2%). In the southern city districts, Rattus norvegicus are present after migration from farmyards previously situated there. The proportion of infected Rattus norvegicus was much higher (16.0%) compared to other SM, but the total number of Rattus norvegicus was quite small (K1 = 0.1%). Of the Leptospira serogroups isolated from Rattus norvegicus, 70% were L. icterohaemorrhagiae.

The most common SM species in the urbanized central city area was Rattus norvegicus, a typical representative of synantropic animals (K1 = 4,6%, and K2 = 12% in average). Despite the fact that proportion of Rattus norvegicus infected in southern city was quite high, the epizootologic potential index (I) was quite low (1.6) due to the low number of recovered rats. On the contrary, in the central city the index (I) of those animals was high (55.2), thus being a significant source of Leptospira icterohaemorrhagie there.
In the dogs with unknown diseases, 46.3% showed presence of antibodies to Leptospira (L. canicola in 27.2%, L. icterohaemorrhagiae in 18.4%, and L. gripotyphosa in 0.7%).

Discussion

The data from the present study demonstrate that SM trapped in the area of Saint Petersburg and its closest suburbs are significantly infected with zoonotic agents causing Hantavirus infection, Q-fever and leptospirosis. The determination of the epizootologic potential index (I), compared to only assessing the percentage of animals infected with zoonotic agent (K2), better permits assessing the role of every animal species as a potential source of infection. Thus, it was shown that Clethrionomys glareolus (I = 10.9), Sorex araneus ( I = 6.6), and Apodemus agrarius  (I = 3.9) are more important sources of Coxiella burnetii in Saint-Petersburg than Micromys minutus (I = 1.4) despite the quite  high K2 of the latter (table 1).
The use of the epizootologic potential index (I) enabled the identification of Sorex araneus (I = 10.5) and Apodemus agrarius (I = 8.9) as principle sources of Leptospira in the northern peripheral districts of Saint-Petersburg, and Clethrionomys glareolus (I = 31.1) and Apodemus agrarius (I = 18.4) in the southern and western parts (table 2). 

Table 2. Percentage of SM trapped in Saint-Petersburg from 1992-1995 and distribution of Leptospira  by SM species

 
 
SM species
Northern districts
South-Western districts
Average number of trapped SM (per 100 traps per day)
Infected animals (%)
EPI*
Average number of SM trapped (per 100 traps per day)
Infected animals (%)
EPI*
Clethrionomys glareolus
(bank vole)
6.0
0.8
4.8
5.1
6.1
31.1
Apodemus agrarius
(striped field mouse)
2.4
3.7
8.9
3.6
5.1
18.4
Sorex araneus
(common shrew)
3.4
3.1
10.5
2.5
2.5
6.3
Microtus arvalis
(field vole)
0.7
2.9
2.0
1.6
2.2
3.5
Others
0.6
4.2
2.5
0.9
1.2
1.1

Evidently the role of SMs as the source of Hantavirus, Coxiella burnetii, and Leptospira varies. Moreover, human beings can be infected in the out-of-city area as well. During the period from 1998 to 2000, 44 cases of Hantavirus infection were registered in Saint-Petersburg (0.3 cases per 100,000 inhabitants). Wild SMs are the only known virus source for humans. The role of wild SMs as a source of C. burnetii is not significant. This disease is only transmitted to humans by ticks. However, since the SMs are donors of C. burnetii to the ticks they make the Q-fever foci stable. They may also be couriers of C. burnetii between natural and agricultural foci of Q-fever.

The role of Apodemus agrarius as a potential C. burnetii source for humans may increase, since the animals tend to migrate to human activity areas. During the last few years in Saint-Petersburg only single cases of Q-fever have been registered despite the fact that wild SM are infected with C. burnetii more often than with Hantavirus. This supports the view that wild SMs are of limited significance as a potential source of C. burnetii to humans.

An inflow of zoonotic agents through domestic dogs and synantropic animals promotes the forming of active infection foci within the city area, and the risk of people being infected increases. This might be illustrated by leptospirosis, with dogs infected with Leptospira canicola and L. icterohaemorrhagie causing significant increase of human morbidity. During the last ten years 739 patients with leptospirosis were registered (1.6 per 100 000 inhabitants). This is 2.7 times higher than during the previous 10-year period of time. City districts with a high percentage of Leptospira-infected dogs also had a high level of human morbidity. The predominance of Leptospira canicola and L. icterohaemorrhagie also in humans may be considered as indirect evidence supporting the speculation that the main sources for human infection are synantropic animals and dogs.

References

1. Daiter AB, Stoyanova NA, Sleptsova VI, et al. Leptospira carrier state in small mammals in open station of North-Western region of the USSR. VII European and IX USSR leptospirosis research conference. Moscow, 1991; 44-45.
2. Rybakova N., Tokarevich N, Chaika N. Q-fever monitoring in Vologda province of northern Russia. Rickettsiae and Rickettsial Diseases at the Turn of the Third Millenium. Elsevier, Paris, 1999; 351-355.
3. Zhavoronkov VG, Doroshina EA, Titova NM. Topical questions of epidemiologic control in Leningdrad Region. EpiNorth 2000;1(2):28-30.


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