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Six out of 20 mosquito species were infected with Wolbachia. Pools of Aedes albopictus , Cx. After checking mosquitoes individually, it was found that there was no development of Dirofilaria to the infective larval stage in specimens infected with Wolbachia. Twenty-two Dirofilaria -infective pools were Wolbachia -free and only two mosquito pools were Wolbachia -infected. The potential for transmission of Dirofilaria in mosquito species naturally uninfected with the symbiotic bacterium Wolbachia is higher than in species infected with the bacterium.

Dirofilariasis is a vector-borne disease common in many countries on various continents [ 27 , 42 , 44 , 60 ].

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Sources of infection for mosquitoes are infected dogs, less often cats and wild canines wolves, foxes, etc. Dirofilaria immitis and Dirofilaria repens are transmitted by culicid mosquito species belonging to the Culex , Aedes , Ochlerotatus , Anopheles , Coquillettidia , Armigeres and Psorophora genera [ 42 , 58 , 69 ]. Vectors ingest microfilariae during a blood meal on an infected host. In mosquito Malpighian tubules, microfilariae develop to the third stage larvae L3 [ 34 ]. The season for Dirofilaria transmission in the central part of Russia begins in late May to early June [ 26 ].

L3 reach the salivary glands and proboscis from where they are transferred while feeding to another host [ 34 , 43 ]. However, development of larvae to the infective stage does not always occur; Dirofilaria remain in the Malpighian tubules and do not undergo further development or are encapsulated by the immune system of mosquitoes, and may also die within a few hours of entering the intestine of a mosquito [ 18 , 34 ].

Thus, only mosquitoes in which development has progressed to the third stage larvae L3 can be considered epidemiologically competent vectors, and the larvae, infective. Dirofilaria infection is endemic in Russia. Two species of Dirofilaria D. Prior to , D. The first case of D. In Russia, mosquitoes infected with Dirofilaria have previously been investigated in the southern regions Astrakhan, Rostov, Krasnodar Krai and Republic of Adygea and the estimated infection rate EIR was 1. Even though dirofilariasis is a concern in Russia, many areas have not been sufficiently studied.

Also, there are no data on the species of mosquito that are potential vectors of dirofilarial worms. Identification of mosquitoes in all cases was conducted only to the genera level: D. An endosymbiotic, maternally inherited bacterium, Wolbachia pipientis Rickettsiales: Rickettsiaceae , hereafter Wolbachia , infects filarial nematodes and many insects, including some mosquito species.

Wolbachia is required for the development and survival of filarial nematodes [ 61 ], whereas its symbiotic relationship with mosquitoes is largely parasitic [ 65 ]. Among the culicid mosquito species, Culex pipiens, Cx. However, it was found that Culex pipiens f. In continental Portugal, Cx. However, D. The hypothesis concerning the influence of Wolbachia on the transmission of Dirofilaria by Cx. There are only three studies that have focused on investigating simultaneous infection with native Wolbachia and Dirofilaria in mosquitoes from natural populations [ 22 , 23 , 51 ].

Therefore, the effect of co-infection with native Wolbachia on mosquito vector competence for Dirofilaria remains unclear. Prior to clarifying whether naturally occurring Wolbachia has any influence on filarial susceptibility or the development of Dirofilaria to the infective stage in the vectors, it is necessary to understand Wolbachia -mosquito interactions, which mosquito species are infected with the bacterium, the variability of bacterial strains, and the frequency with which Wolbachia occurs in mosquito populations. The objectives of the current study were to examine mosquito fauna and to identify mosquito species that can potentially transmit filarial worms in rural and urban localities in the central part of European Russia compared with the Black Sea resorts, and to evaluate epidemiologically dangerous mosquito species in which larvae develop to the infective L3 stage.

All mosquito species were screened to determine their Wolbachia infection status. Collection of mosquitoes in the central part of Russia was conducted throughout the warm season in —, and in the southern part for one month at each point in — and Exact locations and months of gathering are presented in SM1. Figure 1. Map of mosquito sample sites and Dirofilaria infection rates EIRs. EIR values for total D. The exact names and geographical coordinates of the places of collection 1—11 are presented in SM1.

At one of the sampling points in the Moscow region 5 Fig. To compare the infection rate of mosquitoes in urban and rural areas, we collected mosquitoes near human habitations and in forests. Mosquito collection sites in the south were located in human settlements in a resort area. On the Black Sea coast of the Caucasus 8, 9, 10 Fig. The specific name of the tribe Aedini is presented according to the studies of Wilkerson et al.

Identification of the molestus and pipiens forms of Cx. The thorax-head and abdomen of each mosquito in the group were dissected and formed the pool. In some cases, individual thorax-heads were analysed. Extraction was conducted separately for the abdomens and thorax-heads in order to determine infected and infective mosquito specimens, respectively.

For the PCR analysis, we used female mosquitoes which were divided into pools. Each pool was tested separately to identify D. Negative and positive controls were used in each PCR analysis to avoid false-positive results. The positive control used in the study was obtained from adult D. The presence of filarial DNA was confirmed using 1. In the text, all EIRs are given per specimens. In cases where Dirofilaria DNA was detected in pooled abdomens from the mosquitoes, pools of abdomen and individual thorax-heads were tested for Wolbachia infection.

In other cases, pooled mosquito thorax-heads were analysed. To distinguish between two strains of Wolbachia in Ae. The w Pip infections in Cx. The collected mosquitoes included 20 species; 16 species were in the central part of Russia and seven species on the Black Sea coast. The most abundant mosquito species in the temperate climate region was determined to be Ae. In the subtropical climate on the Black Sea coast, the most abundant sampled mosquito species was Ae.

The highest EIR values occurred with the species An. Both Dirofilaria species were found in one pool of Ae. More than one abdomen pool positive with D. Table 1. Mosquito species composition and their collected numbers in studied regions. If we compare infection in the abdomen with the thorax-head, D. The species Ae. In four species, Ae. In the Nizhny Novgorod region Fig. In the Tula region Fig.

In the Moscow region Fig. The first infected mosquitoes were recorded in May and the last in August—September. In the forest zones of the Nizhny Novgorod and Tula regions, with a sample of specimens, no infected mosquitoes were found SM2.

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The presence of Wolbachia was found in six out of 20 studied mosquito species. Specific sample sites and screening results are presented in an additional file SM3. Sequences of Wolbachia wsp genes from all six mosquito species demonstrated that all bacteria belonged to supergroups A or B, which were shared between arthropods Table 3. No filarial bacteria were amplified.

Two Wolbachia strains were present in studied Ae. Based on the wsp gene sequence, Wolbachia strains in Cq. Table 3. Positive pools for both Dirofilaria and Wolbachia. Bold, samples positive for Wolbachia. A total of 90 Dirofilaria positive abdomen and thorax-heads pools were analyzed for simultaneous infection with Wolbachia Table 3. Fifteen pools of Ae. Dirofilaria was found in 22 thorax-head pools of mosquitoes uninfected with Wolbachia and in two thorax-head pools which were positive for Wolbachia. In order to investigate a possible association between the occurrence of Wolbachia and the development of Dirofilaria to the infective third larval stage L3 within mosquitoes, we tested the thorax-heads of individual specimens from 12 pools: 25 individuals five pools of Ae.

There was no possibility to study one pool of Ae. The development of D. Neither D. The detection of infection with D. This is the first large-scale study of the infection of mosquitoes in the European part of Russia involving identification of the mosquito species. The published results on mosquito infestation in Europe, including Turkey, in comparison with our data are presented in Table 4.

Previously, Ae. In our study, infection with Dirofilaria was newly detected in the first four of these mosquito species. However, development of the larvae did not reach the infectious stage. Table 4. Published results about Dirofilaria in mosquito species in Europe, including Turkey, in comparison with data obtained in this study. It should be noted that their epidemiological significance is confirmed by the presence of third-stage larvae in the thorax-heads. Special attention should be paid to Ae. As far as we know, the infection of natural populations of Ae.

Based on a small sample 21 females , the EIR of this species of mosquitoes was reported as 5. In our study, the most abundant species of mosquito was Ae. Infection of Cq. However, in Moldova [ 58 ], mosquitoes of these three species were infected with Dirofilaria to a greater extent than in our results for Russia Table 4.

In our study, Ae. The epidemiological significance of Ae. Its infection rate in different countries varied from 0. In Russia, in the Nizhny Novgorod region, there were no infected mosquitoes of this species; in Tula, D. In the Moscow region, of a small sample of three Ae. The infection rate with D. The difference is that in our samples, both mosquito species were infected, not only with D. In our study, the highest EIR value was found in An. Importantly, some An. The females that flew out after the winter diapause actively attacked both humans and dogs.

In the Nizhny Novgorod region, 2 out of 12 females caught in May were infected with microfilariae. Somewhat different infection rates of this mosquito species were reported in Moldova Table 4. The lowest infection in our study was found in Ae. According to our data, Ae. In Italy, Ae. According to our results, Cx. Differences in infection rates in the same mosquito species from different regions could be connected with ecological factors, such as season, climate and geographical features, which are specific for each region [ 27 ], but also, perhaps to an even greater extent as shown by our results with Ae.

When comparing the total infection of mosquitoes with D. On the Black Sea coast of the Caucasus Fig. Temperature is an important factor for the maintenance of dirofilariasis foci. However, the presence of definitive hosts mainly domestic, office and stray dogs basically determines one or another level of mosquito infection with Dirofilaria. However, in the settlements Fig. Possible reasons for this are that circulation of the pathogen in the two woodlands does not occur, or wild canines are not affected by Dirofilaria or are affected to such a small extent that we could not discern infectionby examining the mosquito vectors.

In the Moscow region, one point was studied in the immediate vicinity of the dog kennel Fig. Infected mosquitoes were not found. In this kennel, the dogs were treated for different infections, including Dirofilaria , and the infection from wild animals did not occur or was extremely low. According to our findings, under similar conditions temperature and the presence of definitive hosts , the effectiveness of mosquitoes as vectors of Dirofilaria was not the same. There were five species of mosquitoes, Ae. Absence of infection in Ae sticticus and Ae.

However, of particular interest is the reason for the absence of infection in Ae. Another interesting finding was the absence of infection in Ae. In contrast to our results, it was reported that Ae. The absence of infection in Ae. In four species Ae. Also, it should be highlighted that in three species of mosquitoes Ae. This fact may indicate that mosquitoes could ingest the filariae at different times and repeatedly, and not all nematodes managed to complete the development cycle to become infective larvae and migrate to the front of the body.

Similarly, it cannot be excluded that not all filariae reach the infectious stage due to possible defense mechanisms activated by host cells, such as encapsulation, melanization, and coagulation [ 12 , 21 , 34 ]. However, in all mosquito species, except Ae. According to published research, the development of Dirofilaria to the infective stage L3 was recorded in Europe in the mosquito species Ae. On the basis of our results, eleven mosquito species are epidemiologically dangerous, when Dirofilaria undergo development to L3 Table 2.

Of particular interest are the species Ae. Aegypti, Ae. It should be noted that the efficacy of Ae. In seven mosquito species, the host effectiveness was less than 1 Table 2.

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Most mosquito species uninfected with Wolbachia showed higher epidemiological potential for Dirofilaria transmission in all studied regions host effectiveness 0. Dirofilaria DNA was detected in abdomen pools of both Wolbachia -infected and uninfected mosquitoes. This result shows that Wolbachia does not prevent the acquisition of Dirofilaria by mosquitoes in nature. However, in eight thorax-head pools, D. Moreover, after individual study of 11 thorax-heads from two Wolbachia positive Cq. We could not study mosquitoes from these two pools individually, so it is impossible to determine whether all the individuals in pool were infected with the bacterium, and to what ecological form f.

Therefore, our findings do not prove a clear influence of bacteria on the development of Dirofilaria. Nevertheless, the ratio of Dirofilaria -infective mosquitoes is much higher in Wolbachia -free mosquito specimens than in Wolbachia -infected, Differences in the effects of different strains of Wolbachia were not recorded. However, given the small sample size of Dirofilaria -infected mosquitoes, further investigation into whether Wolbachia is present in individual Cx.

In contrast, it has been shown that native Wolbachia does not affect the induction of host immune pathways [ 17 , 39 ].


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As a hypothesis, it could be proposed that there is a resource competition in the host for metabolites, because both Dirofilaria [ 19 , 30 ] and Wolbachia [ 68 ] require them for their development. It should be noted that any Wolbachia anti-pathogen effect is dependent on bacterial density [ 40 ], so the development of microfilaria to the infective stage may differ in each mosquito. The study of simultaneous infection of individual mosquitoes with Dirofilaria spp. In conclusion, Dirofilaria were found in 15 mosquito species.

This is the first study conducted in Russia examining the mosquito species as potential vectors of D. Out of pools studied, there were positive abdomen pools and 34 positive thorax-head pools. However, the only management system was showing a significant association with strongyle infection rate. The percentage reduction of faecal egg count for ivermectin and fenbendazole was Based on the result, it can be concluded that ivermectin is suspected for the development of resistance against intestinal strongyle nematode.

From the analysis of percentage reduction of faecal egg counts, fenbendazole was found to be under the resistance level of status. From the analysis, ivermectin treated horses recorded significantly lower mean egg count than fenbendazole treated and untreated control groups of horses. Fenbendazole treated horses also showed significantly lower egg output than untreated groups after treatment Figure 1. The result of the questionnaire survey in this study focused on probing internal parasite control and management practices of horse owners and the parasite resistance problem.

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It is likely to studies done in Germany [ 25 ], UK [ 26 ] and Denmark [ 27 ]. The majority of This could be associated with the fact that animals with access to grazing are more exposed to strongyle nematode larvae than indoor animals, which agreed with the study done by Lind et al. Given this possible bias and other responses about the methods used to estimate body weights, it appears that this practice may be a cause of the incorrect dosage of anthelmintics, which may lead to increased parasitic resistance.

This is supported by the report of Brady and Nichols [ 5 ]. In this attempt, the overall prevalence of strongyle nematode infection in horses was found to be This is in accordance with the finding of Samuel et al. However, our finding is lower than the work of Alemayehu and Etaferahu [ 30 ] who reported The lower prevalence in this study could be due to the fact that study horses were cart horses which have less exposure to the nematode larvae in the field and in some cases horses have been totally restricted from grazing. Moreover, this may be due to the sample size, study type, and season of the year when the study was conducted.

Consequently, the FECR test showed that the anthelmintic resistance was developed and suspected for fenbendazole and ivermectin, respectively. According to Coles et al. If only one of the two criteria is met, resistance is suspected. There has been no available information about anthelmintic resistance of nematodes in equines in Ethiopia.

Most research works regarding anthelmintic resistance and efficacy for GIT nematodes in Ethiopia have been concerned in small ruminants. The resistance of nematode observed in the present study on fenbendazole might be due to the prolonged, frequent, and irrational use and improper dosage. The present finding supports the reports from European countries by Wirtherle et al. This may be due to frequent usage, species of the parasite, and poor management system. This report is in agreement with a field study done by Lind et al. In contrast to the present study, studies carried out in Romania by Traversa et al.

They reported that horses have been dewormed once per year or less or never. This may probably be the reason why the resistance against FBZ was not found in these reports. Hence, the result indicated that ivermectin is suspected for the development of resistance against intestinal strongyle nematode. This finding is in agreement with a number of previous publications from farm horses, in Germany [ 35 ] and in USA [ 12 ].

They reported that reduction of activity of ivermectin and moxidectin against small strongyles seems to be due to the survival of some of the luminal immature stages in the large intestines after treatment. In the present study, based on the analysis, ivermectin resistance has been suspected. This is inconsistent with the report of Papadopoulos et al.

This was due to the fact that the monitoring activity applied on the efficacy of ivermectin against intestinal strongyles was very high.


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This difference in reduced efficacy in this study area may be due to drug usage strategies, biology of the parasite, and the quality of the available anthelmintic drugs. Both fenbendazole and ivermectin were the common anthelmintic drugs used by Gondar town cart horse owners to control parasitic infestation.

However, the current finding indicated that there was a development of fenbendazole resistance, suspecting ivermectin resistance by strongyle nematode of cart horses. Therefore, based on the above conclusions the following recommendations are forwarded. The authors declare that there is no conflict of interests regarding the publication of this paper. BioMed Research International. Indexed in Science Citation Index Expanded. Journal Menu. Special Issues Menu. Subscribe to Table of Contents Alerts. Table of Contents Alerts. Abstract A study was conducted from November to April to determine fenbendazole and ivermectin resistance status of intestinal nematodes of cart horses in Gondar, Northwest Ethiopia.

Introduction Gastrointestinal helminth parasite infection is a major militating factor against profitable animal production in the world over [ 1 ]. Materials and Methods 2. Study Population and Sampling Technique The study was conducted on cart horses using simple random sampling technique. Experimental Design and Methodology A field experimental study design was conducted to assess the anthelmintic resistance of strongyle nematodes of horses to ivermectin and fenbendazole in Gondar town.

Sample Collection and Sampling Procedures Faecal samples were collected directly from the rectum and sometimes freshly voided faeces from selected animals using gloves before and after treatment. Anthelmintic Resistance Test Cart horses aged from 6 years to 12 years and these animals which transport both human and materials were selected to determine the anthelmintic resistance of intestinal strongyle nematodes of horses against ivermectin and fenbendazole drugs.

Table 2: Pre- and posttreatment fecal egg count, standard deviation, and percent reduction in cart horses. References U. Andersen, D. Howe, S. Olsen, and M. Wannas, K. Dawood, and Gh. View at Google Scholar I. Martins, G. Verocai, T. Correia et al. Umur and M. Brady and W. Wolstenholme, I. Fairweather, R. Prichard, G. Von Samson-Himmelstjerna, and N. Getachew, A. Trawford, G. Feseha, and S. Ademola, B. Fagbemi, and O. Nielsen, K. Baptiste, S. Tolliver, S. Collins, and E. Lyons, S. Tolliver, M. Ionita, A.

Lewellen, and S. Trawford, F. Burden, and J. Craven, H. Barnes, S. Henriksen, and P. Zajac and G. Sultan, G. Ayele, B. Tadesse, and A. Reed, M. Bbayly, and C. Saari and S. View at Google Scholar G. Coles, C. Bauer, F. Borgsteede et al. Lester and J. Lassen and S. Hinney, N. Wirtherle, M. Kyule, N. Miethe, K. Zessin, and P.

Relf, H. Lester, E. Morgan, J. Hodgkinson, and J.