Cited by 47Parasitic Diseases Research and TreatmentMosquito-borne diseases and controlVector-borne infectious diseases

Dirofilaria and Wolbachia in mosquitoes (Diptera: Culicidae) in central European Russia and on the Black Sea coast

Open access
Shaikevich, Elena, Bogacheva, Anna, Ganushkina, Ludmila·2019·Parasite

Abstract

Dirofilariasis is endemic in Russia, as well as in many other European countries. The aim of this study was to assess the ability of mosquitoes to transfer Dirofilaria immitis and Dirofilaria repens in regions with temperate and subtropical climates. The possible impact of the symbiotic bacterium Wolbachia on Dirofilaria transmission was also investigated. 5333 female mosquitoes were collected at 11 points in central European Russia and on the Black Sea coast during the period 2013–2017. Out of 20 mosquito species examined, 14 were infected with D. repens and 13 with D. immitis. Both species of Dirofilaria were found in different climatic regions. The total Dirofilaria spp. estimated infection rate (EIR) in the central part of Russia varied from 3.1% to 3.7% and, in the southern region, from 1.1% to 3.0%. The highest estimated infection rate was found in Anopheles messeae, the lowest in Culex pipiens. The greatest epidemiological danger was represented by Aedes aegypti, Ae. geniculatus, An. messeae and Ae. communis. Six out of 20 mosquito species were infected with Wolbachia. Pools of Aedes albopictus, Cx. pipiens and Coquillettidia richiardii were simultaneously infected with Dirofilaria and Wolbachia. 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.

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Written from the paper’s full text.

TL;DR

This study screened 5,333 female mosquitoes from central European Russia and the Black Sea coast for Dirofilaria and Wolbachia, finding Dirofilaria in 15 of 20 mosquito species and Wolbachia in 6 of 20. The authors conclude that mosquitoes naturally uninfected with Wolbachia may have higher potential to transmit Dirofilaria than Wolbachia-infected species.

Key findings

  • Among 20 mosquito species examined, 14 were infected with *D. repens* and 13 with *D. immitis*; total *Dirofilaria* spp. EIR was 2.71 (95% CI 2.18–3.03). The abstract reports total *Dirofilaria* spp. EIR of 3.1%–3.7% in central Russia and 1.1%–3.0% in the southern region.
  • Highest EIRs were in *An. messeae* (8.67), *Ae. aegypti* (5.33), *Ae. geniculatus* (4.85), and *Ae. cataphylla* (4.12); the lowest was in *Cx. pipiens* (1.39 total EIR). The greatest epidemiological danger was attributed to *Ae. aegypti*, *Ae. geniculatus*, *An. messeae*, and *Ae. communis*.
  • Wolbachia was found in 6 of 20 species: 93% of tested *Cx. pipiens*, 68% of *Cq. richiardii*, 56% of *Ae. albopictus*, 37% of *Ae. cinereus*, 7% of *Cx. modestus*, and 3% of *Ae. cantans*. Pools of *Ae. albopictus*, *Cx. pipiens*, and *Cq. richiardii* were simultaneously infected with *Dirofilaria* and Wolbachia.
  • After individual checking, no development of *Dirofilaria* to the infective larval stage was found in specimens infected with Wolbachia; 22 *Dirofilaria*-infective pools were Wolbachia-free and only two mosquito pools were Wolbachia-infected.

Methods

  • Female mosquitoes were collected at 11 points in the Tula, Nizhniy Novgorod, and Moscow regions and on the Black Sea coast (Anapa, Tuapse, Sochi, and “Priboi”) during 2013–2017 in central Russia and in 2012–2013 and 2016 in the south.
  • A total of 5,333 females were grouped into 1,095 pools, usually up to five or six specimens; thorax-head and abdomen were dissected separately. PCR was used to detect *D. immitis* and *D. repens*; Wolbachia was screened in a sub-sample of 2,926 individuals (633 pools) using *wsp*-specific PCR, sequencing, and strain typing.
  • Minimum infection rates and estimated infection rates (EIRs) were calculated, with 95% CIs by the modified Wald method; host effectiveness was calculated as the number of infectious mosquito pools with L3 larvae divided by the total number of mosquitoes studied × 100.

Limitations

  • The paper states that the sample size of *Dirofilaria*-infected mosquitoes was small, that some pools could not be studied individually, and that the findings do not prove a clear influence of Wolbachia on *Dirofilaria* development; further investigation is required.
  • The paper notes that absence of infection in some species may be associated with small sample size, including *Ae. sticticus*, *Ae. punctor*, and *Cx. torrentium*.
  • Evident from the text: Wolbachia screening covered only a sub-sample of 2,926 individuals, and field collection by human landing may not represent all mosquito species equally.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1051/parasite/2019002

Cites

72 of 72 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 51 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Both species of Dirofilaria were found in different climatic regions.

    “Both species of Dirofilaria were found in different climatic regions.”
    Quote in the paperSubstantial claim
  • Findingown data

    Pools of Aedes albopictus, Cx. pipiens and Coquillettidia richiardii were simultaneously infected with Dirofilaria and Wolbachia.

    “Pools of Aedes albopictus, Cx. pipiens and Coquillettidia richiardii were simultaneously infected with Dirofilaria and Wolbachia.”
    Quote in the paperSubstantial claim
  • Findingown data

    Six out of 20 mosquito species were infected with Wolbachia.

    “Six out of 20 mosquito species were infected with Wolbachia.”
    Quote in the paperSubstantial claim
  • Findingown data

    After checking mosquitoes individually, there was no development of Dirofilaria to the infective larval stage in specimens infected with Wolbachia.

    “After checking mosquitoes individually, it was found that there was no development of Dirofilaria to the infective larval stage in specimens infected with Wolbachia.”
    Quote in the paperSubstantial claim
  • Findingown data

    The host effectiveness of Ae. communis was 1.3.

    “Ae. intrudens and Ae. communis host effectiveness was 0.41 and 1.3, respectively.”
    Quote in the paperNot a substantial claim
  • May combine two claims. 45
  • Classified as probably not a substantial claim. 13
  • May combine two claims.

    Findingown data

    The highest estimated infection rate was found in Anopheles messeae, the lowest in Culex pipiens.

    “The highest estimated infection rate was found in Anopheles messeae, the lowest in Culex pipiens.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Twenty-two Dirofilaria-infective pools were Wolbachia-free and only two mosquito pools were Wolbachia-infected.

    “Twenty-two Dirofilaria-infective pools were Wolbachia-free and only two mosquito pools were Wolbachia-infected.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Out of 20 mosquito species examined, 14 were infected with D. repens and 13 with D. immitis.

    “Out of 20 mosquito species examined, 14 were infected with D. repens and 13 with D. immitis.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The total Dirofilaria spp. estimated infection rate (EIR) in the central part of Russia varied from 3.1% to 3.7% and, in the southern region, from 1.1% to 3.0%.

    “The total Dirofilaria spp. estimated infection rate (EIR) in the central part of Russia varied from 3.1% to 3.7% and, in the southern region, from 1.1% to 3.0%.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The development of D. immitis to the infective stage (L3) was successful only in one thorax-head of Wolbachia-free Cq. richiardii (No. 11'-1, SM4), although a pool of five mosquito abdomens gave a positive signal for both D. repens and D. immitis.

    “The development of D. immitis to the infective stage (L3) was successful only in one thorax-head of Wolbachia-free Cq. richiardii (No. 11’-1, SM4), although a pool of five mosquito abdomens gave a positive signal for both D. repens and D. immitis.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    D. repens was found in 4.66% of tested abdomen pools and in 1.74% of tested thorax-head pools.

    “D. repens was found in 4.66% of tested abdomen pools and in 1.74% of tested thorax-head pools.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Both Dirofilaria species were found in one pool of Ae. cantans (twice), Ae. geniculatus (once), Cx. pipiens (once), Ae. intrudens (once) and Cq. richiardii (once).

    “Both Dirofilaria species were found in one pool of Ae. cantans (twice), Ae. geniculatus (once), Cx. pipiens (once), Ae. intrudens (once) and Cq. richiardii (once).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The highest EIR values occurred with the species An. messeae, Ae. aegypti, Ae. geniculatus and Ae. cataphylla, and were estimated as 8.67, 5.33, 4.85 and 4.12, respectively.

    “The highest EIR values occurred with the species An. messeae, Ae. aegypti, Ae. geniculatus and Ae. cataphylla, and were estimated as 8.67, 5.33, 4.85 and 4.12, respectively (Table 2).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    In the subtropical climate on the Black Sea coast, the most abundant sampled mosquito species was Ae. albopictus, followed by Cx. pipiens and Cx. modestus.

    “In the subtropical climate on the Black Sea coast, the most abundant sampled mosquito species was Ae. albopictus, followed by Cx. pipiens and Cx. modestus (Table 1).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Two Wolbachia strains were present in studied Ae. albopictus (wAlbA and wAlbB), wPip-II in Cx. pipiens f. pipiens and wPip-IV in Cx. pipiens f. molestus.

    “Two Wolbachia strains were present in studied Ae. albopictus (wAlbA and wAlbB), wPip-II in Cx. pipiens f. pipiens and wPip-IV in Cx. pipiens f. molestus.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    D. repens infected 14 of 15 mosquito species (EIR = 1.17, 61 positive pools) and D. immitis 13 species (EIR = 1.47, 76 positive pools).

    “D. repens infected 14 of 15 mosquito species (EIR = 1.17, 61 positive pools) and D. immitis 13 species (EIR = 1.47, 76 positive pools).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The collected mosquitoes included 20 species; 16 species were in the central part of Russia and seven species on the Black Sea coast.

    “The collected mosquitoes included 20 species; 16 species were in the central part of Russia and seven species on the Black Sea coast.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    D. immitis DNA was detected in 5.75% of tested abdomen pools and 1.37% of tested thorax-head pools.

    “If we compare infection in the abdomen with the thorax-head, D. immitis DNA was detected in 5.75% of tested abdomen pools and 1.37% of tested thorax-head pools.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    At the recreation center "Priboi", D. repens had an EIR of 0.99 and D. immitis 2.04; this is comparable to values in the central regions of Russia.

    “However, at the recreation center “Priboi” (Fig. 1 #11), D. repens had an EIR of 0.99 and D. immitis 2.04; this is comparable to values in the central regions of Russia (Fig. 1).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    93% of all tested Cx. pipiens were infected with Wolbachia, followed by Cq. richiardii (68%), Ae. albopictus (56%), Ae. cinereus (37%), Cx. modestus (7%) and Ae. cantans (3%).

    “93% of all tested Cx. pipiens were infected with Wolbachia, followed by Cq. richiardii (68%), Ae. albopictus (56%), Ae. cinereus (37%), Cx. modestus (7%) and Ae. cantans (3%).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Filarial DNA was found in 15 species belonging to four genera with the total EIR for both Dirofilaria infections calculated as 2.71 (95% CI, 2.18-3.03).

    “Filarial DNA was found in 15 species belonging to four genera with the total EIR for both Dirofilaria infections calculated as 2.71 (95% CI, 2.18–3.03) (Table 2).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In the Moscow region, the EIR for D. repens was 1.63 and for D. immitis 1.97.

    “In the Moscow region (Fig. 1 #6, 7), the EIR for D. repens was 1.63 and for D. immitis 1.97”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Dirofilaria was found in 22 thorax-head pools of mosquitoes uninfected with Wolbachia and in two thorax-head pools which were positive for Wolbachia.

    “Dirofilaria was found in 22 thorax-head pools of mosquitoes uninfected with Wolbachia and in two thorax-head pools which were positive for Wolbachia.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The first infected mosquitoes were recorded in May and the last in August-September.

    “The first infected mosquitoes were recorded in May and the last in August–September.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    At the resorts of the Caucasian Black Sea coast, in Anapa, Tuapse and Sochi, the rates of mosquito infection were much lower; EIR values were 0.32 for D. repens and 0.81 for D. immitis.

    “At the resorts of the Caucasian Black Sea coast, in Anapa, Tuapse and Sochi (Fig. 1 #8, 9, 10), the rates of mosquito infection were much lower; EIR values were 0.32 for D. repens and 0.81 for D. immitis.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Based on the wsp gene sequence, Wolbachia strains in Cq. richiardii, Ae. cinereus and Ae. cantans differ from wAlb and wPip, so we named these wCrich, wAcin and wOcan, respectively.

    “Based on the wsp gene sequence, Wolbachia strains in Cq. richiardii, Ae. cinereus and Ae. cantans differ from wAlb and wPip, so we named these wCrich, wAcin and wOcan, respectively (pubmlst.org/wolbachia).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    In the Nizhny Novgorod region, EIRs for D. repens and D. immitis were 1.23 and 1.92, respectively.

    “In the Nizhny Novgorod region (Fig. 1 #3), EIRs for D. repens and D. immitis were 1.23 and 1.92, respectively.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    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.

    “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).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Neither D. immitis nor D. repens were found in other individual thorax-heads; parasites were found only in pooled abdomens.

    “Neither D. immitis nor D. repens were found in other individual thorax-heads; parasites were found only in pooled abdomens.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In our samples, both Cx. modestus and Ae. geniculatus were infected not only with D. repens but also with D. immitis.

    “The difference is that in our samples, both mosquito species were infected, not only with D. repens, but also with D. immitis.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    Differences in the effects of different strains of Wolbachia were not recorded.

    “Differences in the effects of different strains of Wolbachia were not recorded.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Ae. diantaeus, mainly collected in the Nizhny Novgorod region, were not infected, while other mosquito species of the same biotope were infected.

    “Another interesting finding was the absence of infection in Ae. diantaeus, which were mainly collected in the Nizhny Novgorod region, where other mosquito species of the same biotope were infected (SM2).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    When comparing total infection by region, almost identical EIR results in settlements of the Central region were noted, with some prevalence of mosquitoes infected with D. immitis.

    “When comparing the total infection of mosquitoes with D. repens and D. immitis by region (SM2), almost identical EIR results in the settlements of the Central region were noted, with some prevalence of mosquitoes infected with D. immitis.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Ae. diantaeus and Ae. caspius were collected in sufficient numbers (117 and 146 mosquitoes) and not in natural forests.

    “However, of particular interest is the reason for the absence of infection in Ae. diantaeus and Ae. caspius, which were collected in sufficient numbers (117 and 146 mosquitoes) and not in the natural forests.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    D. repens DNA in thorax-heads was found in 14 Wolbachia-uninfected and in only two Wolbachia-infected pools, in one of Ae. albopictus and in one of Cx. pipiens.

    “D. repens DNA in thorax-heads was found in 14 Wolbachia-uninfected and in only two Wolbachia-infected pools, in one of Ae. albopictus and in one of Cx. pipiens.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingreasoning

    On the Black Sea coast of the Caucasus, mosquitoes were collected in a resort area where the number of dogs near sample sites was negligible and mosquito infection was lower.

    “On the Black Sea coast of the Caucasus (Fig. 1 #8, 9, 10), mosquitoes were collected in a resort area where the number of dogs near our sample sites was negligible and the infection of mosquitoes was lower.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Out of 1095 pools studied, there were 114 positive abdomen pools and 34 positive thorax-head pools.

    “Out of 1095 pools studied, there were 114 positive abdomen pools and 34 positive thorax-head pools.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Wolbachia pipientis infects filarial nematodes and many insects, including some mosquito species.

    “An endosymbiotic, maternally inherited bacterium, Wolbachia pipientis (Rickettsiales: Rickettsiaceae), hereafter Wolbachia, infects filarial nematodes and many insects, including some mosquito species.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [61] Taylor, 2013, Cellular Microbiology source

      Not checked in the free run.

    • cites [65] Werren, 2008, Nature Reviews. Microbiology source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Prior to 2014, D. repens infection was detected in 850 people living permanently in 42 regions of the Russian Federation.

    “Prior to 2014, D. repens infection was detected in 850 people living permanently in 42 regions of the Russian Federation [54].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [54] Sergiev, 2014, Meditsinskaia parazitologiia i parazitarnye bolezni

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The season for Dirofilaria transmission in the central part of Russia begins in late May to early June.

    “The season for Dirofilaria transmission in the central part of Russia begins in late May to early June [26].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Ganushkina, 2014, Meditsinskaia Parazitologiia i Parazitarnye Bolezni (Mosk)

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    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 1.0%-14.0%.

    “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 1.0%–14.0% [2, 24, 35].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [2] Arakeljan, 2008, Siberian Medical Journal

      Not checked in the free run.

    • cites [24] Ermakova, 2014, International Journal of Infectious Diseases source

      Not checked in the free run.

    • cites [35] Krivorotova, 2016, Parazitologiia

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The first case of D. immitis was detected in 2015 in the Moscow region; an immature female was removed from a 14-month-old child.

    “The first case of D. immitis was detected in 2015 in the Moscow region; an immature female was removed from a 14-month-old child [63].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [63] Tumolskaya, 2016, Parasite source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    D. immitis and D. repens have been detected in the Culex, Aedes and Anopheles genera and the EIR was established as 1.9%-7.0%, 2.3%-6.7%, and 0.6%-3.4%, respectively.

    “D. immitis and D. repens have been detected in the Culex, Aedes and Anopheles genera and the EIR was established as 1.9%–7.0%, 2.3%–6.7%, and 0.6%–3.4%, respectively [2, 24, 35].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [2] Arakeljan, 2008, Siberian Medical Journal

      Not checked in the free run.

    • cites [24] Ermakova, 2014, International Journal of Infectious Diseases source

      Not checked in the free run.

    • cites [35] Krivorotova, 2016, Parazitologiia

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The dirofilariasis zone in the north of the European part of Russia has advanced to 58° N.

    “The dirofilariasis zone in the north of the European part of Russia has advanced to 58° N [4, 10].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [4] Barashkova, 2011, Journal Infectology

      Not checked in the free run.

    • cites [10] Byakova, 2014, Basic Research

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Dirofilaria immitis and Dirofilaria repens are transmitted by culicid mosquito species belonging to the Culex, Aedes, Ochlerotatus, Anopheles, Coquillettidia, Armigeres and Psorophora genera.

    “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].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [42] Mckay, 2013, Journal of Medical Entomology source

      Not checked in the free run.

    • cites [58] Sulesco, 2016, Parasites & Vectors source

      Not checked in the free run.

    • cites [69] Yildirim, 2011, Veterinary Parasitology source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Development of Dirofilaria 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.

    “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].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [18] Castillo, 2011, Trends in Parasitology source

      Not checked in the free run.

    • cites [34] Kartman, 1953, Experimental Parasitology source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Culex pipiens f. molestus from Madeira, Portugal was unable to support the full development of D. immitis, both in nature and after experimental infection with D. immitis.

    “However, it was found that Culex pipiens f. molestus from Madeira, Portugal was unable to support the full development of D. immitis, both in nature and after experimental infection with D. immitis [29].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [29] Gouveia M. 2007. Susceptibility of Mosquito Vectors to Dirofilaria immitis on Madeira Island, Portugal. Tese Doutoramenteo Universidade da Madeira. Funchal, Portugal: Universidade da Madeira. 113 p. hdl.handle.net/10400.13/27.

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Among the culicid mosquito species, Culex pipiens, Cx. quinquefasciatus and Ae. albopictus are known to be infected with Wolbachia and considered as vectors for Dirofilaria.

    “Among the culicid mosquito species, Culex pipiens, Cx. quinquefasciatus and Ae. albopictus are known to be infected with Wolbachia [32, 67] and considered as vectors for Dirofilaria [13–15, 28, 45, 50, 69].”
    Quote in the paperNot a substantial claim0 of 9 sources checked
    • cites [32] Hertig, 1924, Journal of Medical Research

      Not checked in the free run.

    • cites [67] Wright, 1980, Journal of Ultrastructure Research source

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    • cites [13] Cancrini, 2003b, Medical and Veterinary Entomology source

      Not checked in the free run.

    • cites [14] Cancrini, 2006, Journal of Medical Entomology source

      Not checked in the free run.

    • cites [15] Cancrini G, Gabrielli S. 2007. Vectors of Dirofilaria nematodes: biology, behaviour and host/parasite relationships, in Dirofilaria immitis and D. repens in dog and cat and human infections, Genchi C, Rinaldi L, Cringoli G, Editors. Veterinary Parasitology and Parasitic Diseases, Department of Pathology and Animal Health, Faculty of Veterinary Medicine, University of Naples Federico II: Napoli, NA, Italy. p. 48–58. ISBN 9788889132142.

      Not checked in the free run.

    • cites [28] Giangaspero, 2013, Parasitology Research source

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    • cites [45] Morchón, 2007, Vector Borne and Zoonotic Disease source

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    • cites [50] Paras, 2014, Medical and Veterinary Entomology source

      Not checked in the free run.

    • cites [69] Yildirim, 2011, Veterinary Parasitology source

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  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    D. immitis microfilariae development to the L3 stage has recently been found in the thorax-head of one Cx. pipiens f. pipiens from Spain.

    “However, D. immitis microfilariae development to the L3 stage has recently been found in the thorax-head of one Cx. pipiens f. pipiens from Spain [9].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Bravo-Barriga, 2016, Veterinary Parasitology source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In continental Portugal, Cx. pipiens were found to be infected with D. immitis, but were not potentially infective; filarial DNA was detected only in the abdomen and not in thorax-head samples.

    “In continental Portugal, Cx. pipiens were found to be infected with D. immitis, but were not potentially infective; filarial DNA was detected only in the abdomen and not in thorax-head samples [25].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Ferreira, 2015, Parasites & Vectors source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The simultaneous presence of Dirofilaria signals in thorax-head and abdomen pools may indicate that mosquitoes could ingest filariae at different times and repeatedly, and not all nematodes completed development to infective larvae and migrated to the front of the body.

    “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.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Artificial bacterial transfer significantly increases the expression of immune genes, including those involved in the Toll and IMD immune pathways, enhances the mosquito's resistance to pathogens, and inhibits the development of filarial nematodes.

    “It is known that artificial bacterial transfer significantly increases the expression of immune genes, including those involved in the Toll and IMD immune pathways, enhances the mosquito’s resistance to pathogens [5, 48, 49], and inhibits the development of filarial nematodes [1, 33].”
    Quote in the paperSubstantial claim0 of 5 sources checked
    • cites [5] Bian, 2013, Science source

      Not checked in the free run.

    • cites [48] Pan, 2012, Proceedings of the National Academy of Sciences source

      Not checked in the free run.

    • cites [49] Pan, 2018, ISME Journal source

      Not checked in the free run.

    • cites [1] Andrews, 2012, PLoS Pathogens source

      Not checked in the free run.

    • cites [33] Kambris, 2009, Science (New York, NY) source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    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, and with sample size.

    “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. aegypti, Ae. cantans and Ae. vexans, connected with the sample size.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27] Genchi, 2009, Veterinary Parasitology source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The greatest epidemiological danger was represented by An. messeae, Ae. aegypti, Ae. geniculatus, and Ae. communis.

    “The greatest epidemiological danger was represented by An. messeae, Ae. aegypti, Ae. geniculatus, and Ae. communis.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    This is the first study conducted in Russia examining mosquito species as potential vectors of D. immitis and D. repens.

    “This is the first study conducted in Russia examining the mosquito species as potential vectors of D. immitis and D. repens.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    Any Wolbachia anti-pathogen effect is dependent on bacterial density, so the development of microfilaria to the infective stage may differ in each mosquito.

    “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.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [40] Lu, 2012, PLoS Neglected Tropical Diseases source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Our data showed that Ae. albopictus and Culex pipiens s.l. are not the most important vectors of Dirofilaria.

    “Our data showed that Ae. albopictus and Culex pipiens s.l. are not the most important vectors of Dirofilaria.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    For the first time in Europe, Ae. aegypti, Ae. intrudens and Ae. communis mosquitoes have been studied as Dirofilaria vectors, with EIR values ranging from 3.08 to 5.33.

    “For the first time in Europe, Ae. aegypti, Ae. intrudens and Ae. communis mosquitoes have been studied as Dirofilaria vectors, in which EIR values ranged from 3.08 to 5.33.”
    Quote in the paperSubstantial claim
53 of 53
  • The paper relies on this without support.

    Many areas in Russia have not been sufficiently studied for dirofilariasis and mosquito vectors.

    “Even though dirofilariasis is a concern in Russia, many areas have not been sufficiently studied.”
  • The paper relies on this without support.

    There are no data on the species of mosquito that are potential vectors of dirofilarial worms.

    “Also, there are no data on the species of mosquito that are potential vectors of dirofilarial worms.”
  • The paper relies on this without support.

    The infection of natural populations of Ae. aegypti has not been studied.

    “As far as we know, the infection of natural populations of Ae. aegypti has not been studied.”
  • The paper relies on this without support.

    Temperature is an important factor for the maintenance of dirofilariasis foci.

    “Temperature is an important factor for the maintenance of dirofilariasis foci.”
  • The paper relies on this without support.

    Cx. torrentium rarely attack people.

    “Cx. torrentium rarely attack people, and with our collection method, the sample size was only three mosquitoes.”
5 of 5

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Climate change, among other factors, has surely played an important role in the appearance of competent vectors in new regions and countries where their presence had not previously been reported.

    “In addition, climate change (among other factors) has surely played an important role in the appearance of competent vectors in new regions and countries where their presence had not previously been reported [159,162,163].”
  • In Russia, estimated infection rates of D. immitis in mosquitoes varied from 3.1 to 3.7% in the central part and from 1.1 to 3.0% in the southern region.

    “In Russia, Shaikevich et al. [163] estimated that the infection rates in mosquitoes from the central part of Russia varied from 3.1 to 3.7% and, in the southern region, from 1.1 to 3.0%.”
  • The highest infection rate with D. immitis and D. repens was detected in Cx. pipiens s.l. mosquitoes (MIR = 0.6%, EIR = 0.6%), followed by Oc. caspius (MIR and EIR ranged from 0.1 to 0.4%).

    “The highest infection rate with D. immitis and D. repens was detected in Cx. pipiens s.l. mosquitoes (MIR = 0.6%, EIR = 0.6%) followed by Oc. caspius (MIR and EIR ranged from 0.1 to 0.4%), as already documented in central European Russia, Germany, Italy, Turkey and the Republic of Belarus [53].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Ae. cantans D. immitis EIR differs between tables

    Major

    Table 2 gives the D. immitis EIR for Ae. cantans as 1.9, whereas Table 4 gives 1.39 for the same study and species. The discussion also states 1.39.

  • Ae. albopictus is not among the lowest-infection species

    Minor

    The text names Ae. albopictus among the species with the lowest infection, but Table 2 gives it a total EIR of 1.69, above Ae. excrucians at 1.51 and Ae. leucomelas at 1.66.

  • Table 3 does not account for 90 Dirofilaria-positive pools

    Minor

    The stated 90 positive pools exceed the table's 48 D. repens-positive plus 41 D. immitis-positive pools. Even with no overlap, those columns account for at most 89 distinct positive pools.

  • Collection period excludes mosquitoes collected in 2012

    Minor

    The abstract says all 5333 mosquitoes were collected during 2013-2017, but the methods say southern collections included 2012.

  • Thorax-head positives are not always fewer than abdomen positives

    Minor

    The text makes this claim for every species except Ae. aegypti, but Table 2 lists three D. immitis-positive thorax-head pools and only two positive abdomen pools for Ae. geniculatus.

5 of 5

Cites

Flagged first, then by citations

Research works printed but not linked: 11

  1. Arakeljan, 2008, Siberian Medical Journal, 7, 13
  2. Barashkova, 2011, Journal Infectology, 3, 108
  3. Byakova, 2014, Basic Research, 11, 1297
  4. De Carvalho, 2018, Journal of Arthropod-Borne Diseases, 12, 94
  5. Ganushkina, 2014, Meditsinskaia Parazitologiia i Parazitarnye Bolezni (Mosk), 3, 9
  6. Krivorotova, 2016, Parazitologiia, 50, 357
  7. Masetti, 2008, New Microbiolica, 31, 457
  8. Ryabova, 2005, Meditsinskaia parazitologiia i parazitarnye bolezni, 3, 3
  9. Sergiev, 2014, Meditsinskaia parazitologiia i parazitarnye bolezni, 3, 3
  10. Shaikevich, 2007, European Mosquito Bulletin, 23, 25
  11. Tiawsirisup, 2006, Southeast Asian Journal of Tropical Medicine and Public Health, 37, 110

Cited by

Sorted by citations

Authors
Shaikevich, E., Bogacheva, A., & Ganushkina, L.
Affiliations
Lomonosov Moscow State University (RU)
Venue
Parasite
Publisher
EDP Sciences
Published
2019
Volume
26
Pages
2
ISSN
  • 1252-607X (ISSN-L)
  • 1776-1042
OpenAlex
W2909849611
Cited by
47
References
72
Citations by year
2026: 4 · 2025: 1 · 2024: 8 · 2023: 7 · 2022: 10 · 2021: 5 · 2020: 10 · 2019: 1 · 2018: 1
FWCI
4.98
Type
journal article
Language
en
Open access
Locations
  • Parasite (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, cc-by)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
  • Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
Keywords
Dirofilaria immitis, Dirofilaria repens, dirofilariasis, mosquitoes, Wolbachia, mosquito-borne transmission, Anopheles messeae, Culex pipiens, Aedes aegypti, Aedes geniculatus, Aedes communis, Coquillettidia richardii, Aedes albopictus, infection rate, Central European Russia, Black Sea coast
MeSH terms
Mosquito Vectors, Animals, Culex, Dirofilaria immitis, Dirofilariasis, Dog Diseases, Dogs, Female, Larva, Culicidae, Russia, Symbiosis, DNA, Helminth, Wolbachia, Black Sea, Dirofilaria repens

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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