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Prevalence of Dirofilaria immitis in mosquitoes (Diptera) – systematic review and meta-analysis

Seyed Mohammad Riahi
Seyed Mohammad Riahi
, 
Mustapha Ahmed Yusuf
Mustapha Ahmed Yusuf
, 
Shahyad Azari-Hamidian
Shahyad Azari-Hamidian
 oraz 
Rahmat Solgi
Rahmat Solgi
   | 01 sty 2021
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Data publikacji: 01 sty 2021
Zakres stron: 1 - 13
DOI: https://doi.org/10.21307/jofnem-2021-012
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© 2021 Authors, published by Sciendo.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1:

Flow chart detailing the number of studies excluded and included at each step for systematic review of the prevalence of D. immitis infection in Culicidae mosquitoes.
Flow chart detailing the number of studies excluded and included at each step for systematic review of the prevalence of D. immitis infection in Culicidae mosquitoes.

Subgroup meta-analysis of experimental studies reporting Dirofilaria immitis infected and infective rates in vectors grouped by mosquito genus and species.

Minimum infected ratea Minimum infective rateb
Variable Pool size Positive pool Overall prevalence (95% CI) I 2 Positive pool Overall prevalence (95% CI) I 2
Overall 4,512 1,524 379.9 (154.5-636.5) 89.2 251 84.7 (20.5-183.8) 98.8
Method PCR 271 161 649.2 (459.5-817.8) 99.7 44 194.6 (55-388.8) 99.4
Method Dissection 4,241 1,363 253.7 (40.4-565.7) 99.6 207 46.9 (0.9-147) 99.1
Ae. spp. 1,506 905 482.2 (105.2-871.6) 99.6 168 132.4 (17.3-324.2) 98.5
Cx. spp. 2,893 561 61.2 (0.5-197) 98.8 65 55.9 (2.7-163.1) 98.2
An. spp. 90 58 644.4 (536.5-742.6) – 16 177.8 (105.2-274.6) –
Oc. spp. 0 0 0 0 0

Subgroup meta-analysis of field studies reporting pool prevalence Dirofilaria immitis infected/infective rates in vectors grouped by country.

Minimum infected ratea Minimum infective rateb
Variable Pool size Positive pool Overall prevalence (95% CI) I 2c Positive pool Overall prevalence (95% CI) I 2
Global 124,480 1,071 21.9 (14-31.2) 98.6 235 2.6 (1-4.8) 94.4
PAHO 18,690 451 32.4 (13.3-59) 98.2 101 3.8 (0.1-11.1) 95.3
Argentina 2,462 5 0 (0-1.4) 99.9 0 0 (0-0.3) 99.8
Brazil 3,988 56 13.2 (9.8-17.1) 99.9 8 1.4 (0.3-3) 99.8
Mexico 867 32 25 (15.4-36.8) 99.9 21 9.4 (3.7-17.3) 99.8
USA 11,373 358 57.9 (8.1-146.5) 99 72 4 (0-23.4) 96.8
EURO 57,717 240 14.8 (5-28.7) 97.2 71 2.2 (0.1-6.2) 92.9
Italy 3,808 121 30.3 (3.1-80.6) 97.7 30 6.3 (0-20.8) 91.9
Portugal 2,389 58 23.1 (17.4-29.6) 99.5 25 10 (6.3-14.5) 98.4
Slovakia 187 4 14.7 (0.9-39.4) 99.5 0 0 (0-10.2) 98.4
Spain 2,825 4 1.3 (0.2-3.2) 0 1 0.1 (0-1.3) 0
Turkey 613 17 24.5 (12.7-39.3) 5.1 15 21.4 (10.4-35.5) 34.2
Czech 237 0 0 (0-15.4) 0 0 0 (0-15.4) 0
France 797 29 36.4 (24.5-51.8) – 0 0 (0-4.6) –
Germany 955 2 2.1 (0.3-7.5) – 0 0 (0-3.9) –
Russia 78 5 64.1 (21.2-143) – 0 0 (0-46.2) –
Australia 2,389 0 0 (0-0.1) – 0 0 (0-0.1) –
EMRO 190 15 78.9 (44.9-126.9) – 10 52.6 (25.5-94.7) –
Iran 190 15 78.9 (44.9-126.9) – 10 52.6 (25.5-94.7) –
WPRO 47,883 365 25.6 (6.1-57.4) 98.9 53 0.3 (0-2.0) 81.2
French Polynesia 1,194 28 23.5 (15.6-33.7) – 4 3.4 (0.9-8.6) –
Samoa 41,980 179 4.3 (3.7-4.9) – 49 1.2 (0.9-1.5) –
Taiwan 4,537 146 32.2 (27.2-37.7) – 0 0 (0.0-0.8) –
South-Korea 172 12 69.8 (36.6-118.7) – 0 0 (0.0-21.2) –

Subgroup meta-analysis of studies reporting Dirofilaria immitis infected and infective rates in vectors grouped by mosquito genus and species.

Minimum infected ratea Minimum infective rateb
Variable pool size Positive pool Overall prevalence (95% CI) I 2c Q Positive pool Overall prevalence (95% CI) I 2 Q
Total 124,480 1,071 21.86 (14.06-31.1) 98.5 2,475.9 235 2.6 (0.97-4.77) 94.4 622.1
Aedes 62,924 526 29.5 (17.21-46.4) 97.5 1,016.7 138 1.8 (0.03-5.3) 91.6 298.4
Culex 16,652 260 12.36 (5.8-20.88) 92.9 241.8 42 1.28 (0.0-4.04) 83.3 95.6
Anopheles 4,244 157 51.37 (5-133.5) 98.1 372.9 19 3.14 (0.0-12.2) 75.5 28.6
Ochlerotatus 5,382 73 43.29 (0.1-140.6) 96.3 54.9 24 0.97 (0.14-2.27) 0.0 –
Cx. quinciafasiatus 4,892 168 24.7 (7.79-49.4) 92 62.7 13 2.6 (0.0-12.46) 87.6 40.2
Ae. polynesiensis 24,041 198 31.8 (3.5-85.5) 98 100.8 53 1.8 (0.5-3.86) 32.7 2.9
Oc. taeniorhynchus 2,517 44 12.6 (8.42-17.5) 0.0 – 32 4.1 (1.73-7.31) 0.0 –
Oc. sollicitans 2,539 25 0 – – 2 0 – –
Cx. pipiens 5,518 43 6.7 (3.48-10.88) 59.7 19.8 7 0.62 (0-2.29) 48.3 15.5
Ae. ochcaspius 285 14 48.6 (25.81-77.6) 0.0 – 4 10.7 (0.91-27.7) 0.0 –
Ae. vexans 13,439 77 47.1 (1.08-135) 97.6 299.3 30 6.2 (0.0-38.53) 94.0 117.2
Cx. theileri 1,574 43 35.3 (2.06-101.4) 96.2 78.5 25 19.2 (0.06-62.5) 94.5 54.3
Ae. albopictus 2,298 151 49.5 (14.7-101.6) 95.3 169.7 25 3.2 (0.00-15.30) 86.3 58.6

Characteristics of the individual studies included in the meta-analysis based on eligibility criteria.

Country Year of implementation Method Total sample Total pool Total infected pool Total infective pool Quality score References
Brazil 2013 PCR 3115 311 1 0 7 Ogawa et al. (2013)
Mexico 2015 PCR 2618 595 4 0 6 Oswaldo et al. (2018)
USA 2006 PCR 1,922 390 33 0 7 Chambers et al. (2009)
Mexico 2007 Dissection 272 272 28 21 8 Manrique-Saide et al. (2008)
Italy 2012 PCR 40,892 955 21 0 7 Latrofa et al. (2012)
Iran 2005-2011 PCR 190 190 15 10 6 Azari-Hamidian et al. (2009)
USA 2009 PCR 91,798 1,212 184 54 8 Mckay et al. (2013)
Germany 2011-2013 PCR 16,878 955 2 0 7 Kronefeld et al. (2014)
Italy 2000-2002 PCR 3,198 1,364 10 4 6 Cancrini et al. (2006)
Brazil 1995-1996 Dissection 3,677 3,677 55 8 7 Labarthe et al. (1998)
Portugal 2011-2013 PCR 5,866 1,815 54 23 8 Ferreira et al. (2015)
Argentina 2003-2005 Dissection 2,380 2,380 3 0 7 Vezzani et al. (2006)
Russia 2007-2017 PCR 387 78 5 0 8 Shaikevich et al. (2018)
USA 1994 Dissection 188 188 3 0 6 Comiskey and Wesson (1995)
Italy 2002-2003 PCR 1,576 880 6 3 5 Cancrini et al. (2007)
Italy 2003 PCR 154 154 2 1 6 Cancrini et al. (2003a, 2003b)
Italy 2000-2002 Dissection 2,534 336 81 22 5 Cancrini et al. (2003a, 2003b)
Spain 2005-2007 PCR 1,219 1,219 1 0 7 Morchón et al. (2011)
Argentina 2007-2008 PCR 453 82 2 0 6 Vezzani et al. (2011)
Portugal 2002-2003 PCR 554 554 4 2 7 Santa-Ana et al. (2006)
Turkey 2008-2009 PCR 6,153 559 15 14 8 Yildirim et al. (2011)
Spain 2012-2013 PCR 881 881 1 1 6 Bravo-Barriga et al. (2016)
Turkey 2008 PCR 301 54 2 1 8 Bıs¸kın et al. (2010)
Slovakia 2013 PCR 10,500 105 4 0 8 Bocková et al. (2015)
Spain 2004-2006 PCR 725 725 2 0 7 Morchon et al. (2007)
USA 1985-1987 Dissection 9,377 9,377 123 18 7 Parker (1993)
South-Korea 2005 PCR 2,059 172 12 0 6 Lee et al. (2007)
USA 2006-2007 PCR 1,401 206 15 0 8 Licitra et al. (2010)
France 2015 Real time PCR 797 797 29 0 8 Tahir et al. (2017)
Italy 2005 PCR 637 119 1 0 7 Masetti et al. (2008)
Taiwan 1997 Dissection 4,537 4,537 146 0 6 Lai et al. (2001)
Samoa 1978-1980 Dissection 41,980 41,980 179 49 7 Samarawickrema et al. (1992)
French Polynesia 2003-2004 Dissection 1,194 1,194 28 4 8 Russell et al. (2005)

List of published articles included in the systematic review for experiment studies of D. immitis in vectors.

Country Year of implementation Detection method Total sample Total pool Total infected pool Total infective pool Quality score References
Brazil 2000 Dissection 756 756 225 57 8 Ahid et al. (2000)
Italy 2017 PCR 136 136 66 10 7 Silaghi et al. (2017)
Italy 2015 PCR 45 45 37 18 8 Montarsi et al. (2015)
Iran 2017 PCR 90 90 58 16 7 Solgi et al. (2017)
Brazil 2008 Dissection 1,942 1,942 465 0 8 Carvalho et al. (2008)
USA 2005 Dissection 750 750 630 0 8 Debboun et al. (2005)
Brazil 1998 Dissection 73 73 43 0 7 Macêdo et al. (1998)
Australia 1989 Dissection 215 215 0 49 6 Russell et al. (2005)
Brazil 1999 Dissection 505 505 0 101 8 Brito et al. (1999)

Subgroup meta-analysis of field studies reporting pool prevalence D. immitis infected and infective rates in vectors grouped by risk factor.

Minimum infected ratea Minimum infective rateb
Variable Pool size Positive pool Overall prevalence (95% CI) I 2c Positive pool Overall prevalence (95% CI) I 2
Latitude
0-20 44,470 245 16.9 (3.2-40.1) 96.6 53 0.5 (0.2-0.9) 1.8
20-40 25,560 609 29 (15.1-46.9) 97.7 129 5.7 (1.3-12.2) 95.1
>40 54,450 217 17.4 (4.5-37) 98.3 53 1.70 (0-6.1) 93.1
Longitude
0-10 4,218 86 13.1 (1.3-36) 95.7 24 1.9 (0-9.5) 90.9
10-20 52,621 128 12 (1.8-29.6) 98.1 32 2.1 (0-6.7) 93.3
20-50 4,745 96 29.9 (12.9-52.6) 81.9 33 8.4 (0-26-9) 87.8
50-80 12,150 129 6.1 (0-18.8) 93.7 18 0 (0-1.4) 66.9
80-110 2,473 234 58.1 (9.1-143) 97.7 75 12.5 (0-49) 96
>110 48,273 398 34.8 (11.5-69.4) 98.8 53 0.3 (0-1.7) 75.1
Mean temperature °C
7-14.9 52,431 190 23.3 (7.3-46.9) 98 47 2.5 (0-8.1) 92.3
15-21.9 18,905 404 19.6 (6-39.9) 98.1 106 4.1 (0.4-10.4) 94.2
22-28.1 53,144 477 23.9 (10.8-41.5) 98.1 82 1.9 (0.1-5.1) 90.9
Annual rainfall (mm)
<250 49,029 5 0.4 (0-3) 79.5 1 0 (0-0.1) 37.3
251-500 24,280 509 27.8 (16.6-41.5) 96 100 5.1 (1.4-10.2) 92
501-1,000 8,801 345 32 (9.8-65.7) 97.9 85 3.4 (0-12.7) 94.9
>1,000 42,370 212 3.9 (3.3-4.6) 99.7 49 0.6 (0.3-0.9) 99.3
Sea level (m)
<25 15,367 281 28.7 (12.4-50.9) 96.4 52 3.4 (0.2-9.1) 87.8
26-100 6,945 291 36.1 (4.7-93.7) 98.9 98 11.2 (0.3-34.6) 97.6
101-200 95,282 379 13.3 (4.1-26.8) 99.2 57.9 0 (0-1.1) 93.7
201-1000 4,067 58 12.3 (1.4-31.7) 94 3 0.1 (0-1) 0
>1,000 2,819 62 27.8 (4.4-67.3) 95.1 25 10 (0-35.1) 93.8
Mean humidity (%)
<65 5,171 73 12.3 (1.5-29.6) 89.5 24 5.8 (0-19.6) 89.6
66-70 15,821 413 26.9 (6.1-61.1) 98.8 104 7.4 (1.2-18) 95.9
71-75 51,514 132 24.4 (8.2-48.1) 97.6 31 1.8 (0-7.1) 91
76-80 8,579 235 22.2 (9.9-38.8) 93.1 27 1.2 (0-8.5) 93.7
>80 43,395 218 14.1 (0.9-39.4) 95.3 0.49 0.1 (0-0.3) 0
Detection method
PCR 60,539 425 19.3 (7.9-34.9) 98.3 113 2 (0-5.7) 93.7
Dissection 63,941 646 30.5 (1.5-48.5) 98.8 122 4.5 (1.6-8.6) 95.2
Implementation year
1992-2000 55,222 360 10.5 (4-19.7) 97.3 75 0.9 (0.4-1.6) 40.7
2000-2005 6,221 257 57.3 (14.5-124.7) 98 27 9.6 (0-36.4) 96.6
2006-2010 8,525 132 24.4 (10.1-43.9) 95.3 41 3.7 (0.1-10.3) 89.6
2011-2015 6,313 283 19.9 (2.6-50.2) 94.4 91 3.8 (0-14.6) 93.5
2016-2018 48,199 39 10.3 (0–35.1) 97.4 1 0 (0-0.1) 45.4
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