Comparison of Different Sampling Methods to Catch Lymphatic Filariasis Vectors in a Sudan Savannah Area of Mali

Yaya Ibrahim Coulibaly Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;
Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom;
Dermatology Hospital of Bamako, Bamako, Mali;

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Moussa Sangare Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;
Faculty of Health Sciences, Interdisciplinary School of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada;

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Housseini Dolo Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Salif Seriba Doumbia Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Siaka Yamoussa Coulibaly Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Ilo Dicko Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Abdoul Fatao Diabate Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Michel Emmanuel Coulibaly Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Lamine Soumaoro Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Abdallah Amadou Diallo Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Massitan Dembele National Lymphatic Filariasis Elimination Program, Bamako, Mali;

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Sekou Fantamady Traore Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali;

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Michelle Stanton Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom;

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Benjamin Guibehi Koudou Swiss Center for Scientific Research in Côte d'Ivoire (CSRS), Abidjan, Côte d'Ivoire;

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Amy D. Klion Laboratory of Parasitic Diseases, Eosinophil Pathology Section, National Institutes of Health, Bethesda, Maryland;

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Thomas B. Nutman Laboratory of Parasitic Diseases, Helminth Immunology Section, National Institutes of Health, Bethesda, Maryland;
World Health Organization, Vectors, Environment, and Society Research, Geneva, Switzerland;

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Louise Kelly-Hope Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom;

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Moses John Bockarie Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom;
School of Community Health Sciences, Njala University, Bo, Sierra Leone

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ABSTRACT.

There is a need for better tools to monitor the transmission of lymphatic filariasis and malaria in areas undergoing interventions to interrupt transmission. Therefore, mosquito collection methods other than human landing catch (HLC) are needed. This study aimed to compare the Ifakara tent trap type C (ITTC) and the Biogents sentinel trap (BGST) to the HLC in areas with different vector densities. Mosquitoes were collected in two villages in Mali from July to December in 2011 and 2012. The three methods were implemented at each site with one ITTC, one BGST, and one HLC unit that consisted of one room with two collectors—one indoor and the other outdoor. The Anopheles collected in 2011 were individually dissected, whereas those from 2012 were screened in pools using reverse transcription-polymerase chain reaction (RT-PCR) to determine the maximum infection prevalence likelihood (MIPL) for Wuchereria bancrofti and Plasmodium falciparum. The dissection of the females also allowed to assess the parity rates, as well its results. Over the 2 years, the HLC method collected 1,019 Anopheles, yields that were 34- and 1.5-fold higher than those with the BGST and ITTC, respectively. None of the dissected Anopheles were infected. The RT-PCR results showed comparable MIPL between HLC and ITTC for W. bancrofti with one infected pool from each trap’s yield (respectively 0.03% [0.0009–0.2%] and 0.04% [0.001–0.2%]). For P. falciparum, no infected pool was recovered from BGST. The ITTC is a good alternative to HLC for xenomonitoring of program activities.

Author Notes

Address correspondence to Yaya Ibrahim Coulibaly, Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Faculty of Medicine and Odonto-Stomatology, BP: 1805, Point G, Bamako, Mali. E-mail: yicoulibaly@icermali.org

Authors’ addresses: Yaya Ibrahim Coulibaly, Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali, Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom, and Dermatology Hospital of Bamako, Bamako, Mali, E-mail: yicoulibaly@icermali.org. Moussa Sangare, Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali, and Faculty of Health Sciences, Interdisciplinary School of Health Sciences, University of Ottawa, Ottawa, Ontario, Canada, E-mail: mbsangare@icermali.org. Housseini Dolo, Salif Seriba Doumbia, Siaka Yamoussa Coulibaly, Ilo Dicko, Abdoul Fatao Diabate, Michel Emmanuel Coulibaly, Lamine Soumaoro, and Abdallah Amadou Diallo, E-mails: hdolo@icermali.org, salifdoumbia@icermali.org, yamoussa@icermali.org, ilo@icermali.org, afatao@icermali.org, michou@icermali.org, soumla@icermali.org, and abdallahamadoudiallo@icermali.org. Massitan Dembele, National Lymphatic Filariasis Elimination Program, Bamako, Mali, E-mail: masdembele@yahoo.fr. Sekou Fantamady Traore, Filariasis Research and Training Unit, International Center of Excellence in Research (ICER-Mali), Bamako, Mali, E-mail: cheick@icermali.org. Michelle Stanton, Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom, E-mail: michelle.stanton@lstmed.ac.uk. Benjamin Guibehi Koudou, Swiss Center for Scientific Research in Côte d’Ivoire (CSRS), Abidjan, Côte d'Ivoire, E-mail: guibehi.koudou@csrs.ci. Amy D. Klion, Laboratory of Parasitic Diseases, Eosinophil Pathology Section, National Institutes of Health, Bethesda, MD, E-mail: aklion@niaid.nih.gov. Thomas B. Nutman, Laboratory of Parasitic Diseases, Helminth immunology Section, National Institutes of Health, Bethesda, MD, and World Health Organization, Vectors, Environment and Society Research, Geneva, Switzerland, E-mail: tnuman@niaid.nih.gov. Louise Kelly-Hope, Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom, E-mail: lkhope@liverpool.ac.uk. Moses John Bockarie, Center for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, University of Liverpool, Liverpool, United Kingdom, and School of Community Health Sciences, Njala University, Bo, Sierra Leone, E-mail: bockarie@edctp.org.

  • 1.

    World Health Organization , 2020. Programme mondial pour l’élimination de la filariose lymphatique: rapport de situation, 2019 Wkly Epidemiol Rec 23: 509524.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    De Souza DK , Koudou B , Kelly-Hope LA , Wilson MD , Bockarie MJ , Boakye DA , 2012. Diversity and transmission competence in lymphatic filariasis vectors in West Africa, and the implications for accelerated elimination of Anopheles-transmitted filariasis. Parasit Vectors 5: 259.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Ramaiah KD , Ottesen EA , 2014. Progress and impact of 13 years of the global programme to eliminate lymphatic filariasis on reducing the burden of filarial disease. PLoS Negl Trop Dis 8: e3319.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Pedersen EM , Stolk WA , Laney SJ , Michael E , 2009. The role of monitoring mosquito infection in the Global Programme to Eliminate Lymphatic Filariasis. Trends Parasitol 25: 319327.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Govella NJ , Chaki PP , Mpangile JM , Killeen GF , 2011. Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors 4: 40.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Ughasi J , Bekard HE , Coulibaly M , Adabie-Gomez D , Gyapong J , Appawu M , Wilson MD , Boakye DA , 2012. Mansonia africana and Mansonia uniformis are vectors in the transmission of Wuchereria bancrofti lymphatic filariasis in Ghana. Parasit Vectors 5: 89.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Sikaala CH , Killeen GF , Chanda J , Chinula D , Miller JM , Russell TL , Seyoum A , 2013. Evaluation of alternative mosquito sampling methods for malaria vectors in Lowland South—east Zambia. Parasit Vectors 6: 91.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Govella NJ , Moore JD , Killeen GF , 2010. An exposure-free tool for monitoring adult malaria mosquito populations. Am J Trop Med Hyg 83: 596600.

  • 9.

    Casulli A , 2021. New global targets for NTDs in the WHO roadmap 2021–2030. PLoS Negl Trop Dis 15: e0009373.

  • 10.

    Wong J , Bayoh N , Olang G , Killeen GF , Hamel MJ , Vulule JM , Gimnig JE , 2013. Standardizing operational vector sampling techniques for measuring malaria transmission intensity: evaluation of six mosquito collection methods in western Kenya. Malar J 12: 143.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Krajacich BJ et al.2015. Sampling host-seeking anthropophilic mosquito vectors in West Africa: comparisons of an active human-baited tent-trap against gold standard methods. Am J Trop Med Hyg 92: 415421.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Batista EPA , Ngowo H , Opiyo M , Shubis GK , Meza FC , Siria DJ , Eiras AE , Okumu FO , 2018. Field evaluation of the BG-Malaria trap for monitoring malaria vectors in rural Tanzanian villages. PLoS One 13: e0205358.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Gambhir M , Bockarie M , Tisch D , Kazura J , Remais J , Spear R , Michael E , 2010. Geographic and ecologic heterogeneity in elimination thresholds for the major vector-borne helminthic disease, lymphatic filariasis. BMC Biol 8: 22.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Govella NJ , Chaki PP , Geissbuhler Y , Kannady K , Okumu F , Charlwood JD , Anderson RA , Killeen GF , 2009. A new tent trap for sampling exophagic and endophagic members of the Anopheles gambiae complex. Malar J 8: 157.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Govella NJ , Moore JD , Killeen GF , 2010. An exposure-free tool for monitoring adult malaria mosquito populations. Am J Trop Med Hyg 83: 596600.

  • 16.

    Govella NJ , Chaki PP , Mpangile JM , Killeen GF , 2011. Monitoring mosquitoes in urban Dar es Salaam: evaluation of resting boxes, window exit traps, CDC light traps, Ifakara tent traps and human landing catches. Parasit Vectors 41: 112.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Chaki PP et al.2012. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. Malar J 11: 172.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Dembélé M et al.2012. Implementing preventive chemotherapy through an integrated National Neglected Tropical Disease Control Program in Mali. PLoS Negl Trop Dis 6: e1574.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Krockel U , Rose A , Eiras AE , Geier M , 2006. New tools for surveillance of adult yellow fever mosquitoes: comparison of trap catches with human landing rates in an urban environment. J Am Mosq Control Assoc 22: 229238.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Laurence BR , Pester FRN , 1961. The behaviour and development of Brugei patei (Buckley, Nelson and Heisch, 1958) in a mosquito host, Mansonia uniformis (Theobald). J Helminthol 35: 285300.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Laney SJ , Ramzy RMR , Helmy HH , Farid HA , Ashour AA , Weil GJ , Williams SA , 2010. Detection of Wuchereria bancrofti L3 larvae in mosquitoes: a reverse transcriptase PCR assay evaluating infection and infectivity. PLoS Negl Trop Dis 4: e602.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Detinova TS , Gillies MT , 1964. Observations on the determination of the age composition and epidemiological importance of populations of Anopheles gambiae giles and Anopheles funestus giles in Tanganyika. Bull World Health Organ 30: 2328.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Draper CC , Davidson G , 1953. A new method of estimating the survival-rate of anopheline mosquitoes in nature. Nature 172: 503.

  • 24.

    Nelson GS , 1958. Staining of filarial larvae in insects before dissection. Bull World Health Organ 19: 204.

  • 25.

    Service MW , Service MW , 1993. Sampling the Adult Resting Population. Mosquito Ecology. Dordrecht, The Netherlands: Springer, 210290.

  • 26.

    Nelson GS , 1959. The identification of infective filarial larvae in mosquitoes: with a note on the species found in “wild” mosquitoes on the Kenya coast. J Helminthol 33: 233256.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Rao RU , Nagodavithana KC , Samarasekera SD , Wijegunawardana AD , Premakumara WDY , Perera SN , Settinayake S , Miller JP , Weil GJ , 2014. A comprehensive assessment of lymphatic filariasis in Sri Lanka six years after cessation of mass drug administration. PLoS Negl Trop Dis 8: e3281.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Boussari O , Moiroux N , Iwaz J , Djènontin A , Bio-Bangana S , Corbel V , Fonton N , Ecochard RR , 2012. Use of a mixture statistical model in studying malaria vectors density. PLoS One 7: e50452.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Breslow N , Leroux B , Platt R , 1998. Approximate hierarchical modelling of discrete data in epidemiology. Stat Methods Med Res 7: 4962.

  • 30.

    Bates DM, DebRoy S, 2004. Linear mixed models and penalized least squares. J Multivariate Anal 91: 1–17.

    • PubMed
    • Export Citation
  • 31.

    Meyers JI et al.2016. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J 15: 239.

  • 32.

    Katholi CR , Unnasch TR , 2006. Important experimental parameters for determining infection rates in arthropod vectors using pool screening approaches. Am J Trop Med Hyg 74: 779785.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Coulibaly YI , Doumbia SS , Sanogo ZL , Keita SI , Dolo H , Traore SF , Nutman TB , Hope LK , Klion AD , 2012. Alternative mosquito vector collection methods in a Sudan savannah area of Mali that received five MDA rounds for lymphatic filariasis elimination. Abstract 641, 61st Annual ASTMH Meeting.

    • PubMed
    • Export Citation
  • 34.

    Coulibaly YI , Doumbia SS , Soumaoro L , Dicko I , Dembele M , Traore SF , Kelly-Hope L , 2013. Comparison of the ifakara tent trap and the human landing catch for mosquito collection in a Sudan savannah area of Mali. Abstract number 400, 62th Annual ASTMH Meeting.

    • PubMed
    • Export Citation
  • 35.

    Coulibaly YI , Doumbia SS , Dicko I , Soumaoro L , Dembele M , Traore SF , Kubofick J , Klion A , Kelly-Hope L , 2014. Lymphatic filariasis elimination: assessment of two villages with different endemicity levels in a previously highly endemic region (Sikasso) of Mali. Abstract number 1696, 63th Annual ASTMH Meeting.

    • PubMed
    • Export Citation
  • 36.

    Animut A , Balkew M , Lindtjørn B , 2013. Impact of housing condition on indoor-biting and indoor-resting Anopheles arabiensis density in a highland area, central Ethiopia. Malar J 12: 393.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Munhenga G , Brooke BD , Spillings B , Essop L , Hunt RH , Midzi S , Govender D , Braack L , Koekemoer LL , 2014. Field study site selection, species abundance and monthly distribution of Anopheline mosquitoes in the northern Kruger National Park, South Africa. Malar J 13: 27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Chadee DD , Williams SA , Ottesen EA , 2002. Xenomonitoring of Culex quinquefasciatus mosquitoes as a guide for detecting the presence or absence of lymphatic filariasis: a preliminary protocol for mosquito sampling. Ann Trop Med Parasitol 96: S47S53.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Jensen T , Dritz DA , Fritz GN , Washino RK , Reeves WC , 1998. Lake Vera revisited: parity and survival rates of Anopheles punctipennis at the site of a malaria outbreak in the Sierra Nevada foothills of California. Am J Trop Med Hyg 59: 591594.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Lindsay SW , Wilkins HA , Zieler HA , Daly RJ , Petrarca V , Byass P , 1991. Ability of Anopheles gambiae mosquitoes to transmit malaria during the dry and wet seasons in an area of irrigated rice cultivation in The Gambia. J Trop Med Hyg 94: 313324.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Sikaala CH , Chinula D , Chanda J , Hamainza B , Mwenda M , Mukali I , Kamuliwo M , Lobo NF , Seyoum A , Killeen GF , 2014. A cost-effective, community-based, mosquito-trapping scheme that captures spatial and temporal heterogeneities of malaria transmission in rural Zambia. Malar J 13: 225.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Chaki PP et al.2012. An affordable, quality-assured community-based system for high-resolution entomological surveillance of vector mosquitoes that reflects human malaria infection risk patterns. Malar J 11: 172.

    • PubMed
    • Search Google Scholar
    • Export Citation
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