Control trial of Lutzomyia longipalpis s.l. in the Island of Margarita, Venezuela

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1 Tropical Medicine and International Health volume 8 no 12 pp december 2003 Control trial of Lutzomyia longipalpis s.l. in the Island of Margarita, Venezuela M. Dora Feliciangeli 1, Milena B. Mazzarri 2, Sonia San Blas 3 and Olga Zerpa 4 1 Universidad de Carabobo, Facultad de Ciencias de la Salud, Centro Nacional de Referencia de Flebótomos (CNRFV), BIOMED, Núcleo Aragua, Maracay, Venezuela 2 Dirección de Vigilancia Epidemiológica y Control Sanitario Ambiental, Ministry of Health and Social Development, Venezuela 3 Dirección Regional de Salud, Estado Nueva Esparta, Venezuela 4 Instituto de Biomedicina, UCV/MSDS, Caracas, Venezuela Summary The incidence of the American visceral leishmaniasis (AVL) in the Island of Margarita, a major tourist centre in Venezuela, has been increasing between 1998 and Lutzomyia longipalpis s.l. is the recognized vector, which was found naturally infected with Leishmania spp, indistinguishable from the parasites recovered from dogs and children. In , we conducted a control trial in Santa Ana del Valle and Las Cabreras, which have similar epidemiological and ecological conditions. The trial was based on intradomestic residual spraying of k-cyhalotrin, E.C., 25 mg/m 2 and spatial fogging of fenitrothion around the houses at 30 g/ha. Sandfly abundance was recorded using Centers for Disease 2 Control (CDC) traps indoors and outdoors. We found significantly reduced sandfly populations in the target locality. Wall bioassays showed that the residual effect of the insecticide lasts for about 3 months. We believe that indoor spraying with k-cyhalotrin three times a year, at a dose slightly greater than 25 mg/m 2, might reduce the L. longipalpis s.l. population to a level low enough for achieving a significant reduction of the indoor transmission, thus protecting small children from the disease. keywords American visceral leishmaniasis, vector control, k-cyhalothrin, fenitrothion, Venezuela Introduction American visceral Leishmaniasis (AVL) in Venezuela is distributed in 15 of the 23 states in the territory. About 1000 cases were officially reported from 1955 to 2001, an overall average of about 20 cases/year. This is thought to underestimate the true incidence. However, with the re-emergence of AVL in rural foci (Delgado et al. 1998; Zulueta et al. 1999) and the emergence in periurban suburbs (Aguilar et al. 1998) these figures have increased to 50 cases/year in the last years (OPS 1994; Zulueta et al. 1999). At present the Island of Margarita, a major tourist centre in Venezuela, with an extension of 1085 km 2 and a population of inhabitants, constitutes one of the most active foci. Zerpa et al. (2001) have reported 3.6 cases/year for the period and nine cases/year from 1995 to Afterward ( ), 39 cases (13 cases/year), have been added to the official data (Department of Informatics, Institute de Biomedicine, Caracas). Although this tendency may be in part attributed to increased awareness of medical doctors and better methods of diagnosis, increasing poverty and the resulting malnutrition are thought to be the principal risk factor for this epidemiological situation. An entomological survey in March 1998 found one of 23 females (4.3%) of Lutzomyia longipalpis s.l. (Lutz & Neiva 1912) infected with suprapyloric Leishmania (Feliciangeli et al. 1998) in the suburb of Achipano of the capital city Porlamar (63 28 W 9 55 N). In August of that year, in samples from rural villages, another fly (one of 149) was found infected in La Vecindad (11 04 N W). With PCR and DNA-probes this parasite was recognized as indistinguishable from parasites 4isolated from humans and dogs ( Rodriguez N, unpublished data), which have been recently identified as Leishmania infantum, zymodeme MON-1 (Zerpa et al. 2001). These results and the importance of the disease as public health problem in the Island stimulated our vector control trial from January 1999 to February ª 2003 Blackwell Publishing Ltd 1131

2 Materials and methods Study area The village of Santa Ana, Municipality Gómez (11 06 N W), was selected as the target locality, and Las Cabreras, Municipality Marcano (11 03 N W) as the control locality. The distance between villages is about 5 km. The area is covered by deciduous xerophile vegetation, with an average temperature of C and yearly precipitation of mm, and is classified as very dry tropical forest life zone (Ewel & Madriz 1968). Santa Ana had a population of about 5000 inhabitants living in 975 houses, Las Cabreras had 2300 inhabitants in 459 houses. Almost all houses were built under the Government rural housing programme, with complete cement, plastered and oil-painted walls, and zinc roofs. In 1998 one case of AVL had been reported in each locality. Insecticide applications Based on a previous study on the susceptibility to different insecticides of a sandfly species in the complex (L. pseudolongipalpis Arrivillaga & Feliciangeli 2001 from Curarigua, Lara State; Mazzarri et al. 1997), both the pyrethroid k-cyhalothrin and the organophosphate fenitrothion insecticides were used for this trial. Although 5more expensive than the wet powder (WP) formulation, we selected the emulsion concentrate (EC) formulation as recommended by WHO (1997) for smooth and painted walls because of the structure of the houses (cement bricks and oil-painted walls). Another reason for not using the WP formulation is that the walls become marked with white spots. One of us (MBM) has observed that inhabitants find this unacceptable, and soon wash the walls. Moreover, the high temperatures in houses with zinc or asbestos roofs would inactivate the WP, with particles of the insecticide falling from the walls (Najera & Zaim 2001). The indoor residual spraying of k-cyhalothrin EC 2.5% had the target dosage of 25 mg/m 2, using a Hudson X-Pert (flat-spray nozzle T-8002) hand compression sprayer. The insecticide was sprayed on the internal wall surfaces of the houses and on the lower surface of large furniture. The spraying was repeated every 5 months during the trial. Spatial fogging of fenitrothion ULV 50%, around the houses was made using portable Puls-fog equipment at a concentration of 30 g a.i./ha. Sixteen fogging sprays were conducted during the year of study. Except for the months May, June and October when only one was applied, treatments took place at fortnightly intervals until the end of November Dates of insecticide applications are summarized in Table 1. Table 1 Control trial of Lutzomyia longipalpis in the Island of Margarita, Venezuela: dates of interventions Indoors spraying k-cyhalothrin (25 mg/m 2 ) Systematic sandfly sampling Five houses in each village were selected in a radius of 200 m around the patient s house for monitoring control effectiveness, by comparing the phlebotomine sandfly densities in the sprayed village, Santa Ana, vs. the control village, Las Cabreras. Whenever possible, the selection of the houses was based on the presence of dogs and/or chicken in the peridomestic habitat. Sandflies were collected using 10 CDC miniature light traps (John W. Hock Company, Model 512) in each village. Five were placed in the bedrooms, suspended from the ceiling at about 2 m from the ground floor. Another five traps were placed in the peridomicile, in the chicken sheds or in a tree close to the dog sleeping places. All were operating from to hours. The entomological evaluation started 15 days before (21 January 1999) the first residual spraying (4 February 1999) and continued for 13 months (25 February 2000). Bioassays for biological test on wall surfaces Spatial fogging fenitrothion (30 g/ha) 4 February February March March April April May June July July July August August September September October November November December 1999 The residual effect was checked at 7, 69 and 125 days after spraying, on the wall surfaces of cement-plastered and oilpainted walls. The biological tests on walls of five houses (two walls per house) randomly selected from the insecticide-sprayed village were conducted with a laboratory reared susceptible L. pseudolongipalpis, maintained for 10 years at the Centro Nacional de Referencia de Flebótomos (CNRFV), University of Carabobo. Groups of 20 sugar-fed female sandflies were transported to the 1132 ª 2003 Blackwell Publishing Ltd

3 village in their rearing pots, held in plastic cages with paper moistened with distilled water to avoid desiccation before the bioassays. The procedure used followed the protocols of the Ministerio de Sanidad y Asistencia Social de 6 Venezuela (1971) and WHO (1997). The test started at 7.00 am. Samples of 20 sandflies were placed in the plastic cones on sprayed walls at three heights: 0.5, 0.8 and 1.7 m from the ground. Control groups of sandflies were exposed to untreated surfaces on the same kind of the walls which were prepared ad hoc. The exposure time was 30 min, after which sandflies were transferred and kept in uncontaminated plastic cups. Thirty percentage sucrose was offered on cotton balls. The mortality was recorded at 24 h. Results The sandfly fauna in Santa Ana and Las Cabreras during the study constituted four species: L. longipalpis s.l., L. evansi (Nuñez Tovar 1924), L. cayennensis cayennensis (Floch & Abonnenc 1941) and L. dubitans (Sherlock 1962) with an overwhelming predominance of L. longipalpis (>99%) in both localities. Only one # of L. evansi, one # of L. cayennensis and one # and two $ of L. dubitans were collected in Sta Ana. One $ of L. evansi, one # and one $ of L. dubitans and 14 # and four $ of L. c. cayennensis were caught in Las Cabreras. Inspection by the Kolmogorov Smirnov test showed that L. longipalpis catches were not normally distributed in either Santa Ana (N ¼ 1606; Dmax ¼ ; P < 1) or Las Cabreras (N ¼ 1663; Dmax ¼ ; P < 1). Therefore, population densities were compared both before and after treatment, using the non-parametric Mann Whitney U test. The results are given in Tables 2 and 3. As the sample sizes are relatively large, the Z value is used to assess significance (Siegel 1976). Slight differences in the numbers of collections between the control and the treated localities were due to the fact that at some sampling points the householders were absent or a mechanical fail of the trap was noticed, so that count was discarded. The comparison of overall sandfly counts prior to the intervention showed no difference between the adult population densities in Santa Ana vs. the sandfly population in Las Cabreras indoors and outdoors (Table 2), whereas comparison of the sandfly abundance after the chemical intervention showed highly significant differences between the densities of untreated and treated populations (Table 3). Moreover, significant differences were observed in relation to the sex ratio in the treated vs. the control population. The sex ratio (male female) in Santa Ana, indoors, before intervention was 2.74:1. After the intervention it changed significantly to 0.76:1 (Yates corrected v 2 ¼ 32.76, Table 2 Phlebotomine sandfly densities in Santa Ana del Valle and Las Cabreras, Island of Margarita, before a chemical control trial: results of the Mann Whitney U test Santa Ana del Valle/Las Cabreras Indoor Outdoor Females No. captures 5/6 31/41 No. specimens 39/56 678/409 P-value (NS) Males No. captures 5/6 31/41 No. specimens 107/71 790/548 P-value (NS) NS, not significant. Table 3 Phlebotomine sandfly densities in Santa Ana del Valle and Las Cabreras, Island of Margarita, after a chemical control trial: results of the Mann Whitney U test Santa Ana del Valle/Las Cabreras Indoor Outdoor Females No. captures 799/ /810 No. specimens 146/ /2083 P-value Males No. captures 799/ /810 No. specimens 111/ /3892 P-value Highly significant. P < 000) while in Las Cabreras it was not significantly different during the two periods of observation (1.26:1 vs. 1.30:1; Yates corrected v 2 ¼ 0, P ¼ 0.97). The same pattern was observed outdoors: after the intervention, the sex ratio in Santa Ana became significantly female-biased (1.17 vs. 0.90; Yates corrected v 2 ¼ 13.93, P ¼ 002) while in Las Cabreras, although the proportion of males significantly increased in the second period of study (Yates corrected v 2 ¼ 21.88, P < 0005), the ratio was always in favour of males (1.33:1 vs. 1.86:1). Figures 1 4 show the monthly geometric mean abundance of sandflies caught per trap per night during the period of study. The months in which significant statistical differences, using the Mann Whitney test, were observed between counts of the control and target populations, are indicated with asterisks. The effect of the intervention was lower outdoors. Figures from indoors showed that the treatments with k-cyhalothrin had a marked effect on the female and male population, which did not peak during ª 2003 Blackwell Publishing Ltd 1133

4 Tropical Medicine and International Health volume 8 no 12 pp december 2003 Females/trap/night (geometric mean) Feb Dates of spraying, significant z values 7 July 7 Dec Feb 99 Apr 99 Jun 99 Aug 99 Oct 99 Dec 99 Feb 00 Figure 1 Control of Lutzomyia longipalpis in the island of Margarita, Venezuela: monthly indoors female densities. Females/trap/night (geometric mean) Feb 99 Apr 99 Jun 99 Aug 99 Oct 99 Dec 99 Feb 00 Significant z values Males/trap/night (geometric mean) Mortality (%) days 69 days 125 days 7 days 69 days 125 days Cement walls Significant z values Feb 99 Apr 99 Jun 99 Aug 99 Oct 99 Dec 99 Feb 00 Figure 4 Control of Lutzomyia longipalpis in the island of Margarita, Venezuela: monthly outdoors female densities. Oil painted walls Figure 2 Control of Lutzomyia longipalpis in the island of Margarita, Venezuela: monthly outdoors female densities. Males/trap/night (geometric mean) Feb Dates of spraying, significant z values 7 July 7 Dec Feb 99 Apr 99 Jun 99 Aug 99 Oct 99 Dec 99 Feb 99 Figure 3 Control of Lutzomyia longipalpis in the island of Margarita, Venezuela: monthly indoors male densities. the year of study, while the control population showed two peaks, in September and in December. A small recovery was observed 2 months after the first intervention, which might be explained by the loss of residual effect of the insecticide as indicated in Figure 5. This shows that the residual effect of the k-cyhalothrin spraying applied to the house walls, measured by the mortality of the exposed Figure 5 Mortality rates of Lutzomyia pseudolongipalpis in wall bioassays with k-cyhalothrin at different days after treatment. laboratory reared susceptible L. pseudolongipalpis, (n ¼ 1879 specimens) fell considerably during the period of study. No mortality of the insects was recorded on the control surfaces (n ¼ 729). On the contrary, the mortality on the treated surfaces, attributable to the insecticide, dropped significantly between 7 and 69 days (1 10 weeks) on both cement (v 2 ¼ , P < 001) and oil-painted walls (v 2 ¼ 7.94, P < 05) as well as between 69 and 125 days (11 16 weeks), on cement plastered walls (v 2 ¼ 65.50, P ¼ 0001) and oil-painted walls (v 2 ¼ 47.09, P ¼ 001). There were no significant differences in mortality recorded at 1 week on the two kinds of walls, cement and oil-painted (v 2 ¼ 7, P ¼ 0.79) and at 18 weeks (v 2 ¼ 0.47, P ¼ 0.49), while significant differences were observed at 69 days after spraying between the mortality recorded on the two surfaces (v 2 ¼ 16.92, P < 001). Discussion Mathematical models used to compare the effectiveness of various methods for controlling canine and human visceral 1134 ª 2003 Blackwell Publishing Ltd

5 leishmaniasis suggested that in the New World insecticides are expected to reduce the incidence of the disease in humans, a result that should encourage properly designed vector control trials (Dye 1996). In the present work, first it is relevant to notice that our longitudinal study confirmed previous observations that the proven vector in the area, L. longipalpis s.l., is present only at very low densities. It is, however, the predominant species and shows high rates of infection (Feliciangeli et al. 1998). Secondly, the impact of the insecticide spraying and fogging was demonstrated by the comparison of the counts of L. longipalpis s.l. in a target and a control locality over more than 1 year, as it led to a significant reduction of the sandfly population both indoors and outdoors. However, the effect of spraying inside walls on the mean L. longipalpis s.l. abundance was more significant than the spatial fogging. In fact, the indoor population did not peak in the target locality, while the control population increased to almost four times the treated population. In contrast, although a significant reduction of the sandfly abundance in the treated locality was achieved outdoors, both the control and target population peaked with a unimodal seasonal pattern. The inverted sex ratio in the treated population, which was also observed by other authors (Kelly et al. 1997), would indicate that males are more susceptible to the insecticides than females. This makes sense as males are smaller than females. The results obtained with insecticide spraying indoors were similar to the results with L. longipalpis s.l. obtained with deltamethrin (Marcondes & Nascimento 71993) and with cypermethrin (Passerat de Silans et al ). However, when we analysed our data at monthly resolution, 3 months after the first spraying and before the next, the target adult population seemed to recover. Bioassay trials supported these results. In fact, the residual effect of the insecticide-indoor applications lasted for a period no longer than 3 months on both cement and oilpainted walls. The significant difference on the mortality observed for the two kind of walls at 69 days might be interpreted as the result of the higher rate of absorption of the insecticide through the cement wall, which increases when an EC is used (Marcondes & Nascimento 1993) vs. results given by humectable powder formulations (HP) (Le Pont et al. 1989). The effect of the absorption of the insecticide by the wall was not detectable at the extreme dates of observation as the amount of the insecticide was still very high at 7 days, and very low at 125 days. To conclude, we would not recommend spatial fogging, unless the L. longipalpis population had dramatically increased. As this measure is extremely weather-affected, spatial fogging is only recommended in epidemic situations to drastically reduce the population density (WHO 1996, 1997). Moreover, this application is hard to sustain not only in terms of cost, but also because the insecticide pressure could cause the development of resistance in the target population. Since transmission is thought to occur inside the houses (the majority of cases have been children 3-years-old or younger, Zerpa et al. 2001), we would recommend spraying inside walls. However, the dose that we used was very close to that which gave the best results in the laboratory susceptibility bioassays (Mazzarri et al. 1997), which generally is a lower dose than recommended for field trials (Oliveira Filho & Melo 1994). Therefore, increasing moderately the dose and diminishing the period of indoor spraying to 4 months (three interventions per year) might keep the L. longipalpis s.l. populations to a level low enough to achieve an important reduction or even interrupt the indoor transmission. Acknowledgements We thank Martin Ledezma, Arturo Bravo, Aristides Rojas, Roberto Peña y José Luis León for the valuable assistance in the fieldwork. This research was supported by the World Bank and the Government of Venezuela (Projects VEN/ and PCEE-17) and the University of Carabobo (Project FCS ). References Aguilar CM, Fernandez E, Fernández R et al. (1998) Urban visceral leishmaniasis in Venezuela. Memorias do Instituto Oswaldo Cruz 93, Delgado O, Feliciangeli MD, Gomez B, Alvarado J, Garcia L & Bello C (1998) The re-emergence of American visceral leishmaniasis in old focus in Venezuela: present situation of human and canine infection. Parasite 5, Dye C (1996) The logic of visceral leishmaniasis control. American Journal of Tropical Medicine and Hygiene 55, Ewel JJ & Madriz A (1968) Zonas de vida de Venezuela. Memoria explicativa sobre el mapa ecológico. Editorial Sucre, Caracas, 264 p. Feliciangeli MD, Zerpa O, Rodríguez N, Bravo A, Galindo W & Convit J (1998) Hallazgo de Lutzomyia longipalpis (Diptera: Psychodidae) naturalmente infectada con promastigotos en un foco endémico de kala-azar en la Isla de Margarita, Estado Nueva Esparta, Venezuela. Boetín de la Dirección de Malariología y Saneamiento Ambiental 38, Kelly DW, Mustafa Z & Dye C (1997) Differential application of lambda-cyhalothrin to control the sandfly Lutzomyia longipalpis. Medical and Veterinary Entomology 11, Le Pont F, Padilla JM, Desjeux P, Richard A & Mouchet J (1989) Impact depulverization de deltamethrine dans une foyer de leishmanose de Bolivie. Annals de la Societé Belgique de Médicine Tropicale 69, ª 2003 Blackwell Publishing Ltd 1135

6 Marcondes CB & Nascimento JA (1993) Avaliaçao da eficiencia de deltametrina (K-Othrine CE) no controle de Lutzomyia longipalpis (Diptera: Psychodidae) no municipio de Santa Rita, Pariba, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 26, Mazzarri M, Feliciangeli MD, Maroli M, Hernandez A & Bravo A (1997) Susceptibility of Lutzomyia longipalpis (Diptera: Psychodidae) to selected insecticides in an endemic focus of visceral leishmaniasis in Venezuela. Journal of the American Mosquito Control Association 13, Ministerio de Sanidad y Asistencia Social (1971) Actividades del Inspector de Control de Vectores. Manual de Procedimiento. Dirección de Malariologia y Saneamiento Ambiental, 7th edn. 9 Maracay, Venezuela, 113 p. Najera JA & Zaim M (2001) Malaria Vector Control. Insecticides for Indoor Residual Spraying. WHO/CDS/WHOPES/ Oliveira Filho A & Melo MTV (1994) The chemical control of vectors of leishmaniasis. Memorias do Instituto Oswaldo Cruz 83, OPS (1994) Las condiciones de Salud en las Americas. Organización Panamericana de la Salud. Publ. Cient., Washington D.C. 549, 485 p. Passerat de Silans LNM, Dedet JP & Arias J (1998) Field monitoring of cypermethrin residual effect on the mortality rates of the plebotomine sandfly Lutzomyia longipalpis in the Sate of Pariba, Brazil. Memorias do Instituto Oswaldo Cruz 93, Siegel S (1976) Estadística no paramétrica aplicada a las ciencias de la conducta. (ed. Trillas), México, 346 p. WHO (1996) Manual de lucha contra la Leishmaniasis visceral. WHO/LEISH/ Geneva. WHO (1997) Vector Control. Methods for use by individuals and community. (ed JA Rozendaal), Geneva, 442 p. Zerpa O, Pratlong F, Ulrich M & Convit J (2001) Isolation of Leishmania infantum, zymodeme MOM-1 from canine and human visceral leishmaniasis on Margarita Island, Venezuela. Memorias do Instituto Oswaldo Cruz 96, Zulueta AM, Villaroel E, Rodríguez N et al. (1999) Epidemiologic aspects of American visceral leishmaniasis in an endenic focus in eastern Venezuela. American Journal of Tropical Medicine and Hygiene 61, Authors M. Dora Feliciangeli (corresponding author), Universidad de Carabobo, BIOMED, Apartado 4873, Maracay, Venezuela. Fax: ; mdora@telcel.net.ve Milena B. Mazzarri, Ministerio de Salud y Desarrollo Social, Dirección General de Salud Ambiental y Contraloría Sanitaria, Avda. Las Delicias, Maracay, Venezuela. mazzarrim@telcel.net.ve Sonia San Blas, Dirección Regional de Salud, Calle San Rafael, Porlamar, Nueva Esparta, Venezuela. Olga Zerpa, Instituto de Biomedicina, UCV/MSDS, San Simeón a Providencia, al lado de Hospital Vargas, San José, Caracas, Venezuela. ozerpa@telcel.net.ve 1136 ª 2003 Blackwell Publishing Ltd

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