J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

Review Article Control of Phlebotomine Sand Flies in : A Review Article

Mohammad Reza Yaghoobi-Ershadi

Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

(Received 22 Aug 2016; accepted 17 Sep 2016)

Abstract Leishmaniasis has long been known as a significant public health challenge in many parts of Iran. Phlebotomus pa- patasi and P. sergenti are the vectors of Zoonotic Cutaneous Leishmaniasis and Anthroponotic Cutaneous Leish- maniasis respectively, and 5 species of sand flies including P. kandelakii, P. neglectus, P. perfiliewi, P. keshishiani and P. alexandri are considered as probable vectors of Zoonotic visceral leishmaniasis. A literature search was per- formed of the relevant multiple databases from 1966 to 2013 to include studies on sand flies, vector control, leish- maniasis, Phlebotomus. Sand fly control in Iran began in 1966 by Iranian researchers, and long-term evaluation of its effects was completed in the study areas of the country. Herein, a review of vector control strategies in Iran to com- bat leishmaniasis including indoor residual spraying, application of chemicals in rodent burrows, impregnation of bed nets and curtains with insecticides, the use of insect repellents, impregnation of dog collars and the susceptibility of sand fly vectors to various insecticides has been summarized thus far. The investigation of the behavioral patterns of the adults of different sand fly species, introduction of biological insecticide agents, the use of insecticidal plants and other novel strategies for the control of sand fly populations have received much attention in the areas of studies, hence should be recommended and improved since they provide optimistic results.

Keywords: Leishmaniasis, Phlebotomus, Sand flies, Vector control, Iran

Introduction

Leishmaniasis remains a significant public the increasing number of ZCL cases in the health problem over a wide geographical area traditional foci and their transmission to new in Iran. Cutaneous and visceral leishmaniasis foci in the western, southern, southwestern is historical endemic disease in the country. (near the central desert), and northeastern re- Cutaneous leishmaniasis (CL) occurs in two gions of Iran has been of major concern to forms, Anthroponotic Cutaneous Leishman- the health authorities (Yaghoobi-Ershadi and iasis (ACL) and Zoonotic Cutaneous Leish- Javadian 1995, Yaghoobi-Ershadi et al. 2001, maniasis (ZCL). Leishmania major, the caus- 2003, Akhavan et al. 2007). ative agent of ZCL, is endemic in many rural Anthroponotic Cutaneous Leishmaniasis has areas of 17 out of the 31 . been a very old endemic disease in many parts The principal vector of ZCL has been identi- of Iran. The burden of the disease was greatly fied as Phlebotomus papatasi which has a reduced in many foci following the introduc- wide range of distribution, and four species tion of antimalarial measures in Iran, however, of rodents belonging to the family Cricetidae its foci remained active in some large and me- involving Rhombomys opimus, Meriones liby- dium-sized cities such as Tehran, Mashhad, cus, Tatera indica and M. hurrianae are con- Neishabur, and Sabzvar in the northeast, Shiraz sidered as the main reservoir hosts in differ- in the south, Kerman and Bam in the south- ent parts of Iran. Over the last three decades, east (Nadim and Tahvildari-Bidruni 1977,

*Corresponding author: Prof Mohammad Reza 429 http://jad.tums.ac.ir Yaghoobi-Ershadi, E-mail: [email protected], Published Online: October 04, 2016 [email protected] J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

Yaghoobi-Ershadi et al. 2002). Leishmania The practical application of sand fly con- tropica, recognized as the agent of ACL, is trol measures has been appraised in most currently prevalent in 14 foci located in 8 Old World situations (Alexander and Maroli provinces. The vector responsible for the 2003). Indoor Residual Spraying (IRS) with maintenance of L. tropica is P. sergenti, and DDT (dichlorodiphenyltrichloroethane) against human serve as the main reservoir host of malaria vectors in India during the 1950s and the disease, however infected dogs play a again in the 1970s was effective in reducing crucial role as animal reservoir host of the the density of P. argentipes and Visceral parasite (Yaghoobi-Ershadi et al. 2002, 2008). Leishmaniasis (VL) cases, but after the ces- Leishmania infantum, the causative agent sation of IRS, sand fly population and inci- of Zoonotic Visceral Leishmaniasis (ZVL), dence of VL increased (Kishore et al. 2006, has been reported sporadically from all areas Thakur 2007). Indications of the impact of of the country, however, seven endemic foci DDT spraying on sand flies were obtained are located in the southern, southwestern, from a trial conducted in a few coastal vil- western, northwestern and northeastern re- lages in Ramanathapuram district, Tamil Nadu gions of the country (Nadim et al. 1978, of India during 1953–1954. No sand flies Nadim 2008). Leishmania tropica has also could be collected from villages sprayed with been known to cause the disease in immuno- DDT at a rate of 1g/m2 and 2g/m2 for seven suppressed patients (Mohebali 2013). Five and 21 months respectively (WHO 1980). species of sand flies including P. kandelakii, DDT and BHC (Benzene hexochloride) P. neglectus, P. perfiliewi, P. keshishiani, P. have been used extensively in the former alexandri (Yaghoobi-Ershadi 2012) are con- Soviet Union for sand fly control (Perfiliev sidered as probable vectors of ZVL. Dogs, 1966). In a field trial in China, a village foxes, jackals and wolves have been found sprayed at a dosage of 1.58gr DDT/m2 against infected in different parts, but dogs are the P. chinensis in 1951 was protected by a sub- main reservoir host (Navid-Hamidi et al. sequent reduction of sand fly up to eight 1982, Nadim 2008). The mean annual num- years, while in another village sprayed in the ber of leishmaniasis cases has been projected same year at a dosage of 0.128gr gamma as almost 20,000 in Iran during 1983–2014. HCH/m2, the sand fly density showed an an- Nearly eighty percent of these cases are of nual increase until it reached the level of the ZCL form, 0.5% classified as ZVL, and density recorded in an unsprayed area in the rest are ACL (Yaghoobi-Ershadi and Ja- 1956. In a further trial a mixture of both in- vadian 1995, Yaghoobi-Ershadi et al. 2001, secticides was applied in a village in 1953, and Akhavan et al. 2007). Based on proven epi- very few sand flies were observed for six demiological studies, the provinces of Ilam years after spraying (Wang and Wu 1959). in the west, Fars in the south and Khorassan- In Palestine, IRS with DDT provided e- Razavi in the northeast have recorded the more than 50 days of protection against sand highest incidence of CL, ranging between flies (Jacusiel 1947). During 2003–2004, a 59.9–98.8 cases per 100,000 inhabitants (Shir- residual spraying program combined with the zadi et al. 2015). distribution of permethrin-treated bed nets in Official publications have revealed the the Thi Qar Governate of Iraq resulted in a existence of 48 species of sand flies in the significant reduction in VL cases, however, country, 30 species belonging to the genus no information was reported on the insecti- Phlebotomus, and 18 speicies of the genus cides used or any impact of treatment on the Sergentomyia (Yaghoobi-Ershadi 2012, density of sand flies (Jassim et al. 2006). Zahraei-Ramazani et al. 2013, 2015). 430 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

Methods another group of sprayed villages, which showed that the number of sand flies col- The electronic databases including Pub- lected from nearby rodent burrows was simi- Med, Web of Science, Literature retrieval Sys- lar to that recorded before spraying. The abun- tem of the Armed Forces Pest Management dance of sand flies, and the consequent expo- Board, Google Scholar and MEDLINE were sure of people to their bites as they sleep on searched from 1966 to 2013 using the term roofs, could explain how transmission per- Iran in combination with the keywords: Sand sisted despite house spraying. flies, Vector control, Leishmaniasis, Phleboto- Long-term evaluation of the effect of an- mus. A special emphasis was performed to timalarial DDT house spraying on the inci- refer to published original articles within the dence of ZCL was completed during 1966– last 3 decades in international scientific jour- 1971 in Esfahan, central Iran, the results of nals that deal with vector control of sand which were summarized by Seyedi-Rashti flies in Iran. and Nadim (1973) and given in more details by the same authors in 1975. The following groups of villages were kept under surveil- Control Strategies lance (monthly or every three months) since Indoor Residual Spraying 1963 for the detection of ZCL cases from Leishmaniasis control has been a matter which the annual incidence was calculated: of interest by different researchers at the In- Group I, 16 villages sprayed annually with stitute of Public Health, University of Teh- DDT throughout 1966–1969, Group II, three ran, in coincidence with the beginning of ep- villages also sprayed annually with DDT idemiological studies on CL in 1965. Table 1 during 1966–1967, and Group III, four vil- summarizes the comparison results for the lages kept without spraying for comparison. intervention against leishmaniasis vectors in The annual incidence per 1000 population Iran during 1966–2010. The effect of anti- in Group I which was 8.2 and 4.6 respec- malarial spraying on sand fly populations and tively in 1964 and 1965 before spraying de- the incidence of ZCL has been evaluated in creased to 0.7 in 1969 i.e. after four years of Esfahan Province by Nadim and Amini in spraying; following the cessation of spraying 1970. They found that DDT spraying applied in 1970, the incidence increased sharply to at a dosage of 2g/m2 in April in both 1966 15, after which a further increase was rec- and 1967 reduced ZCL incidence, but the orded in 1971. In Group II, which was sur- transmission of the disease was not inter- veyed under IRS for two consecutive years, rupted. As the incidence in 19 sprayed vil- the incidence decreased from 15.9 in 1965 to lages was 3.8 per 1000 in the first year, the 2.9 and 5.7 in 1966 and 1967 respectively, incidence in the second year was calculated but steadily increased after the discontinua- to be 2.7 per 1000. In the control villages, tion of spraying, reaching 17.5–19.7 during the corresponding incidence was highlighted 1969–1971. In Group III (Comparison group) as 14.4 and 10.6 per 1000 respectively. Col- the annual incidence per 1000 ranged be- lection of sand flies in sprayed rooms, with tween 9–21 during 1964–1970 reaching 46.3 the exception of the ones collected which in 1971 when an epidemic of ZCL broke in gave negative results, while sticky paper traps one of the villages. Analysis of the age dis- placed in the same rooms gave positive re- tribution of children's cases in previously sults from June to the end of season, indicat- sprayed and comparison villages indicated ed that P. papatasi has invaded the sprayed that once spraying was stopped, transmission rooms. Additional evidence was collated from was vigorously resumed through the abun- 431 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

dance of rodent reservoirs and sand flies in As the result of an earthquake (6.6 on the the vicinity of villages, striking the children Richter scale) in the city of Bam (Kerman who were protected during the years of Province, southeastern Iran) on December spraying. From these observations, it was 26, 2003, nearly all buildings were destroyed concluded that house spraying cannot be and a suitable condition was obtained for the considered a permanent measure for the con- breeding of P. sergenti, and there was the trol of ZCL in an endemic area, and the fea- danger of an outbreak of ACL in this old en- sibility of alternative control measures involv- demic focus due to the: extent of the de- ing reservoir hosts and immunization should struction, premature warning, raining in sev- be sought. eral times after the earthquake, movement of Nadim et al. (1977) indicated that two a large number of non-immune individuals rounds of antimalaria spraying with malathi- from neighboring and other areas into the on (2g/m2) reduced the level of endemicity affected area and the destruction of all health of ZCL greatly in Khuzestan Province, south- facilities. According to the suggestions of west of Iran, thus epidemiological studies Leishmaniasis Committee of Iranian Ministry have become difficult. of Health, residual spraying with delthame- The absence or scarcity of sand flies rest- thrin at a rate of 25mg/m2 was applied on ing in sprayed rooms was taken as an indica- tents and in the remaining indoors twice, the tion of their susceptibility to insecticides as first in May and the second in late August, noted by Nadim and Amini in 1970. From 2004. Space spraying with Symprator (a com- his previous fauna survey in Bandar Abbas bination of Cypermethrin+ Tetramethrin and and Jask areas in southern Iran under the ap- Piperonyl butoxide) was also applied in dif- plication of DDT, dieldrin and later mala- ferent parts of the city once a week. Inter- thion spraying, Mesghali (1965) inferred that estingly, the comparison of the density of P. P. papatasi hitherto has not shown any in- sergenti before and after the occurrence of the secticide resistance, but the LC50 became earthquake showed that IRS with delthame- higher. Although they were absent in prem- thrin and space spraying with Symprator had ises freshly sprayed with malathion, they were reduced the density of the main vector signif- present outdoors. Almost the same remarks icantly. In early July coincident with the first were repeated in a paper dealing with P. peak, the density of this species was zero. In salehi in Baluchestan, southeast of Iran by late August coincident with second peak of Mesghali and Seyedi-Rashti in 1968. the species, the density had reduced more than In Neishabur, Nadim and Tahvildar-e- 8 fold in outdoors and 14 fold in indoors (In- Bidruni (1977) showed that DDT spraying at stitute of Public Health, unpublished data). a rate of 2gr/m2 in and around houses of Susceptibility tests by WHO standard method acute cases was highly effective on the con- on P. sergenti, collected in the city showed trol of P. sergenti but the endemicity re- that the mortality for diagnostic doses of DDT mained at a little bit higher level than in the 4% and deltamethrin 0.025% were 100%, period before the outbreak. which indicates that the field population of the In 1970 during an epidemic of ACL at Ja- species is susceptible to both insecticides. Ac- natabad district, northwest of Tehran, the pop- cording to the reports of the Disease Manage- ulation of P. sergenti was effectively sup- ment Center, the cases of leishmaniasis had pressed by house spraying with DDT 75% reduced sharply in comparison with the cases WP, at a rate of 2g/m2 and the transmission of the previous year (2003) from April to of the disease was halted (West Health Cen- October. Although we were expecting to ter of Tehran, 1970). have a serious epidemic of ACL in the city. 432 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

In 2005, IRS was applied with deltamethrin, health education. The incidence was 190/ 0.025g/m2 against P. sergenti in the houses 100000 in 1991 which dropped to 123/ with ulcers and their neighboring houses in 100000 in 1992. The difference was statisti- the city of Yazd, central Iran. The operations cally significant (P˃ 0.05). Taking into con- discontinued the transmission of ACL (Heath sideration that 75% of cases in the area were Center of Yazd Province, 2005). children between 1–4 age group, the inci- In order to control ACL in the endemic dence in this age group was compared before focus of Dehbakri, a village of Kerman Prov- and after intervention. The incidence before ince, southeastern Iran, IRS with deltamethrin intervention was 440/100000 which was re- WP 50% was applied at 25mg/m2 against P. duced to 71/100000 at the end of the study sergenti in April 2010. The reduction of the (P˃ 0.05) (Bokaei 1994). density of the species, the percent of blood- Indoor residual spraying is a cost effec- fed and gravid sand flies and also the inci- tive method of controlling of P. sergenti in dence of the disease were significant in the ACL foci during epidemic scenarios in Iran. treated area (Aghaei-Afshar et al. 2013). In temperate regions one round of spraying A field trial which was carried out during with one of available insecticides is needed 1991–1993 in 80 villages of Meshkinshahr but in tropical areas the second round of county, Ardebil Province, northwest of Iran, spraying should be carried out in mid or late reduced the incidence of ZVL due to the August in urban areas. Although spraying of combined application of IRS with DDT 75% houses and shelters is unlikely to be effec- WP 2g/m2 in houses with human or canine tive in ZCL and ZVL foci but one round of cases against P. kandelakii, along with the IRS is recommended in epidemic conditions. culling infected dog and the introduction of

Table1. Comparison results for the intervention against leishmaniasis vectors by indoor residual spraying in Iran, 1966–2010

Locality Year Insecticide Dosage Main Vector Impact Meas- Results Reference (gai/m2) urement Esfahan 1966– DDT 2 P. papatasi Reduced ZCL With discon- Nadim and Amini 1967 (one round) incidence tinuation of 1970, spraying Seyedi-Rashti incidence and Nadim 1973 increased

Khuzestan 1976 Malathion 2 P. papatasi As above Long term Nadim et al. 1977 (2 rounds) studies did not carry out Bandar-Abbas 1965 Malathion 2 P. papatasi As above As above Mesghali 1965 and Jask Neishabur 1976 DDT 2 P. sergenti Reduced ACL Endemicity Nadim and Tah- incidence remained at a vildare-Bidruni low level 1977

Yazd 2005 Deltamethrin 0.025 P. sergenti Transmission of Health Center of mg/m2 ACL reduced As above Yazd Province sharply 2005

433 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

Table 1. Continued… Janatabad 1970 DDT 2 P. sergenti Transmission of ACL cases West Health Cen- (Tehran) ACL discontin- disappeared ter of Tehran ued 1970

Bam 2004 Deltamethrin 25 P. sergenti Reduced density Reduced Institute of Public mg/m2 of sand fly vec- ACL inci- Health 2004 tor dence sharply Dehbakri 2010 Deltamethrin 25 P. sergenti Reduced den- Endemicity Aghaei-Afshar et mg/m2 sity, percent of remained at a al. 2013 blood fed and low level gravid sand flies

Meshkinshahr 1991 DDT 2 P. kandelakii Reduced density Incidence of Bokaei 1994 of the vector VL reduced

Applying chemicals in rodent bur- rows

In 1972, in five villages with a total pop- In 1974, rodent control by carbon mon- ulation of 1471 in the infected area of Esfa- oxide (CO) was carried out against ZCL at han, central Iran rodent burrows were dusted an area of 25 hectare in the village of Ader- with 75% DDT powder within a radius of manabad, Borkhar County, Esfahan Province. 300 meters around the villages, once every Although it was very effective on the control month (June, July, August and September) at of the population of great geribil, Rhombomys a rate of 0.5g/m2 in each burrow with a hand opimus, its effect on the reduction of the density dusting equipment. Dusting of the burrows of P. papatasi and incidence of the disease had no effect on the density of P. papatasi, was not evaluated (Deputy of Health, Esfa- the main vector of L. major in the area. This han University of Medical Sciences, 1974). could be due to the loose nature of the soil In 1978, the effect of insecticide spraying within the area such that the insecticide dust inside the rodent burrows against P. papatasi is quickly buried under soil upon falling to was evaluated in Borkhar area, Esfahan Prov- the ground, having no effect on sand flies ince, central Iran. About 8000 rodent holes in coming out from the depth of the burrows an area of 38 hectare were sprayed by DDT (Seyedi-Rashti and Nadim 1974). 75% WP (4.3gr in each hole), in two rounds, During 1972–1973 coincident with the ac- the first in late June and the second round in tive season of sand flies, rodent control op- early August. Monitoring the density of sand erations within 300 meters of the houses us- flies before and after the spraying showed ing poisoned bait consisting of 12–15 grams that although the operations could reduce the wheat containing 2.5% zinc phosphide was population of sand flies, the density returned carried out against ZCL once every month to its normal level after about a week. This from early June through September in 5 vil- could be due to the curving nature of rodent lages of Borkhar county, Esfahan Province, burrows and the resulting lack of access to central Iran. The method was very effective the depth of holes which are considered the in destroying the rodent reservoirs, but it was best resting place and oviposition of sand ineffective in the reduction of the incidence flies. Hence, this method has no robust effect of the disease. Its effect on the sand flies was in the reduction of sand fly population for a not evaluated in the area (Seyedi-Rashti and longer time (Moosavi 1979). Nadim 1974). Yaghoobi-Ershadi et al. (2000) conducted

434 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

a field trial for the control of ZCL during also conducted against ZCL in four villages 1997–1999 in the rural district of Badrood, around the city of Esfahan, central Iran. The Esfahan Province. Rodent control operations incidence of the disease decreased to 19.2 were carried out within a radius of 500 me- and 11.4 per thousand in areas treated with ters from the houses baited with 12–15 grams phostoxin and zinc phosphide respectively of wheat containing 2.5% zinc phosphide in and the density of P. papatasi in outdoors of each burrow. The evaluation showed that the the village treated with phostoxin was lower control program reduced the incidence of than indoors but its density in the village ZCL 12 fold in the treated village compared treated with zinc phosphide was higher in to the control at the end of the first year of outdoors (Akhavan et al. 2014). operation. Comparison of the density of P. papatasi, in the treated and the control area Impregnated Bed nets and Curtains indicated that the program was effective in the reduction of the density of this species in Nadim et al. (1995) evaluated the use of rodent burrows of the treated area. At the deltamethrin (K-othrin) impregnated bed nets, end of July, coincident with the first peak of 25mg per ml for the control of ACL in a re- P. papatasi its density was 261 per 30 traps stricted area in the city of Bam, Kerman Prov- in the control area which reduced to 75/30 ince southeast of Iran where, it was very hot traps in the treated area. In the second peak during the day in summer but rather good (end of September) the density was 717/30 weather at night. The results showed that the traps and 199/30 traps in the control and number of active cases decreased 2.6 fold in treated areas respectively. The operation was the intervention area but the transmission was also effective in disturbing the sex ratio of not interrupted. Non-significant difference was the species which was 172 and 21.9 in the observed between the density of P. sergenti control and treated areas respectively. There in indoors of the intervention and control areas. was also significant difference between fed During 2003–2004 in a study which was and unfed P. papatasi. It means that in the conducted in the hyperendemic area of CL intervention village the ratio decreased to due to L. major (Borkhar, Esfahan Province, one-third in comparison with the control area. Iran) efficacy of deltamethrin impregnated bed The method was ineffective on the density of nets and curtains, 25mg a.i/m2 polyester mesh P. papatasi in indoors in the study area (Mo- size 156 holes inch2 combination with a health tavalli-Emami 1998). education program were assessed in relation to A comparative study was carried out on ZCL control (Yaghoobi-Ershadi et al. 2006a). the effectiveness of Comavec and zinc phos- The results indicated that the nets could af- phide against the great gerbil, R. opimus in a ford a definite personal defence against sand hyperendemic focus of ZCL in central Iran fly bites and interrupted the transmission of during 2011–2012. The reduction rate of ro- ZCL in the intervention area. Non-impreg- dent holes in intervention areas with Co- nated bed nets and curtains did not give any mavec and zinc phosphide was calculated to protection against the disease. There was no be 48.5% and 58.2% respectively and the in- significant difference in monthly density of cidence of ZCL reduced significantly in the P. papatasi in indoors and outdoors among the treated areas. Comavec seems to be effective villages (P˃ 0.05). on the outdoor density of P. papatasi, the Moosa-Kazemi et al. (2007) carried out a main vector of L. major (Veisi et al. 2012). In field evaluation of deltamethrin-impregnated another study at the same time, a field eval- bed nets and curtains with 25mg/m2, in combi- uation of phostoxin and zinc phosphide was nation with a health education program against 435 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

ACL in the city of Mashhad, northeastern soldiers and emigrants. Based on official re- Iran. The area has a cooler climate in summer ports in 1982 more than 3000 military per- where people sleep in rooms at night. These sonnel referred to provincial health center of nets provided very good protection against Khuzestan for treatment. The density of P. sand fly bites and subsequently reduced the papatasi was in a high level, as in a study on transmission of ACL (4.5 fold) but there was hourly activity of sand flies, the number of non-significant differences in the reduction biting was reported 120 in each hour during the of the density of P. sergenti among different night around the city of Dezful, Khuzestan months. Non-impregnated bed nets and cur- Province. The available repellents such as tains did not provide any protection against Odomos (12% N, N-diethyl-benzamide) and the disease. Bioassays confirmed that the nets Autan (DEET 25%) were used as topical ap- treated with deltamethrin remained effective plication on face and hands by military per- for more than 3 months. High Performance sonnel to protect them from sand fly bites. Thin Layer Chromatography (HPTLC) analy- At the same time, a kind of insect repellent sis of deltamethrin residue on the impreg- called "Trench Pomade" which was a mixture nated bed nets showed that the residue of the of diethyl-toluamide (DEET 25%) and di- insecticide persisted well on impregnated nets methyl-phthalate (DMP 5%) in the ratio of at least 15 weeks after impregnation (Moosa- 5:1 respectively and had been produced at Kazemi et al. 2009). the School of Pharmacy, Tehran University A large scale installation of deltamethrin of Medical Sciences was widely used by impregnated screens and curtains, 25mg/m2, soldiers which provided 11h protection combination with passive and active case sur- against the bites of P. papatasi. About one veillance and treatment was assessed in the million tubes of Trench pomade was produced southeastern Iranian city of Bam during 2008– monthly and 4000 tubes were distributed 2010. The city which was devastated in 2003 every day among the personnel. Each soldier earthquake is known historically as a major was delivering one tube of the pomade twice endemic focus of ACL in the country. Com- in each month (Javadian E, School of Public parison of cumulative incidence between the Health, TUMS, personal communication). The intervention and control areas before and af- vehicle of this cream is Propylene glycol and ter installation indicated a significant differ- is still used by military personnel in the bor- ential reduction in the cumulative ACL inci- derlines of the country. dence in the intervention area. The authors Repellency effect of the plant Myrtle, Myr- believed that the use of impregnated screens tus communis essential oil and DEET against and curtains provided a good barrier in the way P. papatasi, the main vector of ZCL was eval- of sand flies entering the buildings (Noazin uated under laboratory and field conditions et al. 2013). during 2004–2005. The modified K&D (Klun and Debboun) apparatus with Wirtez method Insect repellents was employed in dose-response tests (calcu- lation of ED50 and ED90 values). Significant During the Iran-Iraq war (1980–1988) CL difference was observed between ED50 of due to L. major was prevalent among the sol- DEET and Myrtle essential oil (P˂ 0.05). diers, inhabitants and emigrants in the west DEET was found to be more effective as a of the country especially in the provinces of repellent than Myrtle essential oil against P. Khuzestan, Ilam, Kermanshah, and some parts papatasi (Yaghoobi-Ershadi et al. 2006b). To of Kurdestan (Marivan). Every year more than determine the protection time of Myrtle es- 10 thousand cases were reported among the sential oil and DEET at the laboratory, tests 436 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

were carried out on 9 volunteers for 10 hours methrin and its concentration was 850mg/ in 18 days. The mean protection time for m2. Statistical analysis showed non-signifi- Myrtel essential oil and DEET on P. papa- cant difference between the incidence of tasi was calculated to be 51min and 10h re- ZCL in the permethrin group and that in the spectively. Significant difference was ob- control group (P˂ 0.05) and did not protect served between the protection time of them volunteers (P˂ 0.0001). To find out the protection time from sand fly bites. of the repellency in the field, tests were car- ried out on 9 volunteers in the village of Impregnated dog-collars Matinabad, (Esfahan province) dur- ing 18 nights. The mean protection time of A pilot field study was implemented on Myrtle essential oil 20% and DEET 20% were the effects of deltamethrin-impregnated dog calculated to be 110 minutes, 28 seconds and collars against sand fly bites in Azar-Shahr 10 hours respectively. Significant difference District, an endemic focus of ZVL in Eastern was observed between the protection time of Azarbaijan Province, north-west Iran in 1999. them (P˂ 0.0001). Each dog was fitted with a plastic collar To calculate the protection percent of (length 48cm, weigh 20g) containing deltame- Myrtle essential oil 20% and DEET 20% a thrin 40mg/g and the protective value of col- total of 3981 female P. papatasi were collect- lars were tested against wild caught P. papa- ed on the treated volunteers by Myrtel essential tasi. For each test, the dog was caged in a net oil (1381 flies) and control (2600 flies). No with 70–100 wild caught sand flies over- flies were collected on volunteers against P. night. The results showed that the successful papatasi for 1h following application to hu- blood-feeding by P. papatasi was significantly man volunteers but it decreased to 50% after reduced about 80% (Halbig et al. 2000). 4h. The percentage of protection of Myrtel es- A matched community–based trial under- sential oil 20% and DEET 20% were calcu- took to investigate the epidemiological impact lated 46.41% and 100% correspondingly af- of applying collars to all domestic dogs in ter 10h during 18 nights. The mean number the counties of Kalaybar and Meshkin-Shahr of bites on the treated legs with Myrtel essen- in north-west Iran during 2000–2001. The area tial oil was 7.69+_4.51 bites human-h, whereas is considered as the main focus of ZVL in those figures on the control were 14.33+_3.95 the country. Eighteen villages including nine bites/human-h. A significant difference was treated and nine as control were selected. observed between the protection percent of Leishmania infantum zymodeme MON-1 is the Myrtel essential oil and DEET (P˂ 0.0001) causative agent of the disease and the proba- (Jahanifard 2006). ble sand fly vector is P. kandelakii in the area. Saberi et al. (2011) studied the efficacy of Dog collars consisted of 65cm strip of white DEET repellent pen against ZCL in a mili- polyvinyl chloride weighing 25g, impreg- tary area in Esfahan, central Iran. The trial nated with deltamethrin 40mg/g. The authors was carried out on 430 high school students. reported that serconversion rate in children The results showed non-significant efficacy was 1.49% in the intervention villages and on the prevention of ZCL. 2.4% in control villages. Leishmanian skin Asilian et al. (2003) evaluated the efficacy test conversion was also lowered but not sig- of permethrin-impregnated uniforms for the nificantly. The seroconversion rate in dogs of prevention of ZCL among 324 Iranian sol- the intervention villages was also significantly diers in the hyperendemic area of Esfahan. reduced (Mazloumi-Gavgani et al. 2002). The uniforms were impregnated with per- The efficacy of deltamethrin-impregnated 437 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

dog collars (Scalibor) was evaluated against after 24h. The blood-fed or unfed conditions P. papatasi in an endemic focus of ZVL in of sand flies were determined 2h after expo- Bojnord County, north Khorasan Province, sure to the dogs under stereomicroscope. The northeastern Iran during 2006–2007. In this results showed that the feeding rate of sand experiment 6 healthy dogs with similar age, flies on treated dogs was 3.3 fold lower than sex, weight and race were selected and ran- control and the inhibition of feeding rate on domly classified in two groups as treated and treated dogs was 1.8 fold higher than con- untreated. At the beginning of the transmis- trol. The difference between total mortality of sion season, 3 dogs received collars and the treated and control groups was highly signifi- other group was considered as control group. cant (P= 0.0001) (Jalilnavaz et al. 2016). Two weeks after fitting the collars, one of the treated and untreated dogs were exposed Susceptibility of sand flies to insec- to the bites of wild caught P. papatasi in the ticides evening for 2h under the bed net biweekly. In order to assess the mortality of sand flies, Studies on the susceptibility level of P. they were recaptured at the end of the expo- papatasi to insecticides started in 1970 and sure time and transferred into cups and main- continuing in some foci of ZCL in the coun- tained at optimal condition for 24h. Data try. Seyedi-Rashti et al. (1970) evaluated the analysis revealed that the blood-feeding in- susceptibility of field population of P. papa- dex of P. papatasi was between 13.4–27.6% tasi strain from unsprayed area of Mashhad for dogs with collars and 54.2–59.3% for the by WHO standard method in northeastern dogs of control group which showed signifi- Iran in August 1970. The baseline LC50 val- cant difference (P˂ 0.005). The index of blood- ue for DDT and dieldrin was calculated to be feeding inhibition were calculated to be be- 0.47% and 0.54% respectively (Seyedi-Rashti tween 51.3–66.2% and 37%-44.8% for col- 1971). In susceptibility tests carried out on this lared and collarless dogs respectively and species from the Esfahan area, central Iran showed a significant difference (P˂ 0.01). the LC50 for DDT was 0.47% in September The range of combined effects (inhibition of 1976 (Soltani 1977), indicating no develop- blood-feeding and mortality of P. papatasi) ment of resistance. Another survey was per- was between 72.37–86.62% for collared dogs formed by WHO standard method on wild and 40.74–45.83% for control dogs (Rama- caught P. papatasi from human dwellings in zani Awal et al. 2009). Mashhad (northeast), Esfahan (central Iran) and In 2013, the pour-on formulation of flume- Khuzestan (southwest) during 1985–1986. The thrin on dog (with same race, sex and age) results showed that the LC50 value for DDT was evaluated against blood- feeding and had increased to 2.3% and 3% in Mashhad mortality of sand flies in endemic focus of and Esfahan respectively, disclosing the ex- ZVL in Meshkinshahr, northwest of Iran. Be- istence of selection pressure in the lack of fore the application of flumethrin, direct ag- public health insecticide use (Seyedi-Rashti glutination test (DAT) was used for deter- et al. 1992). mining the positive or negative cases of dogs. Yaghoobi-Ershadi (1993) provided evidence The treated and control dogs were exposed of tolerance of P. papatasi to 4.0% DDT fol- with wild sand flies for 2h under the bed net lowing a standard WHO technique in Esfahan. (2x2x2 meters) once every 20 days during In this program 40 series of susceptibility tests May-September. Both alive and dead sand were carried out on a total of 1248 fed P. flies were transferred in netted cups to the papatasi from 4 villages in the rural district laboratory and their mortality was assessed of Borkhar. Lt50 and Lt90 values were calcu- 438 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

lated to be 18.12 and 63.31min respectively. ceptible to these insecticides in different stud- The mortality rate after one hour exposure to ied areas (Yaghoobi-Ershadi et al. 2003, 4.0% DDT and the 24h recovery period was 2007, Akhavan et al. 2007, Aghaei et al. 2011, 88.8%. When the exposure time increased to Saeidi et al. 2011). 90 and 120min, the mortality rate was 95.2% Several susceptibility tests which have been and 98.8% respectively. Appearance of toler- undertaken on P. sergenti, the main vector of ance on P. papatasi in the area was due to the leishmania tropica in the cities of Mashhad irregular and excess use of Chlorinated insec- (northeast), Kerman and Bam (southeast) dur- ticides in agriculture. The mortality rate of this ing 1970–2010 showed that it was suscepti- species after one hour exposure to 4.0% diel- ble to DDT, dieldrin and deltamethrin (Aghasi drin was 100%. At the same time 32 series of 1996, Yaghoobi-Ershadi and Akhavan 1999). tests were conducted on 1112 P. papatasi In 1994, susceptibility tests were conducted against DDT 4.0% in two villages located in the on P. kandelakii and P. perfiliewi, the prob- rural district of (73–98km, southeast able vectors of ZVL in Meshkinshahr and of Esfahan). Lt50 and Lt90 values was cal- Germi counties, Ardebil province (northwest), culated to be 20.51 and 43min respectively Iran. The results revealed that the both spe- and the mortality rate after one hour exposure cies were susceptible to the insecticides (Rassi and 24h recovery period was 98.61% so it and Javadian 1998). was found to be susceptible to DDT 4.0% (Yaghoobi-Ershadi and Javadian 1993). Concluding remarks In 2001, the tests with WHO technique which was performed in the rural district of The national strategy arranged by the Ira- Borkhar (Esfahan) showed that the suscepti- nian government emphasizes case detection bility of P. papatasi to DDT 4.0% has been and treatment for ACL and ZVL. Results of returned because the mortality rate after one many scientific works in the country state hour exposure was calculated to be 100%. This that, whether integrated vector management was achieved due to the low use of Chlorin- is needed, IRS remains the main support for ated insecticides in agriculture, during the vector control in epidemics which provides a last 9 years in the area (Yaghoobi-Ershadi, cheaper and more practical solution to pre- Tehran University of Medical Sciences, un- vent cases of leishmaniasis. House spraying published data). During 1993–2001 the same with insecticides, although being able to com- study was carried out in the provinces of Fars bat an outbreak, cannot be used on a long- (southwest), Kerman (southeast) and Badrood term basis in urban areas to maintain trans- area in Esfahan and Lt50 ranged between mission at a low level. Well organized town 5.5–29.7 minutes and Lt90 between 18.5–58 planning expansions based on environmental minutes respectively. Phlebotomus papatasi protection measures such as a lack of waste was found to be susceptible to DDT in all of management or open sewage, the presence of these areas (Aghasi 1996, Yaghoobi-Ershadi idle land among the new construction homes, and Akhavan 1999, Rassi et al. 2000). inadequate garbage collection and sanitation, Susceptibility tests which were performed crowded suburban areas with residents of low again during 2002–2013 on P. papatasi against socio-economic levels and with existence with DDT 4%, deltamethrin 0.05% and 0.025% and domestic animals are the key to prevention of propoxur 0.1% by WHO standard method in leishmanisis in urban areas. As they provide a Sabzevar (northeast), Esfahan (Central), Bam, good source for high phlebotomine density and Baft and Dehbakri (southeast) showed that the favorable conditions for disease transmission. field population of the species was still sus- Impregnated bed nets and curtains may 439 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

provide the best way out in rural areas where ing indoor Residual spraying (IRS) with transmission is largely occurs outdoors. The deltamethrin in a new focus of anthro- critical studies such as biting behavior of dif- ponotic cutaneous leishmaniasis (ACL) ferent sand fly species, their resting and breed- in Iran. Asian Pac J Trop Dis. 3(1): 5–9. ing places, the type of plants which provide Aghasi M (1996) Present status of anthro- sugar meal, potential reservoir hosts along ponotic cutaneous leishmaniasis in Ker- with community participation and education man, southeast Iran (MSPH thesis) should be studied in leishmaniasis foci which School of Public Health, Tehran Uni- will help in the battle against sand fly vec- versity of Medical Sciences, No. 1968 tors and reduce the cost of intervention. New Tehran, Iran (in Persian). methodological advances, such as geograph- Akhavan AA, Yaghoobi-Ershadi MR, Hasibi ical information systems and remote sensing F, Jafari R, Abdoli H, Arandian MH, can make a positive contribution to these ef- Soleimani H, Zahraei-Ramazani AR, forts. Increasing the awareness of physicians Mohebali M, Hajjaran H (2007) Emer- and medical staff on the ecology and control gence of cutaneous leishmaniasis due of sand flies and close collaboration between to Leishmania major in a new focus of health authorities and researchers are required southern Iran. Iran J Arthropod-Borne to achieve the best control measures. Health Dis. 1(1): 1–8. education activities focused on sand fly con- Akhavan AA, Veisi A, Arandian MH, Vatan- trol among inhabitants living in foci of leish- doost H, Yaghoobi-Ershadi MR, Hos- maniasis, early reporting of active cases by in- seini M, Abdoli H, Heidari K, Sadjadi dividuals, disease mapping of ZCL, ACL, A, Fadaei R, Ramazanpour J, Aminian ZVL and qualified staff for vector control K, Shirzadi MR, Jafari R (2014) Field are critical points in effective prevention and evaluation of phostoxin and zinc phos- control of leishmaniasis. phide for the control of zoonotic cuta- neous leishmaniasis in a hyperendemic Acknowledgements area, central Iran. J Vector Borne Dis. pp. 307–312. Alexander B, Maroli M (2003) Control of Sincere thanks are extended to Professor phlebotomine sand flies. Med Vet En- KP Chang (Chicago Medical School/RFUMS. tomol. 17: 1 18. USA) for his encouragement the author to write – Asilian A, Sadeghinia A, Shariati F, Imam the present review and Prof A Nadim (Depart- Jome M, Ghoddusi A (2003) Efficacy ment of Epidemiology and Biostatistics, School of permethrin-impregnated uniforms in of Public Health, Tehran University of Medical the prevention of cutaneous leishmani- Sciences) for kindly commenting on an earlier asis in Iranian soldiers. J Clin Pharm draft of the manuscript. I also would like to Ther. 28: 175 178. thank all scientists who have worked on this – Bokaei S (1994) Seroepidemiological survey matter for ages whose work is pointed out here. among the dogs of visceral leishmania- sis in Meshkinshahr focus and evalua- References tion of operational disease control in human (Ph.D Dissertation), School of Aghaei-Afshar A, Vatandoost H, Sharifi I, Ras- Public Health, Tehran University of M- si Y, Abai MR, Oshaghi MA, Yaghoobi- edical Sciences, No. 2224, Tehran, Iran Ershadi MR (2013) First determination (in Persian). of impact and outcome indicators follow- Halbig P, Hodjati MH, Mazloumi-Gavgani AS, 440 http://jad.tums.ac.ir Published Online: October 04, 2016 J Arthropod-Borne Dis, December 2016, 10(4): 429–444 MR Yaghoobi-Ershadi: Control of Phlebotomine …

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