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Sand fly surveillance and control on Camp Ramadi, Iraq, as part of a leishmaniasis control program

2013; Wiley; Volume: 38; Issue: 2 Linguagem: Inglês

10.1111/j.1948-7134.2013.12059.x

1948-7134

Craig A. Stoops, Bryan Heintshcel, Shabaan S. El-Hossary, Rania M. Kaldas, Peter J. Obenauer, Mohammad Farooq, Jeffrey T. Villinski,

Viral Infections and Vectors

Vector-borne diseases are a serious health threat to U.S. troops stationed around the world. U.S. forces deployed to Iraq following the 2003 invasion experienced serious risk of infection by several vector-borne pathogens, specifically cutaneous (CL) and visceral leishmaniasis (VL) (Aliaga and Aronson 2007). Camp Ramadi, a U.S. military Forward Operating Base, was established in 2003 at the Al Anbar provincial capital of Ramadi, approximately 110 km west of Baghdad. In Iraq the total number of cases of CL reported per year from 2004 to 2008 was 1,655 and for VL was 1,711 (Alvar et al. 2012). In Al Anbar province in 2008, the estimated incidence of CL and VL was <1 per 10,000 (Alvar et al. 2012). Because of the war, the number of cases of both CL and VL was most likely underreported in Al Anbar and all provinces of Iraq (Alvar et al. 2012). Because of the risk of vector-borne diseases, each large U.S. military facility, such as Camp Ramadi, had a vector control program operating throughout the year. As part of a base-wide vector control program, unbaited Center for Disease Control and Prevention (CDC) light traps were placed at three locations on Camp Ramadi between April and August, 2009 to gather baseline population estimates of adult sand flies and monitor the success of subsequent control measures. This paper reports sand fly collections over the five-month period, whether they were positive for Leishmania, and describes efforts to control sand fly populations using ultra-low volume (ULV) insecticide applications. Three sites on Camp Ramadi were established for trap placement in areas where U.S. troops worked and lived. Site one was in a grove of palm trees near troop living quarters and the base medical clinic. Site two was in a plot of scrub vegetation near the helicopter landing pad, and site three in tall vegetation near buildings occupied by the base Commander. All three sites had active rodent burrows. Traps were placed 1 m above ground and deployed overnight (from 18:00 until 06:00) approximately every other day. Captured sand flies were taken to the base Preventive Medicine office, frozen, sorted by sex, and counted. Dried specimens were sent to the U.S. Naval Medical Research Unit 3 in Cairo, Egypt, for identification and pathogen testing. As outlined in the Multinational Force Iraq-I Pest Management Plan, control operations were implemented when the number of sand flies collected in unbaited CDC light traps exceeded a threshold of 15 and when the prevailing wind speed was less than 5 mph as measured by a Kestrel 4000™ (Kestrel Meters, Birmingham, MI) weather meter (Blow et al. 2007). Spray operations were carried out after sunset between 21:00 and 05:00. Two pyrethroid insecticides were used: Scourge® Insecticide (Bayer Environmental Science, Research Triangle Park, NC, U.S.A.) and Anvil® 10+10 ULV (Clarke Mosquito Control Products, Roselle, IL, U.S.A). Scourge® was used from April to June and Anvil® from June to August. All safely accessible areas of Camp Ramadi had to be sprayed in their entirety as U.S. troops and civilian personnel worked on nearly every part of the base 24 h per day. Therefore, we were not able to establish an untreated area to compare the number of sand flies in sprayed and unsprayed areas. Due to security outside Camp Ramadi, we were unable to access unsprayed areas off the installation. Trap data were transformed using log (x+1) because there were nights when one or more traps collected no sand flies (Kline et al. 2006). Table 1 provides transformed trap collections before and after ULV applications combined to calculate a mean catch for each night before and after ULV operations. Mean catches, pre-spray and post-spray, and total catches before and after ULV operations were compared with Student's t-test using JMP statistical package (Version 9.02, SAS Inc., Cary, NC). From April to August, 2009, traps were set 57 times and 6,686 sand flies were collected at the three sites combined, of which 6,366 were identified to genus. For identified sand flies, 1,269 (20%) were from species of Phlebotomus; the remainder (5,097, 80%) were Sergentomyia. Female Phlebotomus spp. composed 10% (n= 636) of the total catch, whereas females of Sergentomyia spp. represented 44% (n=2,801) of the total catch. Consistent with seasonal fluctuations of sand fly populations (Coleman et al. 2007), capture rates increased from April to July (April: n=481, May: n=1,109, June: n=1,638, July: n=1,842) and declined in August (n=1,616). Although we did not identify captured sand flies to species level, previous surveys in Iraq indicate three predominant species of Phlebotomus: P. alexandri, P. papatasi, and P. sergenti (Coleman et al. 2007). All three species are known or suspected vectors of Leishmaniasis in addition to biting pests and should be controlled when necessary (Coleman et al. 2007). During five months of the sand fly season, 21 spray operations were conducted by Camp Ramadi vector control contract personnel using a Clarke Pro-Mist ULV machine (Clarke Mosquito Control Products, Roselle, IL): April (n=2), May (n=6), June (n=6), July (n=3), and August (n=4). After analyzing the transformed means of trap captures from all three sites combined before and after a ULV application, there was no significant difference between total pre- and post-spray means using Student's t-test (Table 1). Only the pre- and post-spray means on 25 May had a p-value < 0.05. When we graphed seasonal data as part of a preliminary analysis near the end of the control season, trap collections appeared to be related to something other than our ULV insecticide applications. Based on the observed collection patterns, we suggest that moon phase and illumination influenced trap collections due to the essentially zero cloud cover in Ramadi during the control program. Moon brightness influences trap capture when collecting sand flies with light traps (Santos De-Marco et al. 2002). Figure 1 shows percent moon illumination for Baghdad from March to August, 2009 (http://www.timeanddate.com; Time and Date AS, Stavanger, Norway) against the total number of sand flies collected each trap night from April to August. During the moon cycles, as percent moon illumination increased, trap catch decreased; trap catch increased with decreasing moon illumination. The amount of time the moon is visible in the night sky, not just brightness, may also influence unbaited light trap catches (Santos De-Marco et al. 2002). Moon illumination and other environmental factors, such as temperature and wind speed, also affect sand fly behavior (Alexander 2000). We did not measure environmental factors during the control season, but such factors cannot be ruled out as possible causes of increased or lowered trap captures (Colacicco-Mayhugh et al. 2011). Because known Leishmania reservoirs (jackals, dogs, and rodents) were prevalent on the base, we tested 636 female Phlebotomus spp. (grouped into pools) for Leishmania DNA using real-time PCR (Villinski et al. 2008). None of the pools were positive for Leishmania DNA. Sand flies in Iraq are most active on warm, clear nights with little wind (Colacicco-Mayhugh et al. 2011), conditions that also are favorable for applying ULV-based adulticides (WHO 2006). Space spraying with ULV is widely used to control sand flies, but few rigorous studies have evaluated its efficacy (WHO 2006). Based on our surveillance program, we do not know whether our ULV missions had any impact on sand fly populations. Coleman et al. 2011 found that various insecticide applications, including ULV, did not have a significant effect against sand flies in southern Iraq. Based on field trials in Kenya, however, ULV applications of insecticides killed sand flies (Britch et al. 2011). Our insecticide applications were part of an actual vector control program lacking an untreated area to serve as a control, which complicates the interpretation of our results. Because sand flies are biting pests, as well as Leishmania vectors, we expected sand fly levels to be near zero following ULV applications. The increasing populations of sand flies, which resulted in peak numbers during July (Figure 1), would have been expected in areas without any control program in place (Coleman et al. 2007). More research is needed to determine the optimal dose and spray parameters for conducting ULV insecticide applications against sand flies. Surveillance programs for monitoring control of sand flies in desert habitats should supplement light trapping with other collection methods (Obenauer et al. 2011). We thank A.G. Wheeler Jr. and several anonymous reviewers for thorough reviews of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, nor the U.S. government. First, second, and fifth authors are military service members of the U.S. government. Other coauthors are employees of the U.S. government. This work was prepared as part of our official duties. Title 17 U.S.C. section 17 provides that "Copyright protection under this title is not available for any work of the United States Government." Title 17 U.S.C. section 101 defines a U.S. government work as a work prepared by a military service member or employee of the U.S. government as part of that person's official duties.