One of the most significant modern day efforts to prevent and control an arthropod-borne disease during a military deployment occurred when a team of U.S. military entomologists led efforts to characterize, prevent, and control leishmaniasis at Tallil Air Base (TAB), Iraq, during Operation Iraqi Freedom. Soon after arriving at TAB on 22 March 2003, military entomologists determined that 1) high numbers of sand flies were present at TAB, 2) individual soldiers were receiving many sand fly bites in a single night, and 3) Leishmania parasites were present in 1.5% of the female sand flies as determined using a real-time (fluorogenic) Leishmania-generic polymerase chain reaction assay. The rapid determination that leishmaniasis was a specific threat in this area allowed for the establishment of a comprehensive Leishmaniasis Control Program (LCP) over 5 mo before the first case of leishmaniasis was confirmed in a U.S. soldier deployed to Iraq. The LCP had four components: 1) risk assessment, 2) enhancement of use of personal protective measures by all personnel at TAB, 3) vector and reservoir control, and 4) education of military personnel about sand flies and leishmaniasis. The establishment of the LCP at TAB before the onset of any human disease conclusively demonstrated that entomologists can play a critical role during military deployments.
sand fliesleishmaniasisIraqsurveillancecontrol
In this article, we provide an overview of the general situation that the U.S. Military encountered at Tallil Air Base (TAB), Iraq, in March 2003 and discuss the factors that led to the establishment of a Leishmaniasis Control Program (LCP) at TAB. We also describe each of the four main components of the LCP (vector surveillance, personal protective measures [PPM], sand fly and reservoir control, and soldier education). Although brief summaries of this program have been published separately (Coleman et al. 2004; 2005), we believe that it is important to provide a comprehensive overview of one of the most significant modern day efforts to prevent and control an arthropod-borne disease during a military deployment. Although much of this article relies on anecdote, we believe that this information has both scientific as well as historical value. In the series of articles to follow, we will provide detailed results about the specific components of the program, including: 1) the general biology of phlebotomine sand flies at TAB, 2) our evaluation of a variety of surveillance devices for the collection of sand flies, 3) the impact of environmental conditions on sand fly activity, 4) the efficacy of a variety of area spray measures on sand fly abundance, 5) the efficacy of a variety of residual spray measures on sand fly abundance, 6) testing of sand fly populations for the presence of Leishmania parasites and the genetics of Leishmania parasites isolated from sand flies, 7) our evaluation of PPM as a means of protecting soldiers from sand fly bites, and 8) our overall evaluation of the risk of leishmaniasis at TAB and the efficacy of the LCP.
Historically, leishmaniasis has been a major cause of infectious disease morbidity among military personnel deployed to the Middle East (Kinnamon et al. 1979, Cross et al. 1996). During World War II, 1,000-1,500 cases of cutaneous leishmaniasis (CL) and 50-75 cases of visceral leishmaniasis (VL) occurred in allied forces in the Middle East (Most 1968). During the "Six-Day War" in 1967, up to 50% of Israeli forces operating in parts of the Jordan Valley were infected with leishmaniasis (Naggan et al. 1970), and 20% (12/60) of at-risk personnel assigned to the Multinational Force and Observers (MFO) in the Sinai desert of Egypt in 1990 developed CL (Fryauff et al. 1993). During Operation Desert Storm (ODS), 20 cases of CL and 12 cases of viscerotropic leishmaniasis were diagnosed in the 697,000 allied soldiers deployed to the Arabian Peninsula in 1990 and 1991 (Gasser et al. 1991, Magill et al. 1993, Martin et al. 1998). Most recently, an outbreak of CL caused by Leishmania major Yakimoff and Schokhor occurred in U.S. Military personnel deployed to Iraq during Operation Iraqi Freedom (CDC 2003, 2004; Pehoushek et al. 2004; Weina et al. 2004; Berman 2005; Willard et al. 2005). As of November 2004, 1,178 cases of CL had been identified in U.S. Military personnel (Lay 2004); however, this number is probably an underestimate, and the actual number of cases is estimated to be between 1,500 and 2,000 cases as of 1 January 2006 (P.J.W., personal communication).
Leishmaniasis is a parasitic infection caused by various species of Leishmania. Leishmania parasites are transmitted by the bite of an infected female sand fly. Although primarily a zoonotic disease found in rodents and canids, some species of Leishmania may survive for decades in asymptomatic infected people (Magill 1995). In Iraq, the primary forms of leishmaniasis are CL and VL. CL, caused by L. major, Leishmania tropica (Wright), or both, in Iraq, is manifested as skin lesions or nodules (Weina et al. 2004). Although CL is normally self-healing, it can create serious disability and permanent scars. Individuals who have recovered from CL usually exhibit immunity to reinfection by the species of Leishmania that caused the disease (Magill 1995). Humans are the sole proven reservoir of L. tropica, with transmission from person to person by the vector (WHO 2003). In rural areas, yet to be determined animals are thought to be the reservoirs of L. tropica; however, the full transmission cycle of L. tropica is still under investigation in various foci (Jacobson 2003). For L. major in the Middle East, gerbils, Meriones crassus Sundevall and Meriones lybicus Lichenstein, and the fat sand rat, Psammomys obesus Cretzschmar, are the primary animal reservoirs, and Phlebotomus papatasi Scopoli is the primary vector (Yaghoobi-Ershadi and Javadian 1996, YaghoobiErshadi et al. 2005). Between 1989 and 2001, the reported incidence of CL in Iraq ranged from a low of 2.3 per 100,000 (625 total cases) in 2001 to a high of 45.5 per 100,000 (8,779 total cases) in 1992 (WHO 2003).
VL, primarily caused by Leishmania donovani Laveran and Mensel and Leishmania infantum Nicolle, is characterized by irregular fever, weight loss, swelling of the liver and spleen, and anemia. It is the most severe form of leishmaniasis and is usually fatal if left untreated (Magill 1995). The incubation period for VL ranges from months to years. The intensity of infection is dependent on partial immunity resulting from previous exposure, concomitant illness, malnutrition, and other factors (WHO 2003). The vectors of VL in Iraq have not been fully elucidated; however, Phlebotomus alexandri Sinton has been incriminated in the transmission of L. infantum (Sukkar 1974, Sukkar et al. 1985). Reservoirs of L. infantum are believed to be domestic dogs, jackals, foxes, and potentially rats, whereas humans are the reservoirs of L. donovani (Armed Forces Pest Management Board 1999). An infected human host may serve as a source of infection to sand flies as long as the parasite persists in the circulating blood or skin, even after clinical recovery. Historically, the most important endemic area for VL in Iraq was in the center of the country and in the Greater Baghdad area. Since 1991, the disease has extended to new areas rarely affected before, such as Missan, Thi-Qar, and Basrah governates in southeastern Iraq (WHO 2003). Between 1989 and 2001, the reported incidence of VL in Iraq ranged from a low of 2.6 per 100,000 (491 total cases) in 1989 to a high of 20.0 per 100,000 (3,866 total cases) in 1992 (WHO 2003). During ODS, 12 cases in total of VL due to L. tropica were reported in U.S. soldiers deployed to Saudi Arabia (Hyams et al. 1995). None of these individuals had cutaneous manifestations normally associated with this parasite.
Currently, there are no prophylactic drugs or vaccines that can be used to prevent leishmaniasis (Magill 1995). Therefore, the prevention of leishmaniasis relies upon preventive measures taken to minimize exposure to biting sand flies (Martin et al. 1998). Transmission zones can be extremely focal because of the presumed limited flight range of vector species (Magill 1995). Infection in military personnel occurs when activities such as desert operations expose service members to foci where infected sand flies are found (Martin et al. 1998). Measures used to minimize sand flies bites include application of residual insecticides on tents and buildings, ultralow volume (ULV) space spraying of insecticides by using truck-mounted or aerial spray equipment, and use of PPM such as application of insect repellent on exposed skin, donning of permethrin-treated clothing, and use of insecticide-treated bed-nets (Alexander and Maroli 2003). Because the breeding sites of sand flies are generally unknown, control efforts that focus on immature stages are currently not feasible.
Terrain and Environmental Conditions at TAB
TAB (30° 56′ N, 46° 06′ E) is located 160 miles southeast of Baghdad and 140 miles northwest of Kuwait City (Fig. 1). The largest city in the immediate vicinity of TAB is An Nasiriyah, located ≈17 km to the northeast. TAB is a major tactical airfield in southern Iraq. It encompasses an area of ≈30 km2 and has a fenced perimeter of ≈22 km. It is located in a region of semiarid desert (Fig. 2). The terrain is flat with 120 degrees in the shade, and the open fields and roads bear craters large enough to swallow small trucks. In March 2003,