By James A. Dennett, Ph.D., and Mustapha Debboun, Ph.D., B.C.E.
By In 2015, Harris County, Texas, celebrated the 50th anniversary of the formation of its organized mosquito abatement activities that, through the years, has gone by the names of Harris County Mosquito Control District (1965-95), Harris County Public Health & Environmental Services, Mosquito Control Division (1995-2016), and most recently, Harris County Public Health, Mosquito & Vector Control Division (HCPH-MVCD) (2016-present).
HCPH-MVCD has had eight directors with the direct responsibility of conducting year-round arbovirus surveillance through mosquito collections and evidence-based mosquito control activities within Houston, the fourth-largest city in the nation, and Harris County, the third most populous county in the United States, which spans nearly 1,800 square miles and has an estimated population of 4.5 million people.
Throughout the 52 years that HCPH-MVCD has been in operation, significant events, occurring in Texas and abroad, have helped shape its overall mission, operational methodologies and surveillance techniques through adaptation, innovation and incorporation of existing integrated mosquito control technologies. The following highlight some of the more notable events through the five decades and their impact on HCPH-MVCD.
CURRENT RESEARCH. Research has always played an important role in helping HCPH-MVCD improve mosquito surveillance and control operations by using and incorporating current technologies (see figure 1). Internal and external collaborative research activities have covered numerous topics including mosquito bionomics, comparative mosquito trap testing, new control method evaluations, mosquito host feeding studies, ULV aerosol characterization and adulticide field efficacy testing.
Over the years, HCPH-MVCD has partnered with the University of Texas Medical Branch-Galveston (UTMB-G) and its world-renowned virologists in a West Nile virus (WNV) research grant from 2003 to 2010, with concentration on arbovirus ecology and evolution. In December 2016, the CDC awarded $10 million to UTMB-G to establish the Western Gulf Center of Excellence for Vector-Borne Diseases. The HCPH-MVCD is an important partner of this center and grant that will conduct research on Zika, other arboviruses and a number of vector-borne diseases present in the region.
The HCPH-MVCD is also currently collaborating with Microsoft’s Project Premonition on the development and field testing of a Mosquito Smart Trap to integrate into a large mosquito surveillance program in Harris County and the city of Houston to collect large amounts of mosquito data and selectively capture specific mosquito species, understand foraging behavior and improve epidemiology. In addition, this innovative trapping system will conceptually not only capture mosquitoes, but identify the mosquito species collected, their blood-meal host preferences, arboviruses they carry, and provide much more detail about the mosquito, including the time it was caught, temperature and humidity, etc. (See figure 2.)
IMPACT OF ARBOVIRUSES. Of course, the impact of arboviruses in Harris County and Houston, Texas, has played a major role in the work HCPH-MVCD does.
Saint Louis Encephalitis. The Saint Louis encephalitis (SLE) epidemic in the Houston, Texas, metropolitan area during 1964 was comparable in size to SLE outbreaks that occurred in the Lower Rio Grande Valley 10 years earlier in 1954. The Houston epidemic occurred from June 27 to Oct. 3, 1964, for 15 weeks, with peak number of cases in the 10th week (Aug. 29), with 243 cases (suspected and/or confirmed) and 27 deaths (not including 14 cases outside Houston city limits). Incidence and mortality rates were 19.5 cases/100,000 population, and 2.2 deaths/100,000 population, respectively, with 11.1 percent case fatality ratio (Luby et al. 1967). In the end, there were 376 confirmed cases of SLE and 34 deaths (Parsons 2003).During the 1964 epidemic, the city of Houston provided residents 0.5 percent malathion through disbursement at 55 local fire stations (accounting for 151,000 gallons applied to private properties), 15 trucks equipped with power sprayers (provided by Communicable Disease Center’s San Antonio Aedes aegypti (L.) eradication project) were used for larviciding local ditches with diesel, and a U.S. Coast Guard helicopter applied larvicide and adulticide in the form of 5 percent malathion and 3 percent benzene hexachloride dusts (Anon. 1965).
In response to the epidemic, county officials authorized the formation of Harris County Mosquito Control District, aided by a five-member advisory board, on Nov. 3, 1964. Harris County then budgeted $400,000 for the newly formed district in 1965 (Anon. 1965). Its primary responsibility was to provide control of disease vectors with its operational foundation similarly based upon available mosquito surveillance and control techniques that were being used in Florida, with additional internal policies on insecticide use and environmental protection, that laid the groundwork for the insecticide resistance management (IRM) program that exists today (Bartnett 1990). Upon startup, the District proposed the creation of an encephalitis surveillance program, and an encephalitis laboratory, which was originally within the City of Houston Health Department, but later moved to the District (Bartnett 1990).
Twenty-two SLE isolates from 69,387 Culex quinquefasciatus Say were collected from August-October during the Houston epidemic, with 12 isolates from 6,760 Cx. quinquefasciatus collected Aug. 23-29 (10th week of the epidemic) (Sudia et al. 1967). This immediately elevated the status of Cx. quinquefasciatus as the primary regional vector of SLE for 38 years, until 2002 when SLE all but “disappeared” and West Nile virus (WNV) was first detected within Harris County where it remains the primary vector of now endemic WNV.
Regionally, simultaneous epidemics of SLE occurred in Texas during 1966, with 76 confirmed cases in Corpus Christi and 145 in Dallas. During both outbreaks, emergency operations using aerial applications of malathion (3.08 oz/acre) were conducted (Williams et al. 1975, Hopkins et al. 1975). During the Dallas epidemic, ground-based control operations used insecticidal fogs of 2 percent malathion/diesel and applications of 3 percent benzene hexachloride or 5 percent malathion dusts (Hopkins et al. 1975). Shortly after the epidemic, Corpus Christi began fogging all storm drain systems weekly/biweekly with 5 percent malathion/diesel (Williams et al. 1975).
Subsequent SLE outbreaks have occurred in the Houston area through the years: 1975-76 (58 cases/11 deaths), 1980 (53 cases), 1986 (28 cases), and 1990-91 (65 cases) (Lillibridge et al. 2004). Houston had 10 SLE epidemics over a 26-year period, occurring at three-year intervals from June through November, usually occurring between mid-July through mid-August (Sprenger 1992).
West Nile Virus. WNV was detected in Harris County for the first time in 2002, and at year’s end, 851 pools of Cx. quinquefasciatus out of 6,093 pools tested (13.97 percent) were confirmed positive (Lillibridge et al. 2004). Since 2002, WNV activity in mosquitoes has varied greatly through the years ranging from 23 confirmed WNV mosquito pools in 2008 to 1,286 confirmed pools in 2014 (Randle et al. 2016). According to U.S. Geological Survey data, during the period 2003-2016, there were more than 300 WNV human cases in Harris County.
TREATMENT OPTIONS. Over the years, there have been a variety of mosquito control operations and treatments used by HCPH-MVCD.
Thermal Fogging/Larviciding. In 1965, the Harris County Mosquito Control District initiated thermal fog applications throughout the county during the first season, and shortly thereafter, began fogging underground storm drain systems with malathion, naled (Dibrom), and fenthion (Baytex) for control of Cx. quinquefasciatus(see figure 3).
A 1969 District monthly report (June) stated that 250 gallons of diesel oil/surfactant larvicide provided an estimated 24-hour kill of 102.6 billion mosquitoes in a single, mile-long ditch. In the 1967 District Annual Report, 152, 811 miles were driven over 191 nights during thermal fog applications of Baytex, Dibrom and malathion with 584,492 gallons of insecticide mix used to cover Harris County 12.6 times (Harris County historical unpublished data).
Although limited thermal fogging continued in Harris County through the years, it was discontinued in 2010 due to poor results obtained during 2008-09 (Fredregill et al. 2011).
ULV Applications. Introduction of the ground-based ultra-low volume (ULV) concept and several advantages that ULV had over conventional high-volume (HV) thermal fogging generators were made in 1968, (such as the extremely small amounts of insecticide required for applications and smaller overall equipment size required), and proved that ULV non-thermal (cold) aerosols were just as effective as HV thermal aerosols (Mount et al. 1968).
In the 1969 District Monthly (March) report, there was mention of an invitation to Alameda County, Calif., to evaluate a new ULV ground applicator with the U.S. Navy. In the June-August Monthly reports, Harris County officials approved the purchase of a single LECO ULV application unit for the District that was tested, producing excellent results with malathion. The ULV revolution in Harris County had officially begun.
A new LECO ULV cold aerosol nozzle that effectively applied malathion, naled, and fenthion against Ae. taeniorhynchus (Weid.) in Florida field cage tests was described, and some additional advantages of ground-based ULV were reported after field tests with malathion and Dursban against Cx. quinquefasciatus adults and larvae in Brazoria County, Texas, in that the effects of wind and temperature appeared to be less of a hindrance for ULV applications compared to thermal fogging. Additionally, the importance of ULV to mosquito control operations was accurately forecasted (Mount et al. 1970, McNeill, IV and Ludwig 1970). As one of the best public health insecticides ever offered, synergized resmethrin (Scourge) was successfully used in Harris County from 1984-2011 for 27 years.
Insecticide Resistance and Management. Initial reports of regional insecticide resistance and its management within mosquitoes were published during this period. Highly variable tolerances to organophosphates (chlorpyrifos, malathion and naled) were reported in Cx. quinquefasciatus from two southeastern Louisiana Parishes, Galveston and Brazoria Counties in Texas.
Highly active esterase activity in eight different populations of Cx. quinquefasciatus from Harris County suggested a broad range of insecticide susceptibilities and noted that the frequency of at least one esterase decreased during a five-year period when malathion use was very low (Pietrantonio et al. 2000).
Insecticide resistance management has been active since ULV capability was added to the program in 1969. Seven permanent primary operational areas of interest and two to eight additional areas were selectively chosen for testing each season using a standardized field cage test procedure. This was unique in that a laboratory-susceptible strain of Cx. quinquefasciatus was tested alongside three wild populations to provide comparative efficacy of specific ULV adulticides applied against these populations three to four nights during the season (see figure 4).
The HCPH-MVCD uses evidence-based ULV applications primarily based on the type of arbovirus activity within an operational area. Applications to each area are rotated between chemical classes, namely organophosphates and pyrethroids, using a simple and highly effective method. An easily fabricated selective flow control system has been in fleet service since 2005 and permits rotation between two adulticides (malathion and permethrin) by simply turning a diverter valve (Self et al. 2010). The current 21-vehicle ULV fleet is also outfitted with Monitor 4 flow control and vehicle tracking systems that permit accurate recording of adulticide use and the actual location applications were made.
Site Inspections. In preparation for potential Zika virus activities, HCPH-MVCD Inspection Section began area-wide assessments of peridomestic Aedes habitats throughout Harris County and completed in 2016 a total of 2,556 Resident and Service Requests from Harris County and the City of Houston. Elimination of breeding areas and limited spot treatments with methoprene, Bacillus thuringiensisisraelensis de Barjac, and B. sphaericus Neide-based control products are routinely performed to reduce mosquito populations on site (see figure 5).
SURVEILLANCE ACTIVITIES. Millions of mosquitoes are collected each year; birds are surveyed as well.
Discovery of Aedes albopictus (Skuse). During a routine survey for Ae. aegypti, mosquito collections made on Aug. 2, 1985, ultimately provided national recognition of the Harris County Mosquito Control District in the discovery of breeding populations of the introduced invasive Ae. albopictus in several geographically separated tire piles. Shortly thereafter, research funding was requested to determine distribution, genetics, insecticide resistance status, vector competency and legal implications, in addition to bionomic and ethological studies of the newly established mosquito species (Sprenger and Wuithiranyagool 1986, Bartnett 1986).
Mosquito Collection and Virology Capabilities. The basic foundation of the SLE surveillance program, completed in 1990, was based upon research conducted by MVCD in 1979 and 1982 indicating that CDC light traps baited with carbon dioxide were very effective collecting Cx. quinquefasciatus in the extensive network of storm drain systems in the Houston metropolitan area, with more than 400,000 mosquitoes collected per year at 268 locations (Sprenger 1992). Currently, the entire county is monitored year-round, and quite heavily during the months of highest risk (May-October). The entire county (268 operational areas) is covered on a weekly basis using 134 storm drain (carbon dioxide baited CDC light traps) and 134 gravid traps, primarily for Culex collections to monitor SLE and WNV, set along 27 collection routes (with 6-12 traps per route).
In 2016, 134 BG-Sentinel traps for Aedes surveillance were added to increase capabilities of detecting dengue, chikungunya and Zika viruses. Mosquito identification and pooling of the collections are made three to four days per week, with in-house virology laboratory analysis and test results occurring three times per week. Over most years, nearly 1 million mosquitoes are collected during routine surveillance each year.
Avian Surveillance. Since 1965, active avian surveillance has been important in early detection of arboviruses circulating within the live bird populations throughout Harris County and the city of Houston. In 2002, dead bird collections began and provided additional ability to detect WNV activity. Both programs have detected considerable variation in WNV activity in bird populations with seroprevalence ranging from 2.9-17.7 percent in live bird blood samples and WNV positive dead birds ranging from 0.3-57.2 percent.
EDUCATION AND OUTREACH. Educating residents not only on mosquito-borne diseases such as chikungunya and Zika and how they are spread, but also on personal protective measures against mosquito bites and source reduction steps that should be taken to reduce/eliminate mosquito breeding sites, are key factors in prevention. Ongoing prevention messages focusing on these topics are routinely provided to Harris County residents in an effort to impact the knowledge, attitudes and beliefs of the community toward mosquitoes and the diseases they transmit. Over the last year we have seen an increase in community engagement opportunities both as requests from community leaders and through community partnerships in place. In 2016, we participated in 131 community events, in addition to providing information through a number of other sources such as social media and traditional media outlets. Additionally, we provided more than 94 presentations to local community partners and national public health and legislative partners (see figure 6).
Authors’ Acknowledgement: We want to thank all of the past and present employees for their hard work and dedication towards the development and continued progression of the HCPH-MVCD in its mission to improve surveillance and control of arboviruses and other regional vector-borne diseases.James A. Dennett is a medical entomologist at the Mosquito & Vector Control Division with the Harris County (Texas) Public Health Department. Mustapha Debboun is director of the same department.
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