Two primary species of screwworm flies exist: Old World screwworm flies (Chrysomya bezziana) and NWS flies (Cochliomyia hominivorax).1 As the names suggest, the Old World screwworm flies are naturally found in the Eastern hemisphere and NWS flies are found in the Western hemisphere. Both species are known to cause myiasis (ie, infestation of tissue with fly larvae) in humans and other warm-blooded animals.2
Historically, NWS flies have caused considerable economic losses to cattle and other production animals. In 1934, 1.5 million animal cases of NWS infestation were reported in the Southeastern United States.3 An adult female fly lays eggs in an open wound on a suitable host. After 8 to 12 hours, larvae (screwworms) emerge, enter the wound, and begin to feed on living tissue. After 5 to 7 days, the mature larvae exit the wound and burrow into surrounding soil where they pupate for 7 to 60 days, depending on temperature and environmental conditions.4 After pupating, adult flies emerge, feed, and rest for approximately 3 to 5 days, at which point they are ready to mate and seek out a host for egg laying.1
The NWS flies capable of sustained reproduction were eradicated from the United States in 1966 (Figure 1).5,6 To prevent the spread of NWS flies north from infested countries in South America, the USDA and Panama under the Cooperative US COPEG now maintain a permanent barrier using the sterile insect technique in the Darien Gap region of Panama and Colombia.7 The flies have occasionally reentered the United States on both animals and humans; however, these incursions were identified and mitigated prior to the occurrence of any sustained reproduction of the flies.1
Map showing chronologically the areas from which NWS flies were eradicated in the United States and Central America from 1957 to 2001.5,6
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
Map showing chronologically the areas from which NWS flies were eradicated in the United States and Central America from 1957 to 2001.5,6
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
Map showing chronologically the areas from which NWS flies were eradicated in the United States and Central America from 1957 to 2001.5,6
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
The USDA APHIS defines a suspect case of NWS infestation as an animal or person with clinical signs consistent with blow fly or screwworm myiasis. A presumptive positive autochthonous (locally acquired) case is a suspect case in an animal that has no travel history outside the United States within the previous 10 days and was identified near a previous confirmed positive individual or the causative agent was identified as screwworm by a laboratory other than USDA's NVSL in Ames, Iowa, or identified as screwworm by a collector with screwworm experience. A confirmed positive autochthonous case is when the NVSL confirms the presence of screwworm in an individual with a presumptive positive autochthonous case by visual identification of the egg mass, larvae (first, second, or third instar), or the adult fly. The laboratory further details the differences in these autochthonous (local) cases versus imported cases.8
On September 30, 2016, the NVSL confirmed an autochthonous case of NWS infestation in a Key deer (Odocoileus virginianus clavium) from Big Pine Key, Fla. This case marked the first identification of a sustained and reproducing population of NWS flies in the United States since 1966. Multiple federal, state, and local government agencies collaborated to initiate a response to the outbreak. Although various reports and papers have been written about the incident, this report aims to describe the multifaceted nature of the response, while highlighting the collaborations and multiagency responses needed for successful eradication.
Regulatory Control Measures
Florida Commissioner of Agriculture and Consumer Services, Adam Putnam, issued a Declaration of Agricultural Emergency in Monroe County, Fla, on October 3, 2016, as a result of the NWS detection in the Florida Keys. Subsequently, a “Notice of General Animal Quarantine Zone” was announced by the Florida state veterinarian. This notice stopped the movement of all nonhuman animals into or out of the quarantine area without the permission of FDACS. Specifically, an interdiction station was set up in Key Largo, Fla, at mile marker 106 and served as a location to inspect animals leaving the Florida Keys.
Interdiction station and movement control
The interdiction station was staffed by FDACS Office of Agricultural Law Enforcement personnel and veterinary support staff, along with APHIS veterinary medical officers. The station was operational 24 hours a day until March 19, 2017. Requirements for hauling livestock and poultry (including cattle, horses, chickens, sheep, and goats) out of the quarantine zone included an official certificate of veterinary inspection and proof of treatment effective against screwworm infestation administered 72 hours before traveling or allowing the livestock to be inspected and treated by veterinarians at the interdiction station. Additionally, owners with nonlivestock domestic animals such as dogs, cats, exotic birds, and other companion animals wanting to enter or exit the quarantined area were encouraged to stop at the interdiction station to have their animals inspected and, if necessary, treated.
In total, 17,000 inspections were performed between October 2016 and March 2017. Specifically, 15,696 dogs, 825 cats, 301 chickens, 136 parrots, 16 parakeets, and 11 rabbits were inspected. Eighty horse inspections were also conducted; however, this number does not necessarily represent unique horses because some horses could have been counted more than once owing to the same group of horses moving back and forth between the Florida Keys and the mainland. Fewer than 10 each of other types of animals were inspected, including camels, crabs, ducks, ferrets, finches, goats, hedgehogs, lizards, llamas, opossums, peafowl, primates, raccoons, rodents, sea snails, sheep, snakes, sugar gliders, and pigs. No cases of NWS infestation were identified during inspections at the interdiction station.9
Procedures called for animals entering Monroe County illegally by water to be detained by Department of Homeland Security Customs and Border Protection officers to allow inspection, and if necessary, treatment. No cases of NWS infestation were identified from water interdictions.
Incident command
In early October 2016, the FDACS, Florida's Monroe County, and APHIS established a unified incident command post in Marathon, Fla. The unified incident command included personnel from Monroe County Emergency Management Agency and Board of Health, APHIS International Services, APHIS Wildlife Services, APHIS Plant Protection and Quarantine, APHIS Veterinary Services, USDA Agricultural Research Service, and the USFWS, which included staff from the National Key Deer Refuge. Overall, there were 539 rotations of individual staff members for the incident (deployments): 184 APHIS deployments; 104 other federal government deployments (USFWS and Agricultural Research Service); 224 state and county deployments, including 8 deployments from Monroe County, Fla; and 27 COPEG deployments from Panama. Additionally, approximately 30 APHIS personnel supported the response virtually via telephone and computer over the course of the outbreak. At the height of the response, a total of 158 personnel were deployed. The last response personnel demobilized on April 29, 2017, immediately after the final sterile fly release in the Florida Keys.9
Descriptive Epidemiology
Deer and other wildlife
The first suspect observation of an infested Key deer occurred on July 4, 2016, in Big Pine Key, Fla. That deer was examined by a wildlife biologist from the National Key Deer Refuge, who noted the presence of maggots in a limb wound.a By September 2016, the deer mortality rate had reached a level that was considerably higher than expected and additional cases of infestation in Key deer were being reported. As a result, staff from the National Key Deer Refuge in Big Pine Key contacted the FDACS, who submitted larvae from an infested deer to the NVSL for investigation as a foreign animal disease. The NVSL confirmed that the larvae were NWS on September 30, 2016.
Key deer are a federally listed endangered species, and all mortality events are recorded and geolocated by the staff of the National Key Deer Refuge.10,11 In 2016, the number of deaths of Key deer in the refuge ranged from 7/mo to 30/mo through to the end of September (Figure 2). An observable increase in the deer mortality rate above the expected rate began in late September 2016 and peaked in October 2016. The last case in a Key deer was identified on January 10, 2017.
Monthly number of deer in the National Key Deer Refuge, Big Pine Key, Fla, that died from 2006 through 2015 (median values; gray bars) and during 2016 (black bars).
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
Monthly number of deer in the National Key Deer Refuge, Big Pine Key, Fla, that died from 2006 through 2015 (median values; gray bars) and during 2016 (black bars).
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
Monthly number of deer in the National Key Deer Refuge, Big Pine Key, Fla, that died from 2006 through 2015 (median values; gray bars) and during 2016 (black bars).
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
In a population of 875 Key deer, a total of 10 confirmed NWS-positive autochthonous cases and 125 presumptive NWS-positive autochthonous cases associated with deer death were noted. The loss of these 135 deer represented a total population loss of 15%.10,11 One raccoon was confirmed positive for NWS infestation, which represented the only wildlife species other than Key deer identified as affected.
Domestic animals
Once the NWS infestation in the Florida Keys was confirmed, efforts were made to increase awareness of the parasite among veterinarians throughout the Florida Keys. Active case finding occurred with all suspected infestations among domestic animals being required to be reported to FDACS. The first suspect case in a domestic animal was noted in a dog on July 22, 2016; however, this case was never confirmed as NWS infestation. The first confirmed domestic animal case occurred on September 19, 2016, when a larva was collected by a veterinarian. Although the larva had been collected on that date, the larval sample had not been reported to the FDACS. The FDACS submitted this larval sample after the outbreak response had been initiated, and the NVSL confirmed the larva as NWS on October 7, 2016. No production livestock were ever identified or reported as being infested during this outbreak. Animal infestations were confirmed on 6 islands in the Florida Keys, and NWS flies were detected on 7 additional islands.9 By the end of the outbreak, 3 dogs, 2 cats, and 1 pet pig were confirmed to be positive for NWS infestation, whereas 2 dogs and 1 pet pig were deemed presumptive positive for NWS infestation. No human cases of NWS infestation were reported during or prior to the course of the outbreak.b
A single case of NWS infestation was identified on the Florida mainland. In this situation, 1 dog was identified as having suspect NWS infestation in Homestead, Fla, on December 19, 2016, and this case was subsequently confirmed by the NVSL on January 6, 2017. Calculations suggested that an egg mass was deposited in a wound on the dog on or around December 13. In response, investigation and case-finding efforts began in and around the home of the infested animal. Response personnel completed door-to-door canvassing in a 3- to 10-mile radius around the index premises. This effort included 1,051 residences, 102 veterinary clinics, and 149 farms or ranches, and a total of 1,437 initial contact reports were generated. No additional animals were identified as infested in Homestead, Fla.
Screwworm flies
Because of the geography of the Florida Keys and the presence of NWS infestations on multiple islands, the response to the outbreak entailed unique logistic challenges. Sterile flies were released by means of release chambers that needed to be placed on remote, hard-to-reach islands, requiring travel over water. Thirteen keys were known to be infested with wild NWS flies: Big Pine Key, Big Torch Key, Cudjoe Key, Howe Key, Little Knock-em-Down Key, Little Pine Key, Little Torch Key, Middle Torch Key, Munson Island, No Name Key, Ramrod Key, Sugar-loaf Key, and Summerland Key. Active trapping of flies took place from the beginning of the response on October 9, 2016, until March 15, 2017. The last wild NWS flies were found in the Florida Keys on November 7, 2016, and on the mainland on January 11, 2017.12
Animal Treatments
By October 21, 2016, Key deer were being treated with an avermectin where possible.11 Many deer in the Florida Keys are accustomed to taking food from residents and visitors, allowing responders to administer the medication by hand. The National Key Deer Refuge organized groups of volunteers to feed medicated food to deer at dusk, when the deer were more active. Topical treatments were also administered by use of feed stations with applicators.11 To preserve genetic material from the endangered Key deer as an extinction prevention contingency, 22 testes and 2 ovaries were collected from animals that were too severely affected to be treated and deposited at the Southeast Zoo Alliance for Reproduction and Conservation in White Oak, Fla.
Sterile Insect Technique
Control and eradication of NWS flies was accomplished by use of the sterile insect technique, which was implemented in the Florida Keys on October 11, 2016.13–15 At the start of the outbreak, the Panama COPEG facility immediately increased its production of sterile screwworm pupae.16 Shipments of sterile pupae and release chambers arrived in the Florida Keys on October 10, 2016, along with personnel from Panama and experts to assist with ground release of the flies. In total, 35 release sites were used in the response effort, selected by subject matter experts and aerial surveillance. Thirty-one release sites were in the Florida Keys and 4 on the mainland around Homestead. It is estimated that over 188 million sterile flies were released in Florida during the response. Sterile fly releases were concluded on March 21, 2017, on the mainland, whereas activities continued until April 25, 2017, in the infested zone of the Florida Keys.
Fly site assessments to determine the extent of the NWS infestation in the form of active trapping (involving rotten liver as bait) by technical experts began on October 5, 2016.13 Approximately 1 week after the first detection, strategically planned and mapped site assessments were being conducted by means of active trapping.14,17 Fly site assessments were conducted on 45 separate islands in the Florida Keys, on the mainland around Homestead, and in Everglades National Park to observe, capture, and identify flies. These assessments were also used to determine the effectiveness of the sterile insect technique and distribution of sterile flies. In total, more than 730 fly site assessments were conducted.12
Outreach
Public outreach efforts were possibly the most important factor in the eradication of NWS flies from the Florida Keys. Local participation and support were essential for agencies to conduct their NWS surveillance and eradication activities.
To better inform the public, the FDACS issued a public announcement and created a hotline number for concerned citizens. Incident management team representatives met with area veterinarians to provide information regarding the response and to distribute larvae collection kits. Federal personnel working on public lands on the mainland, including the Big Cypress National Preserve, Everglades National Park, and Biscayne National Park, were briefed on the procedure for submission of larvae from animals with suspected cases. Monroe County outreach targeted humane societies, pet groomers, flea markets, service animal owners, dog parks, hiking trails, and petting zoos. Information sheets were distributed at livestock markets and animal sales statewide. Interested parties were kept informed by radio and newspaper interviews, a nationwide email to USDA-accredited veterinarians, press conferences, public meetings, and veterinary meetings. Free pet screenings for NWS infestation were offered to residents of locally affected areas.
Public information officers reached out to the US Naval Air Station, Key West and the US Coast Guard to coordinate information and provided incident information to walk-in visitors at the incident command post. Moreover, Marathon Airport management and US Customs and Border Protection officials were provided with a procedure for requesting the inspection of pets on incoming small-craft international flights and maritime landings. Outreach resources developed during the incident included handouts (in English and Spanish), posters, emails, fax blasts, and websites. Additionally, an informational door hanger was developed and was distributed door-to-door by local volunteers.
Lessons Learned
Many lessons were learned in this response to an outbreak of NWS infestation. The first was arguably the role of citizen science in the recognition and treatment of a problem. In this outbreak, the public was greatly invested in the maintenance of a healthy Key deer population. Through a series of open meetings, the public was educated on the disease and able to actively engage in reporting new cases and hand-feeding deer with medicated food items. The public was urged to report cases involving Key deer and wildlife to the USFWS Key Deer hotline and report cases involving livestock and pets to the FDACS. Nongovernment agencies such as the Boy Scouts of America helped to facilitate access to hard-to-reach islands and maintained treatment stations on them. The Florida Keys Mosquito Control District was instrumental in placing sterile pupae and maintaining release boxes on keys only accessible by boat. In addition, people voluntarily pulled over at the interdiction station to have their animals inspected. Without the help of the public, many gaps in this response would have remained. It is also important to acknowledge the role of private-practice veterinarians in the treatment of affected pets. Further, this outbreak serves as a reminder that all veterinarians need to remain diligent in reporting cases of suspected foreign animal disease. Considerable delays occurred in identifying myiasis cases as caused by NWS in this outbreak, leading to delays in the overall response.
Federal, state, and local government agencies have worked since this outbreak to better educate staff, veterinarians, biologists, partner agencies, and public interest groups on what transpired. Presentations on screwworm biology and fly surveillance were made by federal and state partners to local, state, and national veterinary groups, veterinary schools, the National Assembly of State Animal Health Officials, the Entomological Society of America, livestock groups, the FBI, and other law enforcement agencies. Furthermore, a news update on the outbreak was published in the JAVMA in 2017.18
The present report serves to document and share the experiences and efforts undertaken to eradicate NWS flies from Florida. The USDA APHIS was able to use information learned from the outbreak to update the APHIS NWS Disease Strategy document, create a story map of the incident available online, and create educational brochures in English and Spanish. Additional supporting reference documents and history can be found on the APHIS Screwworm web page.19
Although attempts to eradicate NWS flies from the Florida Keys were successful, it is important to remember that the United States remains at risk for the reintroduction of these parasites. International movements of people and other animals continue to occur by water, air, and land, and vigilance is necessary to prevent the reintroduction of NWS flies to the United States. The processes and check points currently in place at international ports of entry must be adhered to, and thorough inspections of animals at the ports are important to identify NWS and many other exotic arthropods and pathogens. Veterinarians also have an important role to play in early detection and surveillance for cases following an introduction, particularly in cases in nonlivestock domestic animals.
Conclusion
On March 23, 2017, the USDA APHIS officially announced the eradication of NWS flies from Florida (Figure 3). By that time, operations were complete on the mainland and dramatically scaled down in the Florida Keys, and the interdiction station had closed. The last sterile fly release occurred in the Homestead area on March 21, 2017, and in the Florida Keys on April 25, 2017. This was approximately 7 months after the NVSL confirmed the NWS infestation in Key deer.
Timeline showing key events in the eradication of NWS flies from Florida (FL) in response to an outbreak of NWS infestation in Big Pine Key from 2016 to 2017.9
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
Timeline showing key events in the eradication of NWS flies from Florida (FL) in response to an outbreak of NWS infestation in Big Pine Key from 2016 to 2017.9
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
Timeline showing key events in the eradication of NWS flies from Florida (FL) in response to an outbreak of NWS infestation in Big Pine Key from 2016 to 2017.9
Citation: Journal of the American Veterinary Medical Association 255, 8; 10.2460/javma.255.8.908
The successful eradication of NWS flies from the Florida Keys is a testament to the hard work and commitment of the agencies who were willing to set up sterile fly release sites at remote locations, monitor the distribution of sterile flies and wild flies at surveillance sites, monitor and treat wildlife, conduct outreach within communities, and work as multiagency teams to collect, organize, and disseminate information. This eradication effort saved the endangered Key deer, stemmed untold losses to US agriculture, and kept South Florida residents, visitors, and their pets safe from NWS infestation.
Acknowledgments
The authors thank the following agencies for their invaluable help during this response: Panama-US COPEG, FDACS (Florida Forest Service, Office of Agricultural Law Enforcement, Division of Marketing, Division of Plant Industry, Division of Agricultural Environmental Services, Division of Food Safety, and Division of Animal Industry), Monroe County (Office of County Emergency Management, Offices of the County Mayor and Commissioners, County Mosquito Control, County Sheriff's Office, and Office of Airports Administration), Miami-Dade County, South Florida Water Management District, Florida State local responders and cooperators, Florida Keys Mosquito Control District, USDA Agricultural Service, USDA APHIS (Veterinary Services, Wildlife Services, International Services, Plant Protection and Quarantine, Legislative and Public Affairs), US National Park Service (Everglades National Park), USFWS (Key Deer National Wildlife Refuge), Miami-Dade County (Office of the County Mayor, Office of County Emergency Management, County Animal Control, County Sheriff's Office), Florida Fish and Wildlife Conservation Commission, Florida Cattlemen's Association, Florida Farm Bureau, Florida Veterinary Medical Association, University of Florida Institute of Food and Agricultural Sciences Extension, and the Boy Scouts of America (Sea Base).
ABBREVIATIONS
| COPEG | Commission for Eradication and Prevention of Screwworm |
| FDACS | Florida Department of Agriculture and Consumer Services |
| NVSL | National Veterinary Services Laboratory |
| NWS | New World screwworm |
| USFWS | US Fish and Wildlife Service |
Footnotes
Gibbs S, USFWS, Lower Suwannee National Wildlife Refuge, Chiefland, Fla: Personal communication, 2018.
Monroe County Health Department: Personal communication, 2016.
References
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2. World Organization for Animal Health. Screwworm (Old World and New World). Available at: www.oie.int/fileadmin/Home/eng/Animal_Health_in_the_World/docs/pdf/Disease_cards/SCREWWORM.pdf. Accessed Feb 14, 2019.
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15. Perkins JH. Edward Fred Knipling's sterile-male technique for control of the screwworm fly. Environ Rev 1977;2:19–37.
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