Filth Flies - Significance, Surveillance and Control in Contingency Operations

Preparation of this Technical Guide (TG) was facilitated by Dr. Herbert T. Bolton, CAPT USN (retired), who generously lent his expertise to its development. Dr. Stephen B. Berté, COL USA (retired), CAPT Mark Beavers, USN, and COL Gene Cannon, USA, also provided professional guidance. Maj Brian Spears, USAF, consulted on aspects of aerial pesticide application. Figure 1 was provided by the Centers for Disease Control and Prevention (CDC). Keys and figures in Appendix A were taken from the Medical Entomology Handbook published by the Naval Medical School (1967); the originals were from the CDC or the Notes on Medical Entomology, published by the Naval Medical School (1942). Figures in Appendix B were taken from the U.S. Navy Manual of Preventive Medicine and U.S. Army Field Manual 21-10-1, Unit Field Sanitation Team. Thomas Burroughs, USACHPPM, provided the resistance testing information in Appendix D.

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SECTION 1. INTRODUCTION

Filth flies have been, and will continue to be, a major preventive medicine issue during military exercises and operations conducted in warm weather. Filth flies have been implicated as disease vectors, especially in refugee and prisoner of war camps. They can also be a tremendous nuisance when they interfere with and degrade mission performance. Fly problems may develop around field messing facilities that have inadequate screening, which can result in unsanitary conditions that make it difficult to protect food from fly-borne contamination. Likewise, field latrines constructed without adequate fly exclusion are virtually unusable. In mass casualty situations, such as battlefields and natural disasters, flies will breed in corpses and wounds if they are not controlled or excluded. For these reasons, fly control is often a major responsibility of utmost importance for preventive medicine personnel.

This TG provides basic information about the biology of several fly species known collectively as filth flies. Their medical importance and nuisance impacts are presented within the context of military operations and exercises. In accordance with Department of Defense policy on pesticide use, this TG also provides guidance on preventing fly problems, and implementing control strategies using pesticides and traps.

SECTION 2.

SIGNIFICANCE OF FILTH FLIES TO MILITARY OPERATIONS

2-1. Historical Examples of the Medical Impact of Filth Flies

Filth flies historically have had and continue to have an impact on combat, peacetime contingency operations, disaster relief operations, and refugee health support operations.

Filth flies may interfere with military operations through transmission of disease-causing organisms, contamination of food, myiasis (larval infestation of human and animal tissue), and annoyance or distraction from the job at hand. An increasingly persuasive body of evidence, described in detail below, suggests that flies play a major role in the spread of enteric disease agents. These pathogens have impacted military operations throughout history, underscoring the need for fly control.

Reports of concurrent increases in fly populations and incidence of diarrhea in North African and Middle Eastern military campaigns during World Wars I and II are numerous (Levine and Levine 1991). Colonel J.C.G. Ledingham (1920), Royal Army Medical Corps, Mesopotamian Expeditionary Force in WW I, found a strong correlation between fly density and the incidence of dysentery. In the World War II battle of El Alamein in North Africa, Axis forces suffered severe losses to combat troops due to dysentery presumably caused by flies. On Pacific Islands during World War II, flies developed in corpses on battlefields and excrement in latrines beyond modern comprehension. On Saipan in the summer of 1944, DDT applied from C-47 type aircraft at 7-day intervals was required to bring blow flies under control (Hall 1948). In 1958, a United States Marine Corps (USMC) force sent to Lebanon was incapacitated by dysentery within two weeks. USMC forces deployed to Lebanon in 1982 and 1983 relied heavily upon preventive medicine for protection. This commitment by preventive medicine personnel, which included extensive fly control efforts, resulted in a very low incidence of diarrhea (Daniell et al. 1985).

Flies were a monumental nuisance during the Vietnam War. Reports from one mess hall stated that the fly infestation was so heavy it was difficult to eat without ingesting one or two. It is impossible to estimate the disease transmission that may have been caused by flies in Vietnam, but it was undoubtedly significant. Several factors combined to make flies such a large problem. Many of the flies were breeding in villages near military camps, where they had easy access to animal feces, garbage, and poorly maintained dumps. Garbage collection and land filling, especially at smaller bases, were often inadequate. Human feces in burn barrels were sometimes not completely incinerated. Grease traps were overused or used incorrectly, and heavy rains often interfered with the correct functioning of grease traps and soakage pits. The hot and humid climate was conducive to rapid increases in fly populations. Also, corpses left in the field for several days were heavily infested with maggots, which necessitated application of pesticides inside body bags.

Similar problems were encountered in the Persian Gulf War of 1991 and in subsequent humanitarian relief operations. In 1992-93, relief forces in Somalia faced persistently inadequate sanitation in local villages and cities, resulting in huge fly problems in U.S. military camps. A combination of poor sanitation in Mogadishu and numerous livestock yielded large populations of Musca species. The situation was compounded by varying levels of sanitation (particularly in food service programs) between different contingents of the international relief force.

A Korean Airlines jet crashed on Guam in 1997, resulting in over 200 deaths. Victims were still being recovered 10 days after the crash. Preventive medicine personnel from the U.S. Naval Hospital, Guam, used Fly-Tek (Methomyl) in an attempt to protect corpses; however, many bodies had been almost entirely consumed by maggots before they could be recovered.

2-2. Current Literature on Disease Transmission by Filth Flies

Filth flies have been implicated in the direct and indirect mechanical transmission of a number of pathogens responsible for human diseases, especially those causing diarrheal illness. Mechanical transmission is the transfer of pathogens from one location to another, usually passively or unintentionally. Thus, the mechanical transmission of disease organisms is facilitated by the adult filth flies' habit of walking and feeding on materials that tend to be contaminated, then doing the same on food to be consumed by humans. Secretion of salivary fluids (sometimes incorrectly referred to as vomiting) and defecating while feeding also increase the potential for transmission of pathogens by flies.

The common factor in the ecology of several species of filth flies is their utilization of decomposing organic materials as food sources for the adults and developmental media for their maggots (larvae). Considering that these materials are often carrion, feces and food wastes (all with associated pathogens), the potential for flies becoming contaminated can be quite high. Filth flies have numerous hair-like structures on their legs and bodies that dramatically increase their surface area and aid in harboring pathogens. Their deeply channeled mouthparts and hairy feet, each with sticky pads, can easily be contaminated when in contact with contaminated substrates. Filth flies are potential mechanical vectors of disease-causing organisms because pathogens can be transferred from their contaminated bodies to our food, eyes, noses, mouths, and open wounds.

Filth flies are attracted to a variety of rotting organic materials and feces, but they are also attracted to human foods. In addition to the great number of pathogens filth flies may carry on their body surfaces, they may transmit pathogens to our food in their saliva and feces. Most filth flies have sponging mouthparts and are capable of consuming foods only in a liquid state. Solid foods are liquified by regurgitating the crop contents (along with any pathogens) onto the food material, allowing the vomit to liquefy the solid food. Flies then suck the liquefied food (along with any pathogens) into their digestive tracts. Flies further contaminate food by defecating on it while they feed. Fecal spots are usually darker than vomit spots. House flies can produce from 16 to 31 spots in 24 hours (most of them vomit spots) after just one feeding of milk. From this it is easy to speculate about how many spots could be produced in a food service facility by 10, 50, or 100 flies having constant access to various food sources. Kobayashi et al. (1999) showed that Escherichia coli O157:H7, an extremely virulent serotype of this common bacterium, actively proliferates in the minute spaces of house fly mouthparts, and that this proliferation leads to persistence of the bacteria in fly feces. Based on DNA evidence, they implicated house flies as the source of E. coli in an outbreak in a daycare center in Kyushu in western Japan.

Text Box: Table 1. Significant Pathogens of Human Diseases
Known to Contaminate Filth Flies
amoebic dysentery hepatitis Shigella
anthrax intestinal worms Streptococcus
cholera leprosy trachoma
diphtheria polio tuberculosis
Escherichia coli rotavirus typhoid fever
Eyeworms Salmonella yaws

Over one hundred pathogens that cause human disease are known to contaminate filth flies; the most significant are listed in Table 1. The role that filth flies play in actually transmitting pathogens to humans and to what extent this transmission leads to disease depends on the pathogen and associated environmental factors. In some instances transmission by flies may be significant, while in other instances it is nonexistent. Just because a pathogen is recovered from a fly does not mean that successful transmission is possible. There is strong evidence that flies play an important part in human illness caused by certain enteric bacterial infections (Graczyk et al. 2001).

a. Shigella and Other Enteric Bacterial Infections

Shigellosis is a diarrheal disease caused by Shigella spp. bacteria that include over 40 serotypes. Fever, vomiting and cramps, nausea, and sometimes toxemia are recognized symptoms. The illness is usually self-limited and runs its course in 4-7 days. Outbreaks commonly occur in situations where sanitation has been compromised, as in poorly maintained prisons, hospitals, day care centers, and refugee camps. Shigellosis is endemic in both temperate and tropical environments.

Transmission is mainly through direct or indirect fecal-oral routes, with the prime route thought to be between individuals who fail to wash their hands after defecation. Bacteria are transmitted from contaminated hands to the human or food that they contact. The introduction of only a few Shigella bacteria (as few as 10) can cause illness. While shigellosis transmission is felt to be primarily a disease of unwashed hands, Watt and Lindsay (text box) (1948) showed a strong correlation between filth fly populations and Shigella rates in humans. Cohen et al. (1991) found similar results, including reduced seroconversion in patients, in Israeli military camps where intensive fly control strategies were employed. Recently, Chavasse et al. (1999) described dramatic reductions in diarrheal rates associated with fly control in rural Pakistani villages.

There are strong associations between filth flies and several other diseases (yaws, eye disease, polio, tuberculosis, and various parasites). However, the importance of filth flies in causing human illness through transmission of these pathogens remains undetermined.

b. Myiasis

Myiasis is the invasion of tissues or organs of living humans or animals by fly larvae that may feed on the host’s living or dead tissue (gangrenous or necrotic) or on food ingested by the host. Host reactions may be asymptomatic, minor to violent, or even death. This review will concentrate on human myiasis, in which almost any exposed part of the body is at risk. Myiasis classification may be based on the parts of the body affected, such as enteric (gastrointestinal, gastric, or intestinal), rectal, urogenital, aural (ear), ocular, cutaneous, nasopharyngeal and traumatic (wound) myiasis. Myiasis classification may also be based on the separation of myiasis-producing Diptera into the following three groups.

(1) Accidental Myiasis

Accidental myiasis is most often the result of ingesting maggot-contaminated food. Flies in this group don't require or seek a living body to invade. In fact, most ingested fly larvae are unable to complete their life cycles in the human digestive system. However, enteric myiasis can cause malaise, nausea, vomiting, pain in the abdomen, and bloody diarrhea. Living and dead larvae may pass in the stool. Over 50 species of fly larvae are known to cause enteric myiasis. The most common are the house fly (Musca domestica), the lesser house fly (Fannia canicularis), the latrine fly (Fannia scalaris), and the false stable fly (Muscina stabulans). One of the most problematic fly species associated with enteric myiasis is the cheese skipper (Piophila casei). Cheese skipper females lay eggs on cured meats, old cheese, smoked fish and other materials. The larvae often penetrate the surface fairly deeply, particularly in meat, and go unseen. When humans unintentionally consume cheese skipper larvae, the maggots pass through the digestive system alive, resulting in serious intestinal lesions. Other fly larvae that can survive the human digestive system include the black soldier fly (Hermetia illucens) and the drone fly (Eristalis tenax). Both species are documented to cause severe gastrointestinal disturbances.

Another form of accidental myiasis is rectal, in which flies that feed and develop in excrement deposit their immature stages in fecal material around the anus of humans living in unsanitary conditions, especially infants and sick adults who are unable to care for themselves. The larvae of excrement feeders, such as the drone fly, lesser house fly, latrine fly, false stable fly, and certain flesh flies (Sarcophagidae), will move into the rectum or terminal part of the intestine to complete their development.

(2) Facultative Myiasis

Facultative myiasis occurs when fly species that normally develop in feces or dead animals lay their eggs or deposit their larvae in the tissues of living humans or animals. Maggots of these flies can develop in a living host feeding on dead tissues, but they sometimes invade living tissues as well. Urogenital and traumatic facultative myiasis occur most frequently. Vaginal myiasis is a concern of increased importance because of the larger numbers of women serving in deployed units.

Urogenital myiasis occurs in warm weather when people sleep uncovered. Since the fly species involved are not nocturnally active, eggs are probably laid on affected areas during low light periods of the evening or early morning. Egg laying may be stimulated by discharges from diseased genitals. The result is obstruction, pain, pus, mucus, bleeding, and a frequent desire to urinate. Larvae are expelled with urine. Flies most commonly associated with urogenital myiasis are the house fly, lesser house fly, latrine fly, and false stable fly.

Flies associated with facultative traumatic myiasis are usually carrion breeders. The blow flies (Calliphoridae) are most commonly involved, but flesh flies (Sarcophagidae) and house flies are also known to infest wounds. These flies are normally attracted to odors produced by rotting meat or carrion, and are likewise drawn to foul-smelling, neglected wounds. This can be a potentially serious problem, especially with patients that are to some degree helpless. Infestations can be quite painful. The maggots feed primarily on necrotic tissue, but they may also invade living tissue. Blow flies known to cause facultative traumatic myiasis include the black blow fly (Phormia regina), a green bottle fly (Phaenicia sericata), the secondary screwworm (Cochliomyia macellaria) and several species of Chrysomya.

(3) Obligatory Myiasis

Flies involved in obligatory myiasis are incapable of reproducing without a living host for larvae to feed upon. These flies include blow flies (Calliphoridae), flesh flies (Sarcophagidae), and bot flies (Oestridae, Hypodermatidae and Gasterophilidae).

The primary screwworm (Cochliomyia hominivorax) is a true obligate parasite. Adult females lay eggs only in living tissues of warm-blooded animals and humans; not on cold-blooded animals like reptiles and amphibians, nor in carrion or decaying meat or vegetables. Females are strongly attracted to and lay eggs in open wounds, sores, and the bite sites of ticks and blood-feeding flies. Individual females may lay up to 2,800 eggs in batches of 10 to 400. Adults are a deep metallic greenish-blue, with three thoracic stripes and cheeks covered with yellow, orange or reddish hairs. Without proper keys, it is often difficult to separate larvae and adults of this species from the secondary screwworm (Cochliomyia macellaria) (James 1947).

The primary screwworm is notorious for producing serious morbidity and mortality in livestock. Modern control measures, namely the USDA sterile male release program, have eradicated this fly from the United States to the southern border of Panama. Sporadic accidental re-infestations occur, often through importation of infested livestock. However, C. hominivorax still occurs from Colombia and Brazil to northern Argentina and Chile. Human cases are often associated with livestock infestations.

The bot and warble flies (Oestridae) are obligate parasites of animals that often infest livestock and pets. However, they can infest humans who work with or live near infested animals. Adult bot flies are distinguished from other flies by their hairy, bumblebee-like bodies. Larvae are large and often armored with spines that make removal from flesh difficult. In humans, larvae of the horse bot (Gasterophilus intestinalis) penetrate unbroken skin. Larvae cause a form of cutaneous creeping myiasis as they burrow freely in the skin. Burrowing is usually accompanied by severe itching. Since humans are not the horse bot's normal host, the larvae are unable to survive past the first stage. However, larvae of the ox warble or cattle grub (Hypoderma bovis) are able to complete their larval cycle in humans, often with serious consequences. Cattle grub larvae penetrate unbroken skin and may wander in the tissues of the arms and legs as they develop. As they reach the end of their cycle, larvae move upward, often causing cutaneous creeping myiasis as they search for a site to form a warble in the skin. Besides the severe pain that accompanies creeping myiasis, localized paralysis may occur if larvae invade the spinal cord. Larvae of the sheep bot (Oestris ovis) do not survive for long in humans, although they invade the eyes causing ophthalmomyiasis with accompanying pain and inflamation.

The human bot fly, Dermatobia hominis, is common in parts of Mexico and southward into South America. Adults resemble a blue bottle fly and parasitize a very wide range of animals, including humans. Females capture an insect, such as a mosquito, black fly, horse fly or stable fly, deposit eggs on its body, and release it. Larvae develop in 5 to 15 days, and leave the egg when the egg-laden insect visits a suitable host, such as a human. Entrance into the skin is made through a bite wound or hair follicle. The human bot fly larva produces a boil-like lesion (furuncular myiasis) with no prior wandering. It lives in the host for about six weeks, then exits the wound and drops to the soil to pupate. The larva causes an itching sensation when it enters the skin and for about three weeks thereafter. However, at the end of the third week, larvae can become extremely painful.

2-3. Filth Flies As Nuisance Pests

The great amounts of filth and carrion encountered by military personnel during war, peace keeping, and humanitarian operations are capable of producing huge numbers of filth flies. These flies not only disrupt military operations by affecting human health, but in large numbers they can distract personnel from their work and can significantly degrade morale.

The house fly female is capable of producing about 120 eggs 4 to 6 times in her lifetime. Larvae that hatch from these eggs can develop into adults in about 7 days. The potential for a house fly population explosion in warm conditions during contingencies (poor sanitation, large numbers of refugees or prisoners of war, and/or numerous exposed cadavers) is quite high. Stable flies, Stomoxys calcitrans (usually), are among the few filth flies that bite. Although they are not associated with disease transmission, they can be a formidable nuisance because both sexes must take blood meals to reproduce.

Numerous anecdotal accounts exist of huge filth fly populations in all wars, and in several operations and exercises involving the U.S. military. As recently as 1999, entomologists encountered large filth fly populations (calliphorids) at certain U.S. air bases in Kuwait that were a severe annoyance to day workers and were present en masse in dining facilities.

It is difficult to quantify the emotional effects of large numbers of flies on personnel in an already stressful environment. However, large populations of filth flies certainly distract personnel from their duties. Proper management of latrine wastes, garbage, and dining facilities will significantly reduce fly numbers. This, in turn, will result in more attentive and effective personnel, greatly improving the chances for successful operations in garrison, onboard ship, and in the field.