Traumatic myiasis in dogs caused by Wohlfahrtia magnifica and its importance in the epidemiology of wohlfahrtiosis of livestock

Introduction

Traumatic myiasis (= wound myiasis) describes the infestation of living humans or vertebrate animals with fly larvae which feed and develop in the cutaneous tissues of their hosts, causing a more or less severe traumatizing injury (Hall & Farkas, 2000). Larvae of several species of fly can cause this parasitic infestation of domestic animals; however, the main agents of traumatic myiasis are a few species of blowfly (Calliphoridae) and flesh fly (Sarcophagidae). The association of these larvae with the host has two main forms, either facultative or obligate. Larvae of the facultative myiasis-causing species usually develop on carrion or in other decaying organic materials, but their gravid females can also cause larval infestation of living hosts, usually at sites of previous wounding or other predisposing conditions. A smaller number of fly species cause obligatory traumatic myiasis because their larvae require living animals, including humans, for development.

Traumatic myiasis can lead to serious animal welfare and health problems and economic losses in livestock worldwide, but it can also occur in other domestic species, such as dogs. Traumatic myiasis of dogs is usually reported to be caused by larvae of Lucilia sericata Meigen or Lucilia caesar L. or other blowflies (Wetzel & Fischer, 1971; Rauchbach & Hadani, 1972; Azeredo-Espin & Madeira, 1996; Anderson & Huitson, 2004). Necrotic tissues and/or bacterial skin infections of dogs can attract female flies, which are capable of laying hundreds of eggs, and the sites offer a favourable environment for developing maggots. Dogs confined outdoors are most susceptible to fly strike, especially those which have faecal or urine-stained coats, draining wounds or inflamed tissues (e.g. otitis externa, pyometra or infected paraproctal glands).

Sarcophagid flies can also cause facultative myiasis in dogs: Principato et al. (1994) reported a rare case of an Italian dog with traumatic myiasis caused by larvae of Sarcophaga haemorrhoidalis (Fallen). Obligate traumatic myiasis-causing fly species can also infest dogs, but there have been only a few reported cases. The New World screwworm fly, Cochliomyia hominivorax (Coquerel), which is responsible for severe economic losses in livestock in the New World, has infested many local dogs in Brazil (Cramer-Ribeiro et al., 2003). Larvae of the Old World screwworm fly, Chrysomya bezziana Villeneuve, occurring in Africa and Asia, was found in the wounds of dogs (Chemonges-Nielsen, 2003). The movement of these exotic myiasis-causing fly species, as well as the Tumbu fly (Cordylobia anthropophaga Blanchard), between continents in infested dogs carries a potential threat of introductions to Europe and other continents where they do not yet exist (Anon., 1987; Chermette, 1989; Fox et al., 1992; Hendrix et al., 1995; Dongus et al., 1996; Chemonges-Nielsen, 2003; Ferroglio et al., 2003). Wohlfahrt’s wound myiasis fly, Wohlfahrtia magnifica (Schiner), which is one of the most important obligate traumatic myiasis-causing species in the Palaearctic zone, is widely distributed from the Mediterranean basin, through central and eastern Europe to northern Asia. Infestations with larvae of W. magnifica (wohlfahrtiosis) have been detected in many domesticated animal species (e.g. sheep, horse, cattle, pig and goose) (Hall & Farkas, 2000; Farkas & Képes, 2001; Farkas et al., 2001). Although the occurrence of wohlfahrtiosis in dogs was mentioned almost a century ago (Portschinsky, 1916), few cases have been reported recently (Şaki, 2004; Ütük, 2006).

This paper addresses the particular problem of dogs as hosts of W. magnifica in Morocco and Hungary, with the objective of evaluating their importance in the epidemiology of wohlfahrtiosis of livestock.

Materials and methods

Results

Morocco

Six active cases of traumatic myiasis were observed in the dogs inspected in July 2002. The wounds of two other dogs, which were reported to have been previously infested, were found to be free of larvae but purulent, as noted elsewhere in wounds freed of larvae (Farkas et al., 1997). All the infested dogs were males of mixed breeding and their estimated ages were between 2 and 8 years. They were unchained and allowed to roam freely around the houses and surrounding area. Five dogs had only one wound, with a diameter in the range of 3–15 cm (1, 2). The anatomical locations of the wounds were the penis (one dog, Fig. 3), legs (two dogs) and ears (two dogs, Fig. 1). The sixth dog had a 12–15-cm diameter tumour on the ventral aspect of his neck containing many distinct foci, each completely filled by developing larvae (Fig. 2). Larvae in any focus tended to be at the same stage of development. In September 2002 three further cases of wohlfahrtiosis were recorded in dogs (one male, two of unrecorded sex), all of which had single wounds on the rear limbs (paw, one dog, Fig. 4; leg, two dogs). In both months cases were recorded in the Al-Hoceima province neighbourhoods of Taguidit (35°08′ N, 04°10′ W; four cases), Aghbal (35°10′ N, 04°04′ W; three cases) and Tafensa (35°12′ N, 04°01′ W; two cases).

The larval masses in each wound (range 4–133 larvae) were composed mainly of third instars (in seven of nine cases), but one also contained second instars and one contained only first and second instars. Third instars were always found packed tightly together in the manner of screwworm larvae (C. hominivorax and Ch. bezziana), with their anterior ends buried deeply in the tissues and only their posterior segments containing the posterior respiratory spiracles exposed (Fig. 2). All the recovered larvae and the adults reared in the laboratory were identified as W. magnifica. Wohlfahrtiosis caused severe welfare problems and tissue destruction in most cases (1-4). During our surveys, only four other active cases of wohlfahrtiosis were detected in Al Hoceima province, of which three were on sheep and one on a goat.

Hungary

Four of 12 dogs (33.3%) inspected on the two farms had traumatic myiasis. At farm 1, a 5-year-old male dog of Caucasian breed, kept outside, had developing fly larvae in the external ear canal of his left ear (Fig. 5). The owner reported that the dog vigorously shook its head and scratched at its ears. The hair was wet and malodorous around the infested ear canal. At farm 2, three of nine guard and shepherd dogs kept around the buildings and livestock had active wound myiasis. Two of them were female Kuvasz, a Hungarian breed, and the third was a male of mixed breeding. They were 1.5, 2.5 and 5 years old. Each dog had only one infested wound located, respectively, on the dorsal part of the nose (Fig. 6), on the hind leg or in the vulva region (Fig. 7). The animals were all noticeably preoccupied with their lesions, often trying to lick the wounded areas. The number of larvae found in a wound ranged from 11 to 26 and, as in Morocco, they exhibited screwworm-like behaviour. Moderate bleeding was observed at the wounds. All the second and third instar larvae found in the wounds, and the adults reared from them, were identified as W. magnifica. Many blowflies were observed in the environment around the infested dogs, but no larvae of these flies were noted on the dogs.

Discussion

There are few reports of dogs infested by obligate traumatic myiasis-causing fly species, which, in nature, mainly infest livestock. These species require particular environmental and climatic conditions as adults, and the females usually only infest animals outdoors (Ruiz Martínez et al., 1992). Therefore, stray dogs and dogs kept around livestock with obligate traumatic myiasis are probably more likely to become infested in rural than urban areas, especially if dog owners are negligent of their animals’ health. Larval infestation is not always obvious to owners and, as it is impossible to inspect and treat stray animals, it is probable that many cases of infestations of dogs with larvae of obligate myiasis-causing fly species go unreported. This hypothesis is likely to be true for cases infested with the larvae of W. magnifica, one of the most important obligate myiasis-causing fly species in the Palaearctic zone (Hall & Farkas, 2000).

There are some published reports of wohlfahrtiosis of dogs, but these do not discuss its pathogenesis or epidemiological importance (Portschinsky, 1916; Zumpt, 1965; Şaki, 2004; Ütük, 2006). To our knowledge, these are the first cases of wohlfahrtiosis in dogs reported in Morocco and Hungary. We found wohlfahrtiosis in dogs of a range of breeds and ages, but more case data are needed to conclude the effect of these factors on its incidence. All infested dogs lived close to livestock, where wohlfahrtiosis was endemic. Infested body sites included limbs (six cases), external genitalia (two), ears (three), nose (one) and neck (one). Why were these hosts and particular sites infested?

The specific cues that attract gravid W. magnifica females to hosts and stimulate larviposition are still largely unknown, but odours are important (Hall et al., 1995). Females can certainly be attracted to sites of wounding for larviposition, as has been observed on other host species (Farkas & Képes, 2001; Farkas et al., 2001). Therefore, it is likely that wohlfahrtiosis occurred mainly in male dogs as a consequence of inter-dog aggression, territorial behaviour and fights causing wounds. Over 80% of cases (nine of 11) for which host sex was recorded were in males, and all cases in Morocco were male. According to the owners of dogs in northern Morocco, each infestation appeared at the site of wounds, some of which had been caused by dog bites. Active infestations become highly attractive to gravid females (Hall et al., 1995) and, therefore, multiple infestations with larvae at all stages of development frequently occur (Ruiz Martinez et al., 1987; Farkas et al., 1997).

It has also been reported that wounds are not a prerequisite for infestation by W. magnifica, the females of which can be attracted to healthy hosts without obvious predisposing conditions (Hall et al., 1995). At these hosts they can infest seemingly undamaged sites, particularly natural body orifices. It has been suggested that unknown volatiles produced by microorganisms may be responsible for fly attraction and larviposition responses on healthy animals (Farkas et al., 1997; Tóth et al., 1998). Wohlfahrtiosis was recorded without any preliminary wounds in at least two infested dogs in Hungary. In one of these cases the untreated otitis externa may have been a predisposing factor. In the other case wohlfahrtiosis was found in the seemingly undamaged vulva of a female dog. It is hypothesized that unknown volatiles produced during changed physiological and/or pathological processes – related in one example to otitis externa and, in the other, to the breakdown of products of urine or vaginal discharges – may be responsible for the attraction of gravid females to the ear and vulva regions. The ears of dogs in Brazil were reported to be the site most infested with larvae of C. hominivorax, with otitis being the main predisposing condition leading to myiasis (Cramer-Ribeiro et al., 2003).

Wohlfahrtiosis in dogs has been reported from Russia (Portschinsky, 1916), Turkey (Şaki, 2004; Ütük, 2006) and Israel (D. Zivotofsky, unpublished data, 2004). Compared with the numbers of Wohlfahrtia infestations in livestock, mainly sheep, the actual numbers of dog infestations are low. However, the number of dogs is also much lower than the numbers of sheep or other livestock in the endemic areas. Of the active cases detected in Morocco, a high proportion (nine of 13 cases, 69.2%) of infestations were found in dogs, which is especially high when numbers of dogs and livestock are compared.

Many farm dogs in both countries surveyed go untreated, either because the owners do not realize they are infested or cannot afford to treat the dogs, or because they are negligent. Although the numbers of cases reported here was small, wohlfahrtiosis in dogs may be very important from an epidemiological perspective because farm dogs and strays can act as both reservoirs and carriers of this parasitic fly species. When left untreated, wohlfahrtiosis infestations can produce mature larvae within 5 days (Hall & Farkas, 2000), which leave the wound, develop to adults and then pose a threat to local livestock and humans. Infested stray dogs are never treated and are a particular problem when they exist in large numbers, such as in Morocco, where a conservative estimate of more than 200 000 strays has been reported (Anon., 2000). Reservoir infestations in untreated dogs have been recognized as a problem in other myiasis situations. For example, in a collection of primarily New World screwworm myiasis cases in the urban Kingston area of Jamaica, dogs were found to be the most common hosts (Rawlins & Chen Sang, 1984). This was confirmed by survey during the subsequent campaign to eradicate screwworm on Jamaica using the sterile insect technique; of screwworm cases reported during 1999–2002, 94.6% of those in the Kingston–St. Andrew parish and 10–70% of those in other parishes originated from dogs (M. Vreysen, unpublished report to the International Atomic Energy Agency, 2002). One of the important complicating factors in this campaign was reported to be the urban ‘hot spots’ of incidence in unmanaged and stray dogs (Robinson et al., 2000). It was concluded that the success of the programme required increased emphasis on the treatment of such hot spots (Robinson et al., 2000). Dogs also have the potential to be vectors in the spread of wohlfahrtiosis if this disease is not taken into account when dogs are moved across international boundaries for leisure, sport, breeding and other purposes. There have been a number of cases of similar myiasis-causing fly species moving between continents in infested dogs (Anon., 1987; Chermette et al., 1989; Fox et al., 1992; Roosje et al., 1992; Dongus et al., 1996). The severity of risk for the establishment of this obligate myiasis-causing fly species depends on both location and the season of introduction.

Based on our findings, we conclude that wohlfahrtiosis in livestock cannot be completely controlled without the frequent inspection and treatment of local dogs. Preventing the spread of this myiasis-causing species is of great importance in veterinary medicine. Therefore, we recommend that dog owners are educated concerning the risk factors in endemic regions in order to reduce the prevalence of wohlfahrtiosis in dogs and, thereby, in livestock. Both owners and veterinarians should pay regular attention to any wounds and to the natural orifices of dogs, especially during the fly seasons. The role of dogs in the epidemiology of wohlfahrtiosis merits further attention, especially in countries with large populations of stray dogs.

Conflicts of interest

All authors declare no conflicts of interests.