Introduction

Myiasis is defined as parasitic infestation of the body organs of vertebrate animals and humans by maggots of a variety of fly species that feed upon living or dead tissues (Zumpt, 1965)

Derraik et al (2010) classified the myiasis as, anatomical which includes open wounds, furuncular, intestinal or cavity myiasis or ecological which includes obligatory ,  facultative and accidental (Pseudo) myiasis.

Obligatory or specific  myiasis is caused by parasitic flies which require living tissues for their larval  development . Facultative or semi-specific myiasis is caused by opportunistic flies which live freely and lay eggs on the decaying organic matter and invade the living tissues especially pre-existing wounds. Accidental or pseudo-myiasis occurs when the food contaminated with fly eggs or larvae is ingested by host animals which subsequently develop pathological reactions (Hall, 1991).

Myiasis is distributed worldwide especially in poor socioeconomic regions of tropical and subtropical countries (Francesconi, and Lupi,2012). From Saudi Arabia many workers reported different forms of  myiasis in vertebrate animals and humans (Omar & Abdullah,1992; Badawi 1994; Fatani & Hilali 1994; Hall & Wall 1995; Khayat 2002; Al Ahmad et al 2006; Wakid 2008; Bosly 2013 and  Zaglool et al 2013,) (Table-2), however,  there is a paucity of literature on the identification and the habitats of  myiasis causing flies found in Jeddah which is a large commercial  city and harbour, and a metropolis with large number of animal sheds, through which  millions of livestock enter the kingdom annually. Therefore, the objective of this study was to identify the myiasis causing  flies in Jeddah and characterize their habitats. The results will provide important information that will enable the veterinary and public health authorities to identify the flies  rapidly and accurately and  to take appropriate actions for myiasis  prevention and control.

Material and Methods

Flies were collected from slaughter houses (abattoirs), animal farms , fish and vegetable markets of Jeddah city (Fig.1). Jeddah is a metropolis and a commercial city and harbour located on the west coast of Red Sea. (Latitude 21.29 N and Longitude 39.7 E). The climate is usually moderate except during summer when the temperature is high which might  reach 45⁰C,  and winter is moderately temperate. The average  high is approximately 35⁰C and low average is about 23⁰C. The average relative humidity is approximately between 50% to 60 %.

myiasis causing adult flies were collected by the means of Malaise traps, bait traps, yellow traps and sweeping nets from previously marked locations.  Rotten beef and liver was used in the traps to attract flies. To keep them moist a cotton cloth was used to cover them. The marked locations included slaughter houses located in the districts of municipalities:  Abhur, Al Mattar, Um Elsalam, Al Balad and Al-Janoub,  while the animal farms  especially sheep, goats, camel & horse paddocks located in South Jeddah, East of Harmain Road, Al Nuzah, Um Elsalam, Al Jamia, Asfan and Dhahban districts. (Fig-1)

Figure 1: A map of Jeddah city showing different locations of Flies collection     Click here to View figure

Collected flies were immobilized after  they were kept in the deep freezer for 15 to 20 minutes. After preservation adult flies were morphologically characterized  and  classified with the help of available authentic keys. (Akbarzadeh et al 2015; Al ahmadi and Salem et al 1999, Al Ghamdi and Alikhan 2015; Alikhan et al 2016,; Dabbour and El Dawy 1981, Irish et al. 2014; Mc Alpine 1989;  Nazni et al 2011; Pont 1991; Setyaningrum and Al Dhafer, 2014; Szpila 2012; Verves 2005).

In the present study only salient morphological features of the flies are discussed. The detailed identification key was already published in previous paper (Alikhan et al 2016).

Results and Discussion

According to morphological identification of adult flies the following ten dipteran  fly species belonging to six families were recorded as myiasis causing on the basis of reported cases in Saudi Arabia (Table.2). The flies  collected during survey were Megaselia scalaris, Musca domestica, Fanniia canicularis, Sarcophaga haemorrhidalis (Bercaea cruentata); Parasarcophaga ruficarnis, Wohlfahrtia nuba , Chrysomya marginalis, chrysomya albicep, Chrysomya megacephala, and Oesteris ovis. The present prevalence of each fly species was recorded (Table.1).  The  highest prevalence was recorded for the common house fly Musca domestica  (67.6%). Most of the species were collected from slaughter houses (50%) and animal farms (39%). (Table.1).

Table 1: Showing number of Flies collected by different Traps and their percentage

Table 2: Showing total number of flies and their percentage collected from different locations

Following are the salient morphological diagnostic  characteristics and habitats of the species collected.

Family: Phoridae

Megasellia scalaris (Loew, 1866) (Coffin fly or scuttle fly)

Brownish small fly which is also named as scuttle fly due to its sudden and rapid movements. The adult fly may be easily recognised by “humpbacked” thorax and laterally compressed hind femur.  The fore margins of the wings are thickened, wing veins are parallel to each other and without cross veins. One segmented antenna with long aristae.

Figure 2: Myiasis in a sheep   Click here to View figure

The fly maggots are  found near rotten meat, vegetable remains, trash containers, abattoirs, over animal carcases and near poor sanitary conditions. (it causes human accidental myiasis in wounds, intestine, eyes, respiratory system and urino-genital system).

Table 3: Cases of human and animal myiasis recorded from Saudi Arabia IN HUMANS

Family: Muscidae  

Musca domestica (Linnaeus, 1758) (House fly)

Thorax with 4 black stripes on greyish background, abdomen with yellowish spots on the anterior lateral sides below the wings and a dark midline. Antennae are short and 3 segmented, anal cell in the wing is closed, 4^th vein angled with discal cell.

Figure 3: Myiasis in Human   Click here to View figure

It lives close to humans and contaminate the food, feed and breed in garbage and animal faeces. (It is an agent of accidental myiasis of intestine and urino-genital system).

Family: Fanniidae

Fanniia canicularis (Linnaeus, 1761) (Lesser house fly)

The thorax  is brown-grey  with less distinct three black brown stripes, abdomen yellow in colour, eyes are with white border in male, head silvery in colour, halters are yellowish, the 4^th vein  not angled but straight, anal vein short.

Figure 4: Percent variation in the population density of adult flies causing myiasis in Jeddah   Click here to View figure

High number of Fanniia found in poultry farms and animal sheds. Deposit eggs  on decaying  organic matter such as cow dung, human and poultry faeces.

(It causes accidental myiasis of intestine and urino-genital system)

Figure 5: Percentage of flies causing myiasis collected from different locations of Jeddah   Click here to View figure

Family: Sarcophagidae

Sarcophaga haemorrhoidalis (Fallen,1817) (red-tailed flesh fly)

Thorax with 3 dark longitudinal stripes, antennal arista is plumose at the base and bare at the tip; antenna and palpi are greyish black with white hair on gennae. Abdomen with grey black checker board. Sixth tergite of female is  red in colour, separated with a row of strong bristles at the edge.

Flesh flies usually attracted to rotten meat, fish, vegetables, colonize the corpses, animal and human faeces.

Larviparous (Lay larvae) (Produce myiasis on necrotic or dead flesh in both humans and animals.).

Parasarcophaga ruficarnis (Fabricius,1794) (flesh fly species) 

Can be identified by  white hairs on gennae below eyes, antenna and palpi orange in colour.  Breed both in faeces and dead bodies.

(breeds on flesh  causing myiasis or   carrion and faeces, also a vector for diseases).

Wohlfahrtia nuba (Wiedemann,1830) (spotted flesh fly)

Greyish with three black round spots at the end of each abdominal segment, antennal arista bare or with very short hairs, larviparous. Breed on the open wounds of the camel and causes severe myiasis.

(Causes severe myiasis in Camel it is a secondary invader of wounds.)

Family: Calliphoridae

Chrysomya albicep (Wiedemann,1819) (Blow fly species)

Body  metallic green with narrow dark lines on the rear edge of each abdominal segment; anterior thoracic spiracle white/pale yellow, antennal arista plumose, head with silvery hair.

(Female deposit egg on the decomposing tissues or  in the wounds of living in animals and in humans and causes a specific myiasis in wounds, sores and nasal cavities.)

Chryasomya megacephala (Fibricius,1794) (oriental latrine fly)

Large red eyes with metallic blue/green body, buccal area and gennae  with orange setae. Anterior thoracic spiracle black/brown. Lower calypter white at the base and the rest is dark.

(Causes myiasis in animals and humans resulting into economic  losses in cattle and fish industries all over the world.)

Chrysomya marginalis (Wiedemann,1830)

Anterior wing margins dark, anterior spiracle white in colour. Greater ampulla with thick hairs dorsally. Lower calypter with dense hairs.

Family: Oestridae

Oestrus ovis (Linnaeus, 1758) (Sheep nasal bot fly)

Short stout and  dark grey body with black spots at the abdomen. Head and legs are dull yellow.

Female fly deposit eggs in the nostrils of the camel or sheep. Usually found where sheep camel or goats are reared.

(Responsible for  myiasis of skin, mucous membranes of mouth, eyes or nasal cavities both in animals and humans.)

Most of the reports on myiasis in animals & humans from Saudi Arabia are about the case studies. ( Afifi et al, 2015; Al Otaibi et al. 2016; Al Badri, 2016; Al Ahmad et al, 2006; ). Many myiasis causing flies collected by different workers from other parts of the country such as, Cordylobia anthropophaga, Dermatobia hominis, Wohlfahrtia magnifica, Cephalopina titillator, Chrysomya bezziana etc., may be present in Jeddah region but could not be trapped during this study.  Some of the workers studied the identification of forensic important flies from Jeddah  (Al Ghamdi and Alikhan, 2015, Al shareef H. 2016) but there is no record of myiasis causing flies from this region.

Conclusion

Present study is important  because it provides a list of flies causing myiasis to animals and humans in this part of the kingdom and responsible for the economic losses and agony. The flies may be different taxonomically but they affect animals and humans in the same way and their ecology and habitats also similar.

The easy method of identification is needed for the veterinary & health workers to control the myiasis causing flies and  to reduce the economic loss and human sufferings.

Acknowledgement

The authors are indebted to the Al Amana Public Health Laboratory, Jeddah for providing the facilities to carry out this research work. We are also thankful to all our colleagues for their kind help and suggestions during this study.

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