• View in gallery

    Whole body of the third-stage larva of Lucilia sp. clearly showing the anterior cephalopharyngeal skeleton and the posterior spiracles.

  • View in gallery

    Anterior end of a second instar of Lucilia sericata showing the cephalopharyngeal skeleton (CS) and anterior spiracles with 7–8 lobes (L).

  • View in gallery

    Posterior spiracles (S) of larva that are typical of phorid flies in general and not Megaselia scalaris sp. in particular.

  • View in gallery

    Anterior segments of larva showing the typical cephalopharyngeal skeleton (CS) of the phorid fly Megaselia scalaris.

  • 1

    Hall M, Wall R, 1995. Myiasis of humans and domestic animals. Adv Parasitol 35 :257–334.

  • 2

    Hira PR, Hajj B, Al-Ali F, Hall MJ, 1993. Ophthalmomyiasis in Kuwait: first report of infections due to the larvae of Oestrus ovis before and after the Gulf War. J Trop Med Hyg 96 :241–244.

    • Search Google Scholar
    • Export Citation
  • 3

    Hira PR, Hall MJR, Hajj B, Al-Ali F, Farooq R, Muzairai IA, 1997. Human myiasis in Kuwait due to Oestrus ovis, Psychoda species and Megaselia species. Med Prin Pract 6 :129–136.

    • Search Google Scholar
    • Export Citation
  • 4

    Erzinçlioglu YZ, 1989. The early instars of Lucilia sericata and Lucilia cuprina (Diptera: Calliphridae); myiasis blowflies of Africa and Australia. J Nat Hist 23 :1133–1136.

    • Search Google Scholar
    • Export Citation
  • 5

    Houty W, 1989. Insect Fauna of Kuwait. Kuwaity City, Kuwait: Fahad Al-Marzouk Printing and Publishing Establishment.

  • 6

    Disney RHL, 1991. The aquatic Phoridae (Diptera). Entomol Scand 22 :171–191.

  • 7

    Hall MJR, 1995. Trapping the flies that cause myiasis: their responses to host-stimuli. Ann Trop Med Parasitol 89 :333–337.

  • 8

    Wall R, French N, Morgan KL, 1992. Effects of temperature on the development and abundance of the sheep blowfly Lucilia sericata (Diptera: Calliphoridae). Bull Entomol Res 82 :125–131.

    • Search Google Scholar
    • Export Citation
  • 9

    Greenberg B, 1984. Two cases of human myiasis caused by Phaenicia sericata (Diptera: Calliphoridae) in Chicago area hospitals. J Med Entomol 21 :615.

    • Search Google Scholar
    • Export Citation
  • 10

    Simmers L, 1988. Diversified Health Occupations. Second edition. Albany, NY: Delmar Publishers, 150–151.

  • 11

    Smith DR, Clevenger RR, 1986. Nosocomial nasal myiasis. Arch Pathol Lab Med 110 :439–440.

  • 12

    Amitay M, Efrat M, McGarry JW, Shinwell ES, 1998. Nosocomial myiasis in an extremely premature infant caused by the sheep blowfly Lucilia sericata.Pediatr Infect Dis J 17 :1056–1057.

    • Search Google Scholar
    • Export Citation
  • 13

    Daniel M, Srámová H, Zálabská E, 1994. Lucilia sericata (Diptera: Calliphoridae), causing hospital-acquired myiasis in a traumatic wound. J Hosp Infect 28 :149–152.

    • Search Google Scholar
    • Export Citation
  • 14

    Minár J, Herold J, Elisková J, 1995. Nozokomiálni myiáze ve stredni Evrope. Epidemiol Mikrobiol Immunol 44 :81–83.

  • 15

    Sherman RA, Hall MJR, Thomas S, 2000. Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu Rev Entomol 45 :55–81.

    • Search Google Scholar
    • Export Citation
  • 16

    Amoudi MA, Diab FM, Abou-Fannah SSM, 1989. The occurrence of Megaselia scalaris (Loew) (Diptera: Phoridae) in Saudi Arabia with some aspects on the life history and distribution in Riyadh Province. J King Saud Univ Sci 1–2 :43–51.

    • Search Google Scholar
    • Export Citation
  • 17

    Disney RHL, 1994. Scuttle Flies: The Phoridae. London: Chapman and Hall.

  • 18

    Austen EE, 1910. Some dipterous insects which cause myiasis in man. Trans R Soc Trop Med Hyg 3 :215–242.

  • 19

    Hardy DE, 1951. A case of apparent human myiasis. Proc Hawaiian Entomol Soc 14 :212–213.

  • 20

    Abram LJ, Froimson AI, 1987. Myiasis (maggot infection) as a complication of fracture management: case report and review of the literature. Orthopedics 10 :625–627.

    • Search Google Scholar
    • Export Citation

 

 

 

 

MYIASIS IN KUWAIT: NOSOCOMIAL INFECTIONS CAUSED BY LUCILIA SERICATA AND MEGASELIA SCALARIS

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  • 1 Department of Microbiology, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait; Department of Surgery, Infection Control Department, and Intensive Care Unit, Mubarak Hospital, Kuwait City, Kuwait; Microbiology Laboratories, Farwania Hospital, Kuwait City, Kuwait; Department of Zoology, Cambridge University, Cambridge, United Kingdom; Entomology Department, The Natural History Museum, London, United Kingdom

Myiasis, the invasion of live human tissue by larvae of Diptera, is reported in the nasopharynx and a leg wound in two patients who were hospitalized for more than 72 hours in Mubarak Al-Kabeer Teaching Hospital in Kuwait City, Kuwait. On the fourth and fifth days after a 10-year-old Kuwaiti boy was admitted to the hospital intensive care unit in a bloodied and comatose state following a traffic accident, ‘worms’ that came out of his nostrils were fixed, cleared, and identified as second and third instar of Lucilia sericata (Diptera: Calliphoridae). After 14 days, ‘worms’ were seen in the original dressing of a 35-year-old Iranian man admitted to the Orthopedic Unit of the hospital with multiple lacerations and fractures. The larvae, in various stages of development, were identified as those of Megaselia scalaris (Diptera: Phoridae). Since the presence of larvae in both patients was recorded after a stay of at least 3–4 days in the hospital, by definition, these infestations are considered nosocomial.

INTRODUCTION

Human myiasis is the invasion of the tissues of humans by the larvae of Diptera (true flies). It occurs worldwide, but more often in hot and humid climates. Species causing myiasis can be obligate, facultative, or accidental.1 We have previously reported ophthalmomyiasis of humans due to Oestrus ovis, the sheep nasal bot fly, an obligate parasite of sheep found in Kuwait and worldwide.2 We have also reported facultative and accidental myiasis caused by O. ovis, Psychoda sp., and Megaselia sp.3 We now report on two cases of facultative myiasis, one a case of nasopharyngeal myiasis and another of wound myiasis complicating a skeletal traction. Since both of these infestations manifested more than three days after the hospitalization of the patients, by definition, these may be considered nosocomial.

CASE 1

A 10-year-old Kuwaiti boy was admitted to the Intensive Care Unit (ICU) of Mubarak Al-Kabeer Teaching Hospital in Kuwait City, Kuwait following a traffic accident. He had a head wound on the right side and his face was bloody when admitted. His face was cleaned during subsequent treatment. Further examination showed that be had fractures of both femurs. He had been comatose since being admitted.

On the fourth and fifth days after admission, while still comatose, larvae were seen coming out of both of his nostrils. These were collected into saline and sent to the laboratory for identification. It was reported that larvae were also seen emerging from the right ear, but these were discarded. The nursing staff also reported that they had seen a green fly on the nose of the patient on the fifth day after admission.

CASE 2

A 35-year-old Iranian man was rushed to the Casualty Department of Mubarak Al-Kabeer Teaching Hospital after concrete from a building site at which he was working fell on him. On examination, he had lacerations on the right thigh and lower limb. He also had multiple fractures of the pelvis and the right tibia. After being cleaned, the leg was bandaged from the upper part of the femur to the mid-calf. A skeletal traction was placed on the upper part of the tibia. After approximately 14 days, the gauze bandage at the site of the traction was discolored and foul-smelling. At this time, it was surmised that there was an underlying infection of the skin. When the dressing was being changed, tiny white ‘worms’ were seen on the original dressing around the orthopedic scars. Some of these were placed in saline and sent to the laboratory for identification. No organisms were seen coming out of the wound, which was clean and without necrosis.

MATERIALS AND METHODS

All larvae that were placed in saline were transferred into 70% ethanol. They were cleared in lactophenol, dehydrated, and, where appropriate, mounted as previously described.2

Following the discovery of a fly and the probability that flies had entered the ICU from the vicinity of the hospital, the Insect and Rodent Control Division of the Ministry of Health trapped flies by hand nets between 8:00 AM and 1:00 PM on a single day in the immediate area and identified the species.

RESULTS

Case 1.

Of the five specimens examined in detail from case 1, three were second instar larvae, one was a second instar larvae molting to a third instar, and one was a third instar. On the basis of the morphology and size of the larvae, the cephalopharyngeal skeletons of the third instar with mouth hooks lacking the accessory sclerite, the anterior spiracles and bands of spines, and the posterior spiracles with the complete peritreme (Figure 1), the larvae were identified as Lucilia species (Diptera: Calliphoridae). A closer examination of the second instar showed that the spiracles had 7–8 lobes (Figure 2). This is characteristic of L. sericata rather than L. cuprina, which has 4–5 lobes.4 Lucilia sericata is more widely distributed in Kuwait than L. cuprina, which has been identified from just one location in the country.5 Lucilia sericata is a facultative ectoparasite and is commonly known as the green bottle blowfly or sheep strike blowfly.

Case 2.

The five fly larvae from the second patient were 5–7 mm in length, white, and fusiform. Identification of the larvae as those of a phorid fly, Megaselia scalaris (Diptera: Phoridae), was based on the general appearance of the posterior spiracles (Figure 3), the particular appearance of the cephalopharyngeal skeleton (Figure 4), and the dimensions of the various processes and the fine hairs and spiracles on the integument of the abdominal segments.6 Furthermore, our specimens were matched against voucher specimens of larvae from a series of which some were reared to adults.

Fly capture.

Fifty flies were caught around the vicinity of the hospital, especially the kitchen area. These were identified as Musca domestica (94%), Musca sorbens (2%), and Chrysomya albiceps (4%).

DISCUSSION

The three most damaging species of flies causing wound myiasis of humans globally are the two calliphorid screworm blowflies Cochliomyia hominivorax and Chrysomya bezziana and the sarcophagid fleshfly Wohlfahrtia magnifica. The larvae of all three species are obligate parasites and require a living host. Many other species of blowfly and, to a lesser extent, fleshfly can be facultative parasites of humans, including species of the genera Lucilia, Chrysomya, Calliphora, Phormia, and Sarcophaga.1

The identification of the larvae of Lucilia sp. posed difficulties here because none could be reared to adults for confirmation based on adult morphology. However, the available characteristics, especially the number of lobes of the anterior spiracles of the second instar larvae (Figure 2), together with knowledge of the distribution of Lucilia species in Kuwait, indicate that the larvae were L. sericata.

The eggs of Lucilia sp. are laid on the host. Adult flies are highly sensitive to chemical stimuli and able to locate suitable oviposition sites readily.7 Wounds with necrotic areas are ideal sites for egg deposition and larval development. The rate of development after deposition is temperature dependent. Above 30°C, the incubation of eggs of L. sericata took 10–12 hours and completion of the larval feeding stage an additional 2.5 days,8 giving a total of three days to the end of feeding. Greenberg9 indicated that the average minimum duration from egg laying to completion of the second instar stage for Phaenicia (= Lucilia) sericata was just over two days (50 hours) at 29°C. The normal range of human body temperature is 36.1–37.8°C,10 but nostril temperature might be approximately 30°C.9

In case 1, larvae of L. sericata were noted four days (96 hours) after admission to the hospital. Our belief that the myiasis was nosocomial is based on the development rates of the larvae, which were approximately at the second to third instar transition, therefore, no more than two or three days old. If the egg deposition had occurred at the accident site, the larvae would then have been at least mature, post-feeding third instars. The observation by the nurses of a green fly on the patient while he was in the ICU is further evidence of the potential for nosocomial infestation. Facilitatory conditions in this case included the patient’s inability to fend off flies, the initial presence of blood/mucus around the wounds, the hot/ humid climate, and the ground floor location of the ICU. Thus, the evidence indicated that the nasal infestation occurred during hospitalization and is, therefore, considered nosocomial. Nasal infestations were the most common in a short review of hospital-acquired myiasis in the United States they occurred in four of six cases, five of which were due to P. sericata.11 Nosocomial myiasis of the nasal cavities due to L. sericata has also been reported in the Middle East12 and Europe.13,14

In the second case, the wound was cleaned and bandaged at the time of admission and larvae were found long after 72 hours of hospitalization. These facts therefore characterize this infestation as nosocomial. It could be argued that this was a case of myiasis or merely an infestation of the dressing. The fact that there was no necrotic tissue does not exclude myiasis because maggot infestations can diminish the growth of pathogenic bacteria during the healing of a wound.15

The identification of M. scalaris is of clinical significance. An earlier report from Kuwait implicated Megaselia sp. in intestinal myiasis.3 At that time, not much significance was placed on this finding because the organism could have been in food products that originated abroad and were imported into Kuwait. Thus, Megaselia sp. was not regarded as indigenous per se. However, more than 60 Megaselia spp. are now known in the Arabian peninsula (Disney RHL, unpublished data), and the widely distributed M. scalaris has been reported in Kuwait (Al-Houty W, unpublished data), Saudi Arabia,16 and Yemen (Disney RHL, unpublished data). Megaselia scalaris has a global distribution and has been reported in cases of wound myiasis from a number of locations around the world.17 Austen18 reported 63 larvae of M. scalaris in a wound on a man’s foot in Belize, while Hardy19 reported larvae of the same species invading a one-year-old surgical site on the chest of a patient in Hawaii. Ours is the first such report from Kuwait.

These two reports of nosocomial myiasis are important for reasons other than the peculiarities of each case. Myiasis causes anxiety and confusion even among medical staff. Potential morbidity caused by myiasis includes intense pruritus and irritability. Transmission of infectious agents and local tissue damage should also be considered in the management of this disease.

Most reports of nosocomial myiasis have been of sporadic, facultative infestations, particularly in debilitated patients.11 Factors contributing to noscomial infections include hypoesthesia or disturbed consciousness, which prevents the patient’s sensation of fly contact, as was certainly the case in our first patient. Furthermore, paralysis or immobility may prevent a patient from fending off a fly even if detected, as was probably the case in both our patients.

Preventive measures against phorids are difficult because they are so small and can enter through most fly screenings and, as in this case, underneath bandages. However, for prevention of blowfly and fleshfly myiasis, maintaining clean dressings on wounds will stop infestation by species that would otherwise deposit eggs or larvae into open wounds. Particular attention should be given to the wound dressings and plaster casts of elderly or infirmed patients because these can actually conceal infestations to which these patients are unable to respond.20 The case of nasal myiasis we report was difficult to prevent because bandaging the patient’s nose was not an option. However, where a high risk of myiasis is identified, even such wounds can be protected by covering with mosquito netting, through which the patient can breathe. Both cases we report were a challenge to what might normally be perfectly adequate practice to prevent hospital-acquired infestations. As well as bandaging and regular inspection of wounds, to minimize development of and therefore damage caused by any eggs/larvae that are deposited, fly screens can be placed over windows to prevent fly entry and fly electrocutors can be installed on the walls in rooms and corridors to kill any flies that do enter.

This is the first report of nasopharyngeal and wound myiasis in Kuwait. There is a paucity of such information from this country, probably because specimens tend to be discarded without study due to a lack of expertise in identifying fly larvae and in the absence of a reference center. Since both infections were identified 72 hours after the hospital admission, these cases can be categorized as nosocomial. We hope that our report will stimulate others to present similar clinical findings and to contribute to the pool of knowledge on the subject in Kuwait and the Middle East from which there is a dearth of such data.

Figure 1.
Figure 1.

Whole body of the third-stage larva of Lucilia sp. clearly showing the anterior cephalopharyngeal skeleton and the posterior spiracles.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 70, 4; 10.4269/ajtmh.2004.70.386

Figure 2.
Figure 2.

Anterior end of a second instar of Lucilia sericata showing the cephalopharyngeal skeleton (CS) and anterior spiracles with 7–8 lobes (L).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 70, 4; 10.4269/ajtmh.2004.70.386

Figure 3.
Figure 3.

Posterior spiracles (S) of larva that are typical of phorid flies in general and not Megaselia scalaris sp. in particular.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 70, 4; 10.4269/ajtmh.2004.70.386

Figure 4.
Figure 4.

Anterior segments of larva showing the typical cephalopharyngeal skeleton (CS) of the phorid fly Megaselia scalaris.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 70, 4; 10.4269/ajtmh.2004.70.386

Authors’ addresses: Parsotam R. Hira and Jamshaid Iqbal, Department of Microbiology, Faculty of Medicine, Kuwait University, Kuwait City, Kuwait, E-mail: hira@hsc.kuniv.edu.kw. Reem M. Assad, Department of Surgery, Mubarak Hospital, Kuwait City, Kuwait. Ghufran Okasha, Infection Control Department, Mubarak Hospital, Kuwait City, Kuwait. Faiza M. Al-Ali, Microbiology Laboratories, Farwania Hospital, Kuwait City, Kuwait. Kamal E. H. Mutawali, Intensive Care Unit, Mubarak Hospital, Kuwait City, Kuwait. R. Henry L. Disney, Department of Zoology, Cambridge University, Downing Street, Cambridge CB2 3EJ, United Kingdom. Martin J. R. Hall, Entomology Department, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom.

Acknowledgments: We thank the physicians in the District General Hospitals for referring the patients to us.

Financial support: This study was supported by the Office of the Vice-President for Research, Kuwait University (grants MI 015, MI 06/01, and MI 054) and the Kuwait Foundation for Advancement of Sciences (KFAS 84-07-01).

REFERENCES

  • 1

    Hall M, Wall R, 1995. Myiasis of humans and domestic animals. Adv Parasitol 35 :257–334.

  • 2

    Hira PR, Hajj B, Al-Ali F, Hall MJ, 1993. Ophthalmomyiasis in Kuwait: first report of infections due to the larvae of Oestrus ovis before and after the Gulf War. J Trop Med Hyg 96 :241–244.

    • Search Google Scholar
    • Export Citation
  • 3

    Hira PR, Hall MJR, Hajj B, Al-Ali F, Farooq R, Muzairai IA, 1997. Human myiasis in Kuwait due to Oestrus ovis, Psychoda species and Megaselia species. Med Prin Pract 6 :129–136.

    • Search Google Scholar
    • Export Citation
  • 4

    Erzinçlioglu YZ, 1989. The early instars of Lucilia sericata and Lucilia cuprina (Diptera: Calliphridae); myiasis blowflies of Africa and Australia. J Nat Hist 23 :1133–1136.

    • Search Google Scholar
    • Export Citation
  • 5

    Houty W, 1989. Insect Fauna of Kuwait. Kuwaity City, Kuwait: Fahad Al-Marzouk Printing and Publishing Establishment.

  • 6

    Disney RHL, 1991. The aquatic Phoridae (Diptera). Entomol Scand 22 :171–191.

  • 7

    Hall MJR, 1995. Trapping the flies that cause myiasis: their responses to host-stimuli. Ann Trop Med Parasitol 89 :333–337.

  • 8

    Wall R, French N, Morgan KL, 1992. Effects of temperature on the development and abundance of the sheep blowfly Lucilia sericata (Diptera: Calliphoridae). Bull Entomol Res 82 :125–131.

    • Search Google Scholar
    • Export Citation
  • 9

    Greenberg B, 1984. Two cases of human myiasis caused by Phaenicia sericata (Diptera: Calliphoridae) in Chicago area hospitals. J Med Entomol 21 :615.

    • Search Google Scholar
    • Export Citation
  • 10

    Simmers L, 1988. Diversified Health Occupations. Second edition. Albany, NY: Delmar Publishers, 150–151.

  • 11

    Smith DR, Clevenger RR, 1986. Nosocomial nasal myiasis. Arch Pathol Lab Med 110 :439–440.

  • 12

    Amitay M, Efrat M, McGarry JW, Shinwell ES, 1998. Nosocomial myiasis in an extremely premature infant caused by the sheep blowfly Lucilia sericata.Pediatr Infect Dis J 17 :1056–1057.

    • Search Google Scholar
    • Export Citation
  • 13

    Daniel M, Srámová H, Zálabská E, 1994. Lucilia sericata (Diptera: Calliphoridae), causing hospital-acquired myiasis in a traumatic wound. J Hosp Infect 28 :149–152.

    • Search Google Scholar
    • Export Citation
  • 14

    Minár J, Herold J, Elisková J, 1995. Nozokomiálni myiáze ve stredni Evrope. Epidemiol Mikrobiol Immunol 44 :81–83.

  • 15

    Sherman RA, Hall MJR, Thomas S, 2000. Medicinal maggots: an ancient remedy for some contemporary afflictions. Annu Rev Entomol 45 :55–81.

    • Search Google Scholar
    • Export Citation
  • 16

    Amoudi MA, Diab FM, Abou-Fannah SSM, 1989. The occurrence of Megaselia scalaris (Loew) (Diptera: Phoridae) in Saudi Arabia with some aspects on the life history and distribution in Riyadh Province. J King Saud Univ Sci 1–2 :43–51.

    • Search Google Scholar
    • Export Citation
  • 17

    Disney RHL, 1994. Scuttle Flies: The Phoridae. London: Chapman and Hall.

  • 18

    Austen EE, 1910. Some dipterous insects which cause myiasis in man. Trans R Soc Trop Med Hyg 3 :215–242.

  • 19

    Hardy DE, 1951. A case of apparent human myiasis. Proc Hawaiian Entomol Soc 14 :212–213.

  • 20

    Abram LJ, Froimson AI, 1987. Myiasis (maggot infection) as a complication of fracture management: case report and review of the literature. Orthopedics 10 :625–627.

    • Search Google Scholar
    • Export Citation
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