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Human myiasis in New Zealand: imported and
indigenously-acquired cases; the species of concern and clinical
aspects
José G B Derraik, Allen C G Heath, Marius
Rademaker
Myiasis is defined as “the infestation of live human
and vertebrate animals with dipterous larvae, which, at least for a certain
period, feed on the host’s dead or living tissue, liquid body-substances,
or ingested food”.1 From a
parasitological perspective myiases may be classified as obligatory, facultative
or accidental.1,2
Obligatory parasites—dependent on the host for a part
of their life cycle.3 The larvae are deposited
either directly on the skin or mucous membranes (e.g. Oestrus spp. and
Rhinoestrus spp.), penetrate normal skin (e.g. Gasterophilus
spp. and Hypoderma spp.), or become superimposed on pre-existing wounds
(e.g. Chrysomya spp.).
Facultative parasites—normally free-living, with
larvae developing in decaying organic matter,3
but which may occasionally contaminate living tissue, such as pre-existing
wounds, ulcers and cavities (e.g. the genera Musca and
Calliphora).
Accidental myiasis or pseudomyiasis—it occurs when the
larvae of a normally free-living species are swallowed with contaminated food,
passing through the alimentary canal where they may cause pathological
reactions.1
The literature on human myiasis in New Zealand is scarce,
but recently two cases have been discussed in this journal, both of which were
acquired overseas.4,5 In this review, we
provide a comprehensive account of human myiasis in New Zealand by: i) examining
the Diptera species present in New Zealand that have been associated with human
myiasis; ii) reviewing the published and unpublished records of human myiasis in
New Zealand, which were either indigenously-acquired or imported; iii) briefly
outlining the diagnostic and clinical features of human myiasis and its
treatment, as few medical practitioners in New Zealand are acquainted with such
a condition.
Clinical features of human myiasisMyiasis in humans may lead to a number of clinical features.
Cutaneous myiasis is characterised by infestation of the skin and subcutaneous
tissue, and is mostly caused by the larvae of obligatory parasites, although a
number of facultative parasites may be associated with wound myiasis. Cutaneous
myiasis can be sub-divided into furuncular, creeping, wound and
subcutaneous:
Myiasis
may also affect body cavities such as the ears, eyes, nose, and genitals, as
well as the gastrointestinal tract:
Figure 1. Lucilia sericata. Although
an agent of human myiasis, this species is medically employed in maggot
debridement therapy (adult photo courtesy of John Carr; larvae photo believed to
be in the public domain)
 Myiasis-causing flies established in New ZealandThere are no native fly species in New Zealand that are
known to have caused myiasis in humans. Although numerous introduced species of
Diptera present in New Zealand cause myiasis, most are not commonly associated
with human cases. Nevertheless, a number of these have been recorded to cause
human myiasis overseas (Table 1) and, in some rare instances, in New Zealand as
well (Table 2).
Most of the species listed in Table 1 are not obligatory but
rather facultative parasites. One such species is the common house fly Musca
domestica (Figure 2), which is associated in particular with wound myiasis
(Table 1). Although this species is extremely widespread and abundant throughout
the world, human myiasis caused by M. domestica appear to be relatively
rare.9
A number of the species listed in Table 1 are obligate
parasites of other mammals. For example, 15 years ago it was estimated that at
least NZ$30–40 million in annual losses were accrued by sheep farmers in
New Zealand111 due to myiasis associated with
the blow flies (Calliphoridae) Lucilia (=Phaenicia) cuprina,
Lucilia (=Phaenicia) sericata, Calliphora stygia and
Chrysomya rufifacies.10-12 These
species are also occasionally found on other livestock such as goats and
cattle,11 but may cause myiasis in humans
(Table 1).
Lucilia sericata in particular, seems to be
associated with human wound myiasis in some
countries,13 and less commonly in other forms
of myiasis. Other species occasionally associated with ovine myiasis such as
Calliphora hilli and C. vicina are also implicated in human
myiasis (Table 1). In New Zealand, one case of aural myiasis caused by
Lucilia sericata was recorded in the Waikato region (Table 3).
Recently two new introduced species of facultative
parasites Megaselia scalaris and M. spiracularis (Phoridae)
have been recorded in New Zealand.14 Larvae of
M. scalaris have been associated with a number of cases of human
myiasis, but human parasitism by M. spiracularis appears to be
extremely rare (Table 1). Two other species of arguably lesser economic
importance in New Zealand are Oestrus ovis and Gasterophilus
intestinalis (Table 1). The only other member of the Oestridae in New
Zealand, Gasterophilus nasalis is reported to be incapable of
penetrating human skin,1 but has been
associated with gastro-intestinal myiasis (Table 1).
Figure 2. Musca domestica, the common
house fly (adult photo courtesy of Joseph Berger; larvae photo courtesy of
Clemson University, USDA Cooperative Extension Slide Series).
 Table 1. Diptera species present in New Zealand
and records of human myiasis caused by them overseas. The list of Diptera was
primarily based on available resources14,63,64
and on information from known authorities on this group
† Identification uncertain.
|
|
Origin of infestation
|
Species
|
Type of myiasis
|
References
|
|
Imported
|
Dermatobia hominis
|
cutaneous
|
5, 110
|
|
New Zealand
|
Gasterophilus intestinalis
|
cutaneous
|
30
|
|
|
Oestrus ovis
|
ophthalmic
|
15, 16, 17, 18
|
|
|
|
nasal
|
15
|
Table 3. Unpublished accounts of imported and
indigenously-acquired cases of human myiasis in New Zealand
|
Origin of infestation
|
Species
|
Comments
|
|
Imported
|
?Dermatobia hominis
|
• ca.1999. Female tourist arriving in New Zealand
from Latin America. A single unidentified larva was removed from the
patient’s skin in the occipital region. In view of the country of origin
of the infestation, the species involved is presumed to be D. hominis
(Joan Ingram, pers. comm. 2009).
|
|
|
|
• 2008. Cutaneous myiasis on tourist arriving from
the Amazon region. Species presumed to be D. hominis (Kerry Read, pers.
comm. 2009).
|
|
|
Dermatobia hominis
|
• March 1999, Auckland Hospital. A 2nd-instar larva
surgically removed from the right shoulder of a female tourist arriving in New
Zealand from Bolivia (Trevor Crosby, pers. comm. 2010).
|
|
|
|
• April 1999, Auckland Hospital. A 3rd-instar larva
removed from the leg of a female tourist arriving in New Zealand from Bolivia
(Trevor Crosby, pers. comm. 2010).
|
|
|
Unidentified sp.
|
• 2009. Waitakere Hospital. No details available,
except that the patient was a New Zealander who had recently returned from a
trip to South America (Fiona Larsen, pers. comm. 2010).
|
|
New Zealand
|
Eristalis tenax
|
• Two cases of intestinal myiasis, the most recent
of which was recorded in a patient from Blenheim in 2000. No further information
is available (Graeme Paltridge, pers. comm. 2010).
|
|
|
Lucilia sericata
|
• April 1999, Waikato Hospital. Numerous larvae
were removed from the left mastoid cavity of an 81-year-old male (Dallas Bishop,
pers. comm. 2009).
|
|
|
Oestrus ovis
|
• January 1997, Hamilton. First instar larva
removed from the eye of a human male (larva submitted to ACG Heath at the time
by WG Elmsbury).
|
|
|
|
• February 2005, Auckland Hospital. Three first
instar larvae were removed from the eye (conjunctival sac) of a woman who lived
in semi-rural Auckland (larvae provided to ACG Heath at the time by James Usher,
LabPlus).
|
|
|
Unidentified sp.
|
• Waikato Hospital. Three cases of wound myiasis on
leg ulcers on elderly patients, as a result of poor care (pers. obs.).
|
|
|
|
• Palmerston North. No date or details available,
except that the patient had extensive myiasis on the leg (Scott Barker, pers.
comm. 2010).
|
|
|
|
• 1995. Napier. Myiasis on leg ulcers of a male
indigent, as a result of poor wound care (Ian McQuillan, pers. comm.
2010).
|
|
|
|
• 2002, wound myiasis on a mentally ill woman from
Canterbury as a result of poor wound care (Graeme Paltridge, pers. comm.
2010).
|
Figure 3. Oestrus ovis, the sheep
botfly (adult photo courtesy of Anthony Daley; larvae photo courtesy of the
Universidad Autònoma de Barcelona)
Although the larvae of some flies may cause irreversible
damage to orbital contents (e.g. Cochliomyia
hominivorax),28 O. ovis
ophthalmic myiasis is said to be self-limiting in humans, as the larvae
generally do not develop beyond first stage in the human
eye.1,22 As a result, the course of O.
ovis myiasis is almost invariably benign conjunctival myiasis
(ophthalmomyiasis externa) in healthy human
hosts.28 Since O. ovis is widespread
in New Zealand,19 and its clinical effects are
relatively minor, it is likely that numerous cases of O. ovis
ophthalmomyiasis externa go unreported.
One case of cutaneous myiasis in New Zealand due to
Gasterophilus intestinalis (the horse botfly; Figure 4) has also been
recorded.30 Horses are the primary hosts for
this botfly, in which the larvae migrate through the animals’ alimentary
canal to complete their life cycle.30 This does
not occur in humans, and infestation appears to be limited to cutaneous myiasis.
As with O. ovis, G. intestinalis appears incapable of
developing beyond the first larval stage in human
hosts.17,30
Figure 4. Gasterophilus intestinalis,
the horse botfly (adult photo courtesy of Robert Nash; larva photo courtesy of
Kalumet)
There have been at least two recorded cases of intestinal
myiasis caused by Eristalis tenax (Figure 5; Table 2), but no specific
details have remained for any of the cases (Graeme Paltridge, pers. comm. 2010).
Eristalis tenax (Syrphidae; commonly known as hover fly or drone fly)
is a cosmopolitan species. There are occasional records of myiasis associated
with it, particularly of accidental intestinal myiasis (Table 1) resulting from
the ingestion of contaminated food.106 Clinical
presentation is varied, and although it may be asymptomatic some patients may
experience abdominal pain, nausea and
vomiting.106
Figure 5. Eristalis tenax, the
drone-fly or hover fly. Note the bee-like appearance of the adult and the
characteristic ‘rat-tailed’ larva (adult photo courtesy of
Fir0002/Flagstaffotos; larva photo courtesy of Jarmo Holopainen)
Despite the lack of published records, myiasis associated
with infected wounds does occur in New Zealand (Table 3). Although we do not
know the frequency of such occurrences or the species involved, these seem to be
primarily opportunistic myiases associated with the elderly at home, as a result
of poor wound care (pers. obs.; Graeme Paltridge, pers. comm. 2010).
Lastly, an article from Japan describes the case of a woman
who apparently contracted cutaneous myiasis by the cattle warble fly,
Hypoderma bovis (Oestridae), while travelling in New
Zealand.31 This species has not
established in the Southern Hemisphere,19 and
it does not occur in New Zealand, although it has been introduced at least once
on imported cattle from the UK (G. Adlam, pers. comm. 1977). Since H.
bovis is established in Japan,32 the
infestation most likely occurred in that country.
Imported cases of myiasis
Imported cases of human myiasis are a worldwide occurrence
among travellers returning from the
tropics.33-38 Although a few fly species may be
involved, human cases appear to be caused primarily by Dermatobia hominis
(Cuterebridae; Figure 6)33,35,37,39 and
Cordylobia anthropophaga
(Calliphoridae).35–38 Both species
have a life cycle that alternates free-living and parasitic stages, causing
primarily cutaneous myiasis.
Figure 6. Dermatobia hominis, the
human botfly (adult photo courtesy of Lyle J Buss; larva photo courtesy of
Medical Illustrations, Christchurch Hospital)
Although these are particularly common overseas, cases of
myiasis in travellers returning to New Zealand are rarely described. We have
been able to ascertain the occurrence of only seven cases of imported myiasis in
New Zealand, just two of which have been published in the medical literature
(Tables 2 & 3). Dermatobia hominis was the likely culprit in six
cases (certainly in two); a case of wound myiasis due to Lucilia
cuprina imported from Fiji has also been recorded (Tables 2 & 3).
Surprisingly, there seems to be no recorded cases of
Cordylobia anthropophaga myiasis imported into New Zealand (the larvae
in Edwardes4 was removed while overseas), but
in view of its importance in cases worldwide we provide a more in depth
discussion of this species and D. hominis as well.
Dermatobia hominis
The human botfly is widespread in tropical and subtropical
Latin America, from the south of Mexico to the north of
Argentina,40,41 and one report suggests that it
is established in Saudi Arabia.42 The adult fly
lays eggs on the body of anthropophilic insects which they catch, usually
mosquitoes (Culicidae), but flies from six other Diptera families have also been
implicated as vectors.43 Eggs remain attached
to the vector and emerge upon contact with the skin of the host, eventually
penetrating the skin and disappearing into the subcutaneous
tissue.43 The range of hosts includes a large
number of vertebrates such as humans, monkeys, most domestic animals, and
birds.41,44 Although cases of D.
hominis myiasis are primarily cutaneous, there are a number of records of
ophthalmomyiasis.45 In some cases, the larvae
may burrow into deeper tissues causing severe symptoms: deaths from larvae
burrowing through the fibrous portion of the fontanelle of neonates have been
reported.44,46
The larvae are parasitic from the
1st to 3rd
instars,40 taking 30 to 40 days for larval
development to occur.47 Eventually larvae will
abandon the host, falling onto the soil where they pupate, developing into
adults some 30 to 60 days later.47 The
incidence of D. hominis is directly related to suitable climatic
conditions,40,48 preferring a high relative
humidity and high mean temperatures
(ca.20°C).41 Although D. hominis
is present in subtropical South America, it seems unlikely that it would
encounter suitable climatic conditions for establishment even in the warmest
regions of New Zealand.
Cordylobia anthropophaga
The tumbu fly is widespread in sub-Saharan
Africa,36 and it is a common cause of human
myiasis36,49,50 Cordylobia anthropophaga
females lay egg batches directly on dry shaded ground, but these are also
laid on laundry.50 As a result, cutaneous
myiasis can occur from contact with infested clothing, leading to parasitism in
normally unexposed areas of the body, such as the
genitals.51,52
Larvae hatch in 1–3 days but may survive for
9–15 days unnourished, until activated by the host’s body heat or
movement.2,50 They are able to attach
themselves and immediately burrow into the skin of an unsuspecting host,
remaining at the site of entry, where they grow for 8–15 days in a
furuncle-like lesion.2,50,53 Once the growth
period is over, the third stage larva leaves the furuncle, falling to the ground
to pupate.50,53 Apart from humans, C.
anthropophaga is known to affect dogs and
rats,2 but it is likely to also infest a range
of other hosts.
Myiases due to C. anthropophaga are likely to be
relatively benign as the larvae do not migrate into deeper
tissues.2,53 Further, it seems that C.
anthropophaga larvae secrete an antibacterial fluid, which may prevent
secondary infection.54
Prevention relies on ironing clothes prior to use, or drying
them in full sunlight or under a mosquito
net.36,55 Insect repellents are considered
ineffective in the prevention of this
myiasis.36
Although C. anthropophaga is a common cause of
myiasis in travellers returning from endemic
areas,35,36 the evidence that it has become
established outside its African range and Saudi
Arabia2,36 is poor and based solely on isolated
case reports. These include cases in England,56
Netherlands,57 and
Spain.36 A further report from Britain claims
that the infestation was acquired in
Portugal.58 However, although the patient
herself had not visited any known endemic areas prior to her return to the UK,
one cannot disregard the possibility that she had been in contact with
contaminated clothing brought from Africa, as happened in cases acquired in
England56 and
Australia.119
One report from Japan describes successful emergence of a
C. anthropophaga adult from a pupa at room
temperature,59 but this is unlikely to have
occurred outdoors, and even more unlikely to have successfully led to an
established population. In view of its tropical distribution and the
species’ lack of establishment in countries with warmer climates and
greater frequency of imported cases, the risk of C. anthropophaga
becoming established in New Zealand is considered to be very low.
Diagnosis and treatment in New Zealand
As is the case with other rare conditions, diagnosis of
myiasis may be easily missed. However, since Diptera species able to cause
myiasis in humans are present in New Zealand and the rate of international
travel continues to increase, it is important that primary care physicians and
nurses are aware of the clinical features of myiasis.
Patients often describe the sensation of movement under the
skin in association with a lesion resembling a boil or
furuncle.60 In the case of exotic species such
as D. hominis and C. anthropophaga, such symptoms
would be associated with recent travel history to the tropics, providing the
attending medical practitioner with clues to reach an appropriate diagnosis.
However, whilst the absence of recent travel to the tropics minimizes the
likelihood of myiasis, it does not entirely exclude it, in view of the fly
species present in New Zealand.
Numerous techniques have been employed to remove the
larvae.60 In the case of furuncular lesions,
occlusion of the skin pore for up to several hours to block the larva’s
breathing orifice is a widely used method. This can be achieved with a variety
of substances such as petrolatum, paraffin, beeswax, pork fat or chewing
gum.60,61 These force the larva to protrude its
posterior spiracle in search of air, consequently facilitating its removal. This
is a useful technique as some botflies have a tapered shape with rows of spines
and hooks which prevent simple extrusion through the central punctum (Figures 4
& 5).
When the larva surfaces for air, it can be manually
extracted with the aid of forceps, with care not to puncture the larva.
Alternatively, ethyl chloride sprays, liquid nitrogen, 15% chloroform in oil or
1% ivermectin cream have been used alone or in combination. Additionally,
lidocaine can be injected into the base of the tissue cavity which the larva
inhabits, thereby forcing the larva to the surface through hydrostatic
pressure.112
Pressure extraction by the application of slow, firm
pressure to the sides of the lesion (similarly to squeezing an acne spot) is
commonly used. A study in Ethiopia found that 87% of rural residents used this
method to remove C. anthropophaga
larvae.62 However, this can result in
secondary infections, abscesses, severe inflammatory reactions and even fatal
outcomes due to incomplete removal of the
larvae.54,62 Therefore, it is important to
extract the larvae in its entirety.
If the larva cannot be easily extracted, it may be necessary
to enlarge the opening with a small incision under local anaesthetic.
Alternatively, the whole lesion (and larva) can be primarily excised under local
anaesthetic. It is important that the wound is thoroughly cleaned after removal
of the larva.
For wound and cavitary myiasis, the cavity or wound can be
irrigated with 15% chloroform in oil or soaked with 1%
ether.113,114 Larvae can then be removed with
forceps using an aseptic technique. Ivermectin has also been used for some cases
of myiasis, particularly involving the eye and
mouth.115-117
Conclusions
It seems that the most important myiasis-causing species in
New Zealand is the sheep nasal botfly Oestrus ovis. However, since such
cases tend to be self-limiting, and the infestation is usually benign, it is
likely that the majority of cases go unreported in the literature. As a result,
the actual prevalence of myiasis in New Zealand is likely to be considerably
greater than what is reported.
The increasing rate of international travel and the
consequent greater number of travellers arriving from tropical regions is likely
to lead to an increase in the number of cases being imported into New Zealand.
Fortunately, the main species involved are not likely to
become established in New Zealand and are therefore unlikely to pose a
biosecurity risk, although this risk assessment may change in the future under a
climate change scenario. Nonetheless, it is important that medical practitioners
are acquainted with the diagnosis and treatment of myiasis.
Also, in order to obtain an accurate estimate of myiasis
incidence in the country, we encourage that such cases are appropriately
recorded and/or published in the medical literature. For this purpose,
assistance with larval identification can be obtained (ACG Heath; email: allen.heath@agresearch.co.nz).
Ideally, specimens should be preserved in a solution of 70%
ethanol and 30% distilled water, but if necessary they may be also preserved in
methylated spirits or spirituous liquors, which are likely to be available in
most homes in New Zealand.
Competing interests: None.
Author information: José G B
Derraik, Honorary Research Associate, Disease & Vector Research Group,
Institute of Natural Sciences, Massey University, Albany Campus, Auckland; Allen
C G Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and
Infectious Disease, Wallaceville, Upper Hutt; Marius Rademaker, Honorary
Associate Professor, Department of Dermatology, Waikato Hospital, Hamilton
Acknowledgements: We would like to
acknowledge Graeme Paltridge (Canterbury Health Laboratories), Trevor Crosby
(Landcare Research), Dallas Bishop (Asurequality), Joan Ingram, Kerry Read, Mark
Jones, James Usher, WG Elmsbury, Ian McQuillan, Scott Barker, Fiona Larsen, and
other persons who contributed with specimens, unpublished material and
observations. Thanks to Martin Hall (Natural History Museum, U.K.) and Trevor
Crosby for valuable feedback on this manuscript. Thanks also to the
photographers and organisations who kindly gave us permission to use their
images to illustrate this article: Anthony Daley; John Carr; Joseph Berger
(Bugwood.org); Lyle J Buss (University of Florida); Robert Nash (National
Museums Northern Ireland); Medical Illustrations (Christchurch Hospital);
Clemson University (USDA Cooperative Extension Slide Series); Universidad
Autònoma de Barcelona; Jarmo Holopainen (University of Eastern Finland);
and Fir0002/Flagstaffotos (license: http://en.wikipedia.org/wiki/GNU_Free_Documentation_License).
Correspondence: José G B Derraik.
Email: derraik@gmail.com
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