ARTICLE
Auteur(s) : Andreas M
Sesterhenn1, Wolfgang Pfützner2, Daniel M
Braulke1, Susanne Wiegand1, Jochen A
Werner1, Anja Taubert3
1Department of Otolaryngology, Head & Neck
Surgery, Philipps-University Marburg, Deutschhausstrasse 3, 35037
Marburg, Germany
2Department of Dermatology and Allergology,
Philipps-University Marburg, Deutschhausstrasse 3, 35037 Marburg,
Germany
3Institute of Parasitology, Justus Liebig
University Giessen
accepté le 26 Août 2008
Human myiasis, i.e. the infestation of live humans with
dipterous larvae feeding on the host’s tissue, occurs worldwide and
mainly in tropical areas, but is rarely described in European
countries and North America. After deposition of the eggs on the
wound surface, larvae hatch out and preferably colonize the
affected lacerated, moist and exudative tissue. A broad range
of fly instars have been described as the origin of myiasis,
comprising different diptera families, such as Calliphoridae,
Sarcophagidae and Oestridae. Flies causing myiasis, in general, are
categorized into three main groups according to the types of
host-parasite relationship: obligative, facultative and accidental
myiasis-producing flies [1]. In Europe, species provoking human
myiasis are mainly obligate or facultative and mostly concern the
development of wound myiasis brought about by either sarcophorid
larvae of Wohlfahrtia spp. or calliphorid instars of Calliphora or
Lucilia spp.. One representative of the latter group is Lucilia
sericata, the most common species in Germany, which is also known
as the green bottle blowfly or the sheep strike blowfly. This
species represents a widespread causative organism of myiasis of
sheep in Europe [1, 2] and has been reported to affect humans as
well [3-9]. Human myiasis, in general, is reported to occur
especially in elder, sometimes debilitated patients, who display
disturbed consciousness or hypoesthesia preventing them from
recognising the fly’s contact or fending off these arthropods [5,
10]. Worldwide, cases of myiasis in humans have been reported for
multiple localisations, such as the foot, sternal, vulvar or
tracheostomy wounds, leg ulcer, nose/sinuses, ear, eye (orbit),
oral cavity or lymph nodes [11-21]. Some of them had a nosocomial
background [22] and a few were associated with tumor lesions [7,
23-37].
Since 2002 altogether 3 patients have presented with myiasis in
cutaneous neck metastases during the follow-up of head and neck
cancer patients in the oncology clinic of our department. In the
last case an exact parasitological work-up of the maggots was
performed. Reports on myiasis in malignant wounds resulting from
head and neck cancer are rare in the medical literature.
A thorough medline search revealed 19 reports on myiasis
associated with malignant wounds resulting from head and neck
cancer. Furthermore, an approved and effective treatment concept
for cases of cutaneous myiasis in malignant wounds in head and neck
cancer patients does not exist, to our knowledge. The aim of this
study is the presentation of a further case and review of the
literature, with a focus on treatment options.
Case report
Clinical course
A 61-year-old male patient was initially diagnosed as suffering
from recurrent squamous cell carcinoma of the right oropharynx
(T2N2bM0) in September 2005. The first-line surgical treatment
included conventional tumor resection, bilateral neck dissection
and reconstruction of the defect using a microvascular anastomosed
radial-forearm flap. Based on the histologically proven
loco-regional lymphnode metastasation the patient received
chemo-radiotherapy. During oncological follow-up one year after the
first diagnosis, the patient presented with a rapidly growing,
progressive neck mass in level IV and V on the right side. MRI
scanning showed a tumor of 41 × 28 × 24 mm in size.
A punch biopsy was performed. The histological result revealed
a recurrence of cancer. For this reason the patient received
brachytherapy and subsequent re-irradiation.
In January 2007 a second recurrence on the right side of the
neck with infiltration of the subcutaneous tissue was diagnosed.
The interdisciplinary oncological conference of the local
comprehensive cancer center recommended, as the treatment of
choice, surgical revision in terms of a radical neck dissection
with resection of the infiltrated skin area and restoration using a
pedicled myocutaneous pectoralis-major-flap, with a palliative
intention. Additionally there was suspicion of pulmonary
metastases. Therefore the patient received palliative
chemotherapy.
The patient was discharged from hospital at his own wish and did
not attend the scheduled appointments of oncological follow-up.
Four months later another cervical recurrence became evident on the
right side. When he presented again at the clinic, a giant
exophytically growing, superinfected skin metastasis was visible
(figure 1).
Furthermore, there was an unbearable malodour resulting from the
secreting lesion. On closer inspection, multiple active maggots
were found infesting all over the surface of the affected area
(figure 2). The
lesion was macroscopically cleared of visible maggots by mechanical
removal. Some of them were sent for parasitological diagnosis. In
the absence of reliable treatment options, the lesion was rinsed
using an H2O2-solution and metronidazol twice
a day. Additionally, dressings were changed twice a day. In the
further course no more maggot infestion was observable
macroscopically. After electrosurgical debulking of the metastasis
the patient was referred to the local hospice for the best
supportive care, where he died several weeks later.
Parasitological examination
Larvae were placed in 70% ethanol and thoroughly examined
microscopically. The posterior spiracles and the cephalopharyngeal
skeletons were excised, mounted in Berlese mixture and analysed
microscopically. Of the specimens examined, one was a second instar
larvae, the others, third instars. The larvae were identified as
Lucilia species (Diptera: Calliphoridae) on the basis of different
morphological findings: the larvae were typically maggot form
shaped (figure
3A) and their anterior spiracles protruded through the body
wall, forming fan-shaped structures with 8 finger-like lobes each.
The posterior spiracles contained a peritreme that formed a fully
closed ring, also surrounding the clearly visible button (figures 3B, C). The
slits of the spiracular plates were straight and parallel to each
other (figure
3C). The mouth hooks of the cephalopharyngeal skeletons
lacked an accessory oral sclerite (figure 3D).
Discussion
Human myiasis caused by instars of Lucilia sp. represents a disease
rarely observed in Germany due to the climate and hygienic
conditions common in this country. However, we describe here a case
of wound myiasis occurring in a patient with extensive cervical
cutaneous metastasation. As typical for reports on myiasis in
non-tropical areas, the current case occurred in the summer, i.e.
when the fly population is at its highest density. In contrast to
flies causing obligate myiasis, the feeding behaviour of larvae of
Lucilia spp. usually is restricted to superficial nutrition on the
epidermis, lymphatic exsudates or on necrotic tissue, and only
occasionally concerns healthy tissue [1]. Nevertheless, extensive
tissue damage may occur and severe clinical disease comprising
toxaemia has been reported for sheep struck by L. cuprina [38]. One
major problem in myiasis is the putative transfer of bacterial
pathogens. In general, larvae causing myiasis have been
demonstrated to carry a broad spectrum of bacteria [39, 40] and
may, in consequence, contribute to the progressive aggravation of
inflammatory processes.
In the current case the identification of the pathogen was based
on morphological aspects of the larvae as rearing to adults for
conformational analyses was not performed. However, the available
characteristics clearly indicated Lucilia spp. Furthermore, the
number of lobes of the anterior spiracle and the knowledge of the
distribution of Lucilia spp. in Germany pointed to L. sericata as
the infesting species.
Including the present one, so far 20 cases of cutaneous myiasis
in malignant wounds resulting from primary cancer of the head and
neck area have been published in the literature (table 1). Cases were predominantly associated with
squamous or basal cell cancer of the skin. Regarding therapeutical
approaches, a systemic medical or standard treatment protocol for
human myiasis is currently not available, to our knowledge. In this
respect there is a clear treatment dilemma. Ectoparasitic drugs are
known to have irritating and sometimes severe toxic side effects
when applied to open wounds, and should therefore only be used with
restriction and care. Furthermore clinical trials on the efficacy
of ectoparasitic drugs like lindane, malathion, permethrin,
pyrethrum or ivermectin in human myiasis have not been conducted so
far. In a case report, Osorio et al. suggested that ivermectin may
play an important role in the treatment of severe cases of orbital
myiasis due to Cochliomyia hominivorax [41]. Radmanesh suggested
paralyzing larvae by pouring a drop of lidocain over them [30]. In
most cases a surgical excision (n = 9) of the infested lesion was
performed after the maggots were mechanically removed (n = 7).
Local treatment like antiseptic rinsing (n = 7) or application of
petroleum jelly (n = 3) was another effective therapy option.
Advanced disease in head and neck cancer is often associated
with the occurrence of disseminated loco-regional and distant
metastases. At this stage of the disease the point of incurability
will be reached when effective treatment options have all been
tried or are regarded as ineffective. Soon the disease gets out of
control, with subsequent unstoppable progression of cancer. From
experience it is known that many of the affected patients develop
extensive cutaneous metastases in this situation, which may grow,
fungating and exophytically. If wound care and dressing changes at
this stage are inadequately and only sporadically performed, the
affected patients are at risk of developing severe superinfections
of the exulcerating metastases from different origins (e.g.
bacteriological, parasitological). Thus, unpleasant odorous
secretions are likely to result. This kind of tissue is attractive
to different species of flies, which may deposit their eggs in this
medium, especially in the spring and summer months.
Although squamous cell cancer can originate throughout the body,
involvement of the skin tends to occur with a special predilection
in the head and neck area since this part of the body usually
remains uncovered. However, it seems to be indispensable that
malignant wounds (whether primary tumor or metastasis) if situated
in exposed locations like the scalp, face or neck, should always be
covered by dressings in extenso. Furthermore, dressings have to be
changed and wounds should receive local treatment on a daily basis.
On the other hand, advanced terminal head and neck cancer is often
associated with intermittent haemorrhage from malignant neck
wounds. This is a sign of an impending bleeding of the carotid
artery or of one of its branches which mostly peaks in a disaster.
For this reason health care professionals avoid frequent dressing
changes and wound care in these situations, to prevent disastrous
bleeding episodes. In this regard, occlusive foil dressings may be
a reliable alternative to conventional gauze dressings.
None of the published cases reports on permanent health damage
to the infested individual, so far. Interestingly, some of these
species (e.g. L. sericata) are most commonly used in medical maggot
debridement, with therapeutic intent for various indications. These
larvae are cultured axenically and subsist on non-viable tissue and
will starve if fed clean granulation tissue.
To imagine an infestation of parts of one’s body by fly larvae
is a horrifying and nauseating scenario for most people. If such a
situation is recognized by the patient himself, especially by
patients suffering from end-stage cancer, this fact inevitably
brings to mind the impending prostration and decomposition of the
whole body. The awareness of myiasis is likely to cause sustainable
psychological effects on patients’ minds. This circumstance must be
avoided and calls for immediate termination of the infestation.
Furthermore, it stands to reason that the situation described is
also extremely burdening for all those involved with its treatment,
such as the relatives and attending staff. Most medical and nursing
staff appear unprepared or unwilling to make the assessment of
maggots themselves. Unlike almost any other clinical specimen,
maggots are often discarded (in haste and with disgust), rather
than submitted to the laboratory for analysis. Infested patients
should not be treated with disgust, and their maggots should not be
hastily discarded. Histories and physical examinations always must
be comprehensive, and the condition of the patient’s hygiene and
clothing must be noted [42]. On the other hand, nosocomially
acquired infestations appear quite common, occurring in hospital
rooms with unscreened windows that had most likely been opened.
Important features contributing to nosocomial infestations listed
by Greenberg [13] are: a) helpless and debilitated patients, b)
blood and/or odours of decomposition, c) nursing neglect, d) summer
season. Furthermore it is likely that many cases of myiasis go
unreported for various cultural, social, and medicopolitical
reasons [43].
The present article highlights the urgent need for patients to
understand the importance of keeping malignant wounds, not only in
the head and neck area, dressed, and for nursing staff to be
informed about patients leaving hospital with malignant wounds
requiring dressing and supervision. The current treatment concept
in the case of myiasis in malignant wounds comprises mechanical
removal of maggots, surgical debridement of the infested wound bed,
intensive rinsing with antiseptic solutions and consistent dressing
changes on a daily basis. A complete covering of the wound
surface is indispensable, especially in the summer months.
Table 1 Cases of cutaneous myiasis in malignant wounds
in the head and neck area
|
Author
|
Year
|
Species
|
Localization
|
Histology
|
Therapy
|
|
Arbit E et al. [26]
|
1986
|
Diptera Sarcophaga
|
Skin (scalp/scull)
|
SCC
|
Removal by ethyl alcohol; Surgical excision
|
|
Agarwal DC et al. [27]
|
1990
|
NOS
|
Orbit/eye
|
BCC
|
Removal; Turpentine oil packing; rinsing with KMnO4;
antibiotics
|
|
Anegg B et al. [23]
|
1990
|
Lucilia sericata
|
Skin; Helix
|
Bowen’s disease
|
Removal
|
|
Bosniak SL et al. [28]
|
1990
|
NOS
|
Skin; Eyelid
|
BCC
|
Surgical debridement
|
|
Novelli MR et al. [29]
|
1993
|
NOS
|
neck lymph node
|
CA NOS
|
Surgical excision of lymph node
|
|
Phillips WG et al. [24]
|
1993
|
Calliphorid larvae
|
Skin; temporal (during RT)
|
SCC
|
Dressing with povidone iodine + paraffin gauze, surgical
excision
|
|
Radmanesh M et al. [30]
|
2000
|
Chrysomyia bezziana
|
Orbit/eye
|
BCC
|
Orbital exenteration
|
|
Sherman RA [41]
|
2000
|
Lucilia sp.
|
Neck fistula from oropharyngeal cancer
|
CA NOS
|
NOS
|
|
Sherman RA [42]
|
2000
|
Lucilia sericata
|
Skin; facial
|
CA NOS
|
NOS
|
|
Caca I et al. [31]
|
2003
|
Hypoderma bovis
|
Orbit/eye
|
BCC
|
Orbital exenteration; total maxillectomy
|
|
Kokcam I et al. [32]
|
2005
|
Wohlfahrtia magnifica
|
Skin; fronto-temporal
|
BCC
|
Removal; dressing with povidone iodine
|
|
Hawayek LH et al. [33]
|
2006
|
« botfly larvae »
|
Skin; parieto-occipital
|
SCC
|
Application of petrolatum jelly
|
|
Rubio C et al. [25]
|
2006
|
Chrysomya sp.
|
Skin metastasis (neck) from laryngeal cancer
|
SCC
|
Surgical excision
|
|
Rubio C et al. [25]
|
2006
|
Sarcophaga
|
Skin (scalp)
|
BCC / SCC
|
Antiseptic treatment; petroleum jelly
|
|
Rubio C et al. [25]
|
2006
|
Sarcophaga
|
Skin; preauricular
|
BCC
|
Antiseptic treatment; petroleum jelly
|
|
De Souza A et al. [34]
|
2006
|
NOS
|
Skin; facial
|
BCC
|
Surgical excision
|
|
Bouwman LH et al. [35]
|
2007
|
Lucilia sericata
|
Skin; fronto-parietal
|
BCC
|
Surgical excision
|
|
Cheshier SH et al. [36]
|
2007
|
Lucilia sericata
|
Skin (scalp)
|
Angiosarcoma
|
Removal
|
|
Gabriel JG et al. [37]
|
2008
|
NOS
|
Skin; cervico-facial
|
SCC
|
Removal
|
|
Carvalho RW [21]
|
2008
|
NOS
|
Skin; buccal mucosa
|
SCC
|
Removal
|
|
Sesterhenn AM et al. [present article]
|
2008
|
Lucilia sericata
|
Skin metastasis (neck) from oropharyngeal cancer
|
SCC
|
Removal; rinsing with H2O2 and metronidazol;
electro-surgical debulking
|
Acknowledgements
Financial support: None. Conflict of Interest: None.
References
1 Hall M, Wall R. Myiasis of humans and domestic animals.
Adv Parasitol 1955; 35: 257-334.
2 Hall MJ. Traumatic myiasis of sheep in Europe: a review.
Parasitologia 1997; 39: 409-13.
3 Granz W, Schneider D, Schumann H. Human myiasis
in middle Europe. Z Gesamte Inn Med 1975; 30: 293-301.
4 Bauch R, Ziesenhenn K, Groskopff C. Lucilia
sericata myiasis (Diptera, Calliphoridae) in gangrene of the foot.
Angew Parasitol 1984; 25: 167-9.
5 Daniel M, Sramova H, Zalabska E. Lucilia
sericata (Diptera: Calliphoridae) causing hospital-acquired myiasis
of a traumatic wound. J Hosp Infect 1994; 28: 149-52.
6 Minar J, Herold J, Eliskova J. Nosocomial
myiasis in Central Europe. Epidemiol Mikrobiol Imunol 1995; 44:
81-3.
7 Minar J, Valkoun A. Myiasis in a skin tumor.
Epidemiol Mikrobiol Imunol 1998; 47: 32-4.
8 Amitay M, Efrat M, McGarry JW, et al.
Nosocomial myiasis in an extremely premature infant caused by the
sheep blowfly Lucilia sericata. Pediatr Infect Dis J 1998; 17:
1056-7.
9 Hira PR, Assad RM, Okasha G, et al.
Myiasis in Kuwait: nosocomial infections caused by Lucilia sericata
and Megaselia scalaris. Am J Trop Med Hyg 2004; 70: 386-9.
10 Lettau LA. Nosocomial transmission and infection control
aspects of parasitic and ectoparasitic diseases. Part III.
Ectoparasites/summary and conclusions. Infect Control Hosp
Epidemiol 1991; 12: 179-85.
11 Mielke U, Schlote A. Hospital infection resulting
from maggots. Z Arztl Fortbild 1980; 74: 556-8.
12 Jacobson JA, Kolts RL, Conti M, et al.
Hospital-acquired myiasis. Infect Control 1980; 1: 319-20.
13 Greenberg B. Two cases of human myiasis caused by
Phaenicia sericata (Diptera: Calliphoridae) in Chicago area
hospitals. J Med Entomol 1984; 21: 615.
14 Smith DR, Clevenger RR. Nosocomial nasal myiasis.
Arch Pathol Lab Med 1986; 110: 439-40.
15 Burgess I, Spraggs PD. Myiasis due to
Parasarcophaga argyrostoma--first recorded case in Britain. Clin
Exp Dermatol 1992; 17: 261-3.
16 Josephson RL, Krajden S. An unusual nosocomial
infection: nasotracheal myiasis. J Otolaryngol 1993; 22: 46-7.
17 Bayer HG. Myiasis maligna of nose and ears in Ceylon;
recommendation of a new treatment. AMA Arch Otolaryngol 1954; 59:
104-7.
18 Brauneck H. Über maligne Fliegenmadeninfektion (Myiasis)
des Ohres. Z Laryngol Rhinol Otol 1953; 32: 333-4.
19 Braverman I, Dano I, Saah D, et al. Aural
myiasis caused by flesh fly larva, Sarcophaga haemorrhoidalis. J
Otolaryngol 1994; 23: 204-5.
20 Chung PR, Jung Y, Kim KS, et al. A human
case of internal myiasis in Korea. Korean J Parasitol 1996; 34:
151-4.
21 Carvalho RW, Santos TS, Antunes AA,
et al. Oral and maxillofacial myiasis associated with
epidermoid carcinoma: a case report. J Oral Sci 2008; 50: 103-5;
(Erratum in: J Oral Sci 2008; 50(2): following 237. Filho, José RL
[corrected to Laureano Filho, José R]).
22 Joo CY, Kim JB. Nosocomial submandibular infections
with dipterous fly larvae. Korean J Parasitol 2001; 39: 255-60.
23 Anegg B, Auer H, Diem E, et al. Wound
myiasis. Facultative myiasis. Hautarzt 1990; 41: 461-3.
24 Phillips WG, Marsden JR. Opportunistic cutaneous
myiasis following radiotherapy for squamous cell carcinoma of the
left temple. Br J Dermatol 1993; 129: 502-3.
25 Rubio C, Ladrón de Guevara C, Martín MA,
et al. Cutaneous myiasis over tumor-lesions: presentation of
three cases. Actas Dermosifiliogr 2006; 97: 39-42.
26 Arbit E, Varon RE, Brem SS. Myiatic scalp and
skull infection with diptera sarcophaga: case report. Neurosurgery
1986; 18: 361-2.
27 Agarwal DC, Singh B. Orbital myiasis--a case
report. Indian J Ophthalmol 1990; 38: 187-8.
28 Bosniak SL, Schiller JD. Ophthalmomyiasis in an
eyelid reconstruction. Am J Ophthalmol 1990; 109: 101-2.
29 Novelli MR, Haddock A, Eveson JW. Orofacial
myiasis. Br J Oral Maxillofac Surg 1993; 31: 36-7.
30 Radmanesh M, Khataminia G, Eliasi P,
et al. Chrysomyia bezziana-infested basal cell carcinoma
destroying the eye. Int J Dermatol 2000; 39: 455-7.
31 Caça I, Unlü K, Cakmak SS, et al. Orbital
myiasis: case report. Jpn J Ophthalmol 2003; 47: 412-4.
32 Kokcam I, Saki CE. A case of cutaneous myiasis
caused by Wohlfahrtia magnifica. J Dermatol 2005; 32: 459-63.
33 Hawayek LH, Mutasim DF. Myiasis in a giant squamous
cell carcinoma. J Am Acad Dermatol 2006; 54: 740-1.
34 De Souza A, Clancy P. Facial skin myiasis
associated with advanced skin cancer: failure of early detection.
Skinmed 2006; 5: 48-9.
35 Bouwman LH, Stigter DA, van Baalen JM.
Invasive basal cell carcinoma causing skull and dura destruction.
Dermatol Surg 2007; 33: 980-1.
36 Cheshier SH, Bababeygy SR, Higgins D,
et al. Cerebral myiasis associated with angiosarcoma of the
scalp: case report. Neurosurgery 2007; 61: E167; (discussion
E167).
37 Gabriel JG, Marinho SA, Verli FD, et al.
Extensive myiasis infestation over a squamous cell carcinoma in the
face. Case report. Med Oral Patol Oral Cir Bucal 2008; 13:
E9-E11.
38 Guerrini VH. Ammonia toxicity and alkalosis in sheep
infested by Lucilia cuprina larvae. Int J Parasitol 1988; 18:
79-81.
39 Caballero M, Hernández G, Poudevigne F,
et al. Isolation and identification of bacteria associated
with the screwworm fly Cochliomyia hominivorax, coquerel and its
myiasis. Ann N Y Acad Sci 1996; 791: 248-54.
40 Tóth EM, Hell E, Kovács G, et al.
Bacteria isolated from the different developmental stages and
larval organs of the obligate parasitic fly, Wohlfahrtia magnifica
(Diptera: Sarcophagidae). Microb Ecol 2006; 51: 13-21.
41 Osorio J, Moncada L, Molano A, et al.
Role of ivermectin in the treatment of severe orbital myiasis due
to Cochliomyia hominivorax. Clin Infect Dis 2006; 43: e57-e59.
42 Sherman RA. Wound myiasis in urban and suburban United
States. Arch Intern Med 2000; 160: 2004-14.
43 Lukin LG. Human cutaneous myiasis in Brisbane: a
prospective Study. Med J Aust 1989; 150: 237-40.
|
Printable version
Version PDF
