ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

Neotropical Helminthology, 2018, 12(2), jul-dic:233-242.

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

CUTANEOUS MYIASIS BY COCHLIOMYIA HOMINIVORAX COQUEREL, 1858 (DIPTERA:

CALLIPHORIDAE) ASSOCIATED WITH ORAL NEOPLASIA, IN GERIATRIC PATIENT

MIIASIS CUTÁNEA POR COCHLIOMYIA HOMINIVORAX COQUEREL, 1858 (DIPTERA:

CALLIPHORIDAE) ASOCIADA CON NEOPLASIA ORAL, EN PACIENTE GERIÁTRICO

1 Control Laboratory of Arthropods and Vectors. National University of San Marcos Faculty of Biological Sciences

2 Laboratory of Human and Animal Parasitology. National University of San Marcos. Faculty of Biological Sciences

3 Private medical center

*Corresponding author: E-mail: jch4920@hotmail.com

1 1 2 3

Julia Castro-Hidalgo ; Nelly Milla Nuñez ; Asucena Naupay Igreda & Javier Zegarra Velit

ABSTRACT

Key words: Cochliomyia hominivorax – cutaneous myiasis – oral neoplasia – Peru – third larvae stage

We report a case of a specific cutaneous human myiasis, associated to oral neoplasia. The presentation of

this case corresponds to a 78 years old adult male patient coming from Chorrillos district, Lima, Peru who

at the time of being treated at a medical center, presented an open ulcerative wound in the lower right

maxillary in which larvae of flies of different stages were observed. Biological material extracted from the

wound was identified as Cochliomyia hominivorax (Coquerel, 1858) (Diptera: Calliphoridae), by the

morphological characteristics of third instar larvae through the optical and scanning electron microscopy.

In this case, the presence of C. hominivorax was favoured by the oral lesion of the patient who attracted

flies to lay their eggs on the edge of the lesion.

Neotropical Helminthology

233

Volume12,Number2(jul-dec2018)

ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)

Lima-Perú

VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043

RESUMEN

Palabras clave: Cochliomyia hominivora – larvas de tercer estadio – miasis cutánea –neoplasia oral

Se registra un caso de miasis cutánea específica, asociada a neoplasia bucal. La presentación del caso

corresponde a un paciente geriátrico de sexo masculino, de 78 años de edad, procedente del distrito de

Chorrillos, Lima, Perú que al momento de ser atendido en la clínica, presentaba una herida ulcerosa

abierta, en el maxilar inferior derecho en la que se observó gran cantidad de larvas de diferentes estadios.

El material biológico extraído de la herida del paciente fue identificado como Cochliomyia hominivorax

(Coquerel, 1858) (Diptera: Calliphoridae), por las características morfológicas de la larva de tercer

estadio a través de la microscopia óptica y electrónica de barrido. En este caso clínico, la presencia de C.

hominivorax se vio favorecida por la lesión bucal del paciente que permitió atraer a las moscas para que

coloquen sus huevos en el borde de la lesión.

Myiasis is a zoonotic infestation that affects the

live or necrotic tissues of human and other

vertebrate animals and is caused by different larval

stages of flies, which during a certain period feed

on live or dead tissues or body fluids from the

natural cavities of the host, or by the intake of

contaminated food. Myiasis are called

"gusaneras", "bicheras", "coqueras" and are

produced by species of flies of the Order Diptera:

Suborder Brachycera (Acha & Szyfres, 2003;

Carles-Tolrá, 2015). The necrobiontofagas larvae

invade wounds or lesions, body regions with

purulent discharges such as nose, ears or genitals,

reaching up to the living tissues. These flies are part

of the cadaveric fauna. Worldwide there are

330,570 million people at risk of being affected by

this parasitism (Botero & Restrepo, 2012). In

humans, the infestation is accidental and the risk

groups are immunocompromised people,

indigents, elderly people and animal breeding staff.

The main risk factors are open wounds, exposure of

ulcers, hemorrhoids, bacterial infection of wounds

or natural cavity, sleeping outdoors, poor hygiene,

not wearing footwear, eating contaminated food.

Myiasis are rapidly evolving, very aggressive and

with tissue destruction and the main locations

occur in the skin, mouth, eyes, breasts, intestinal

tract and genitourinary (Coronel et al., 2016).

Myiasis are classified according to the type of

tissue they invade, by the organ they affect

(foruncular, cutaneous, cavitary, and intestinal), by

the type of invasive process (obligatory, facultative

and accidental) and by the clinical forms that have

been found in man. Cutaneous myiasis have two

clinical forms according to the invaded tissue:

forunculosa caused by Dermatobia hominis

(Linnaeus, 1781), and ulcers such as those caused

by Cochliomyia hominivorax (Coquerel, 1858),

Sarcophaga haemorrhoidalis (Fallén, 1817) and

Hypoderma bovis (Linnaeus, 1758) (Páez & Villa,

2017).

Cochliomyia hominivorax known as "screw

worm", is a diptera of the Family: Calliphoridae,

which seriously affects livestock and especially

cattle. The distribution of the screw worm is

conditioned to the climatic changes, the low

temperatures prevent them from surviving, or,

234

Neotropical Helminthology, 2018, 12(2), jul-dic

INTRODUCTION

MATERIAL AND METHODS

because the animal population is insufficient to

maintain the biological cycle (Graham, 1985;

Villarreal et al., 1993).

The females are attracted by wounds or secretions

where they lay their eggs at the edges of the

wounds, in the injured mucous membranes that are

associated with the natural openings of the body

such as the sinuses, eye sockets, mouth, ears and

vagina. They deposit an average of 200 eggs

(between 10 and 490) in a characteristic flat, roof-

shaped mass (Becerril, 2014).

Larvae of C. hominivorax cause facultative or

semi-specific myiasis, have occasional parasite life

and invade lesions or purulent body regions. The

larvae hatch before 24 h after oviposition and begin

to feed on tissue fluids, with the head facing down

and penetrating the hole in the wound, causing

massive tissue destruction. The larvae reach

maturity between 4 and 8 days after hatching and

leave the wound, fall to the ground, bury

themselves and initiate pupation. The period of life

under normal conditions from egg to adult is 3 to 4

weeks. The wounds tend to attract other flies which

also deposit their eggs aggravating myiasis in this

way (Francesconi & Lupi, 2012). The objective of

the present work was to describe the case of

cutaneous myiasis of a geriatric patient, with an

advanced stage of oral carcinoma, through the

taxonomic identification of the third stage larvae

extracted from the lesion.

Male patient, 78 years old, retired, native of

Germany, peruvian resident for 40 years, of

protestant religion, coming from La Encantada de

Villa urbanization, district of Chorrillos in Lima,

Peru. The patient enters the emergency of the

medical center having a history of malignant

neoplasm of the mouth and having received

chemotherapy treatment.

The patient was transferred from another local

clinic, with a nasogastric tube and when he was

received in the clinic, he had 10 g hemoglobin,

3,300,000 cc red blood cells and 9,950 mm 3

Castro-Hidalgo

button, incomplete perithema of dark

pigmentation, with strongly pigmented tracheal

trunks. Through the morphological characteristics

of L larvae, C. hominivorax was identified, using

the taxonomic keys of Dale (1985), Gómez et al.

(2008) and Florez & Wolff (2009) (Fig. 4).

To corroborate our diagnosis the L were processed

by scanning electron microscopy, using the critical

point desiccator brand Electron Microscopy

Sciences Model: EMS850 and the gold metalizer

brand: SPI supplies. The microscopic scanning

observation revealed the same characteristics

found with optical microscopy (Fig.5)

Myiasis caused by C. hominivorax is a zoonotic

parasitism recognized by the International Office

of Epizootics (OIE), and its notification is

obligatory. In animals, the main risk factor is open

wounds that can occur due to natural causes or

caused by man due to practices during the cattle

exploitation, and another factor are the natural

openings of the host. (Forero et al., 2007). This

infestation in humans is almost always accidental

and can be caused by opportunistic dipterous.

Parasitism depends on environmental factors such

as the presence of gravid flies, season and area of

residence. There are also the risk factors that the

host provides such as the poor hygiene condition;

inadequate treatment of wounds and ulcers;

exposed and suppurative lesions that are attractive

for the oviposition of flies. Another factor is the

patient's condition (age, physical limitation,

alcoholism, drug addiction, chemotherapy

treatment) and / or patient's health status, as well as

the presence of comorbidities (cancer, diabetes and

tuberculosis) (Reinoso & Alemán, 2016).

Patients with neoplasms in cavities, with open

wounds and skin diseases offer the possibility of

other infections such as cutaneous myiasis.

Visciarelli et al. (2003) observed in a 36 years old

patient with pediculosis, wounds on the scalp that

were superinfected with larvae of C. hominivorax.

The patient was a field worker and had neglect of

his personal hygiene, malnutrition and a head

leukocytes. A tumor and lesion were observed in

the right maxilla region, irregularly shaped, 5 cm

long, 3 cm in diameter and 2.5 cm deep; of net

edges, bleeding bed and multiple tunnels at the

base of the wound (Fig.1). In addition, the patient

showed perforated deep ulcers, which

communicated with the oral region, with the

presence of necrotic tissue, bloody exudate and

foul odor, from which 28 larvae of different size

emerged.

We proceeded to the extraction and separation of

the larvae by stages and they were fixed in 70%

ethyl alcohol for later taxonomic identification

(Fig. 2).

Identification of larval forms

The identification of the species was performed on

larvae that were at the beginning of the third stage

(L ) because they were the most robust, 15-16 mm

long, creamy white with reduction in thickness

from the cephalic segment to the sixth segment and

then decreasing towards the posterior end.

The L were heavily armed with large spines of 1 to

3 points, often 1 or 2 spines on its cuticle visible to

nd th

the naked eye. From the 2 to the 9 segment they

were observed surrounded with a band of thorns

organized in irregular rows, being longer than the

th th

previous rows and in the 7 and 9 segments they

presented thorns in the posterior margins, reduced

to one or two rows and confined to the ventral

surfaces.

The 10 segment with an anterior band of spines

somewhat reduced and usually interrupted on the

back, with ventral and ventrolateral spines a little

scattered laterally and dorsally. The 11 segment

with an incomplete anterior band and smaller

spines; and in the posterior margin a band of 2 or 3

rows of anterior curved spines were observed. The

12 segment presents restricted spines to the

ventral and ventrolateral surfaces. The

cephalopharyngeal apparatus with dorsal arms

longer than the ventral ones (Fig. 3).

The anterior spiracles of L are small fan-shaped

with finger-like extensions located near the base of

the second segment, usually with 6 to 11 papillae

each. To observe the posterior spiracles, the 12

segment was cut and the vertical spiracular plates

were observed, those that showed imperceptible

235

Neotropical Helminthology, 2018, 12(2), jul-dic

RESULTS AND DISCUSSION

Cutaneous myiasis by Cochliomyia hominivorax

Myiasis is the infestation of living vertebrates by

fly larvae that feed for at least part of their

development on the host's dead or living tissues,

body substances, or ingested food The occurrences

of traumatic myiasis in humans and animals in

urban and rural environments represent serious

economic and public health concerns (Zumpt,

1965).

Batista da Silva et al. (2011), reported a 49-year-

ol d tracheos to mized man u nd ergoing

chemotherapy treatment who was parasitized in the

hospital in São Gonçalo, Rio de Janeiro, Brazil, by

larvae of the screwworm, C. hominivorax in the

thoracic cavity.

In Tucumán (Argentina), Olea et al. (2014), was

reported the first case of cutaneous myiasis in a

patient diagnosed with type II diabetes, with ten

years of evolution and with neuropathy. The 54-

year-old male patient presented with an ulcer

approximately 4 cm in diameter in the right foot

from which 5 larvae were extracted. Third instar

larvae were identified as C. hominivorax and adults

emerged at 12 days confirming the diagnosis

injury with a serosanguineous secretion.

In children with pyodermatis on the scalp, larvae of

flies have also been extracted and by the stench

presented by the wounds, they were identified as C.

hominivorax (Miranda, 2007). Post-scratching

lesions in a 3 years old patient with chickenpox

were also superinfected with C. hominivorax

larvae (Heizenreder et al., 2009).

In prostrate patients, they also show some

susceptibility to acquire this type of opportunistic

infections, thus a case of myiasis in the oral cavity

is reported by C. hominivorax in a patient prostrate

due to Parkinson's disease, from Huacho (Lima,

Peru) (Espinoza et al., 2009).

Trombetta et al. (2009), reported a case of

cutaneous myiasis in a 32-year-old man with a

history of alcoholism and drug addiction, which

had a head wound with severe bacterial infection.

71 larvae were extracted from the wound which

were identified as C. hominivorax. This infestation

is almost always accidental in humans and in this

case was favored by the condition of the patient.

236

Figure 1. Patient with lesion in the region of the right maxilla where larvae of C. hominivorax was observed.

Neotropical Helminthology, 2018, 12(2), jul-dic Castro-Hidalgo

Cochliomyia hominivorax. Patients with D.

hominis presented skin lesions and abscesses while

cases with C. hominivorax had a history of

tuberculosis or cancer of the larynx or breast

(Failoc-Rojas et al., 2018).

In the present clinical case, the patient had received

chemotherapy treatment for presenting oral

neoplasia, and lesions of the mouth, buccal mucosa

and cheek were infected with larvae of C.

hominivorax, being this the first time were the

association cutaneous myiasis- oral neoplasia is

mentioned in literature. The importance of a quick

diagnosis is highlighted by the aggressiveness of

the biontophage larvae that are capable of

destroying even bone tissue (Pérez-Caballero et

al., 2012).

The role of C. hominivorax as a producer of

specific human miasis, favored by the patient's

condition, is highlighted (Calderón et al., 1995;

Maguiña-Vargas et al., 2005; Mengarelli &

Cevallos 2012; Domínguez et al., 2016).

Cutaneous myiasis are the most frequent in rural

environments, however in the case that occurs,

occurred in urban environment.

Ethical responsibility

The authors declare that no human experiments

have been carried out for this investigation.

through their morphological characteristics.

A case of oral myiasis caused by C. hominivorax

was reported in a person with neuropsychomotor

limitation who presented lesions in the maxilla and

mandible. They extracted 45 maggots from the

lesions and 75 when general anesthesia and

nasotracheal intubation were applied to the patient.

This study recommends dentists who must

recognize parasites that affect the oral cavity

(Pereira et al., 2015). Reinoso & Alemán (2016),

report the first case of maxillary myiasis in Cuenca

(Ecuador), in a 24-year-old patient with prolonged

mouth opening, spastic paralysis and muscular

rigidity in all four extremities. Third instar larvae of

C. hominivorax were extracted from the gingival

mucosa and the tear orifice. By surgical

debridement they found larval tunnels in the upper

labial frenum and in the palate presenting great

bloody flow.

A retrospective study was conducted in

Lambayeque (Peru), of the cases diagnosed of

myiasis in two hospitals from January 2012 to

December 2015, which were compiled from the

clinical files. They chose the cases in which larval

development was observed and a clinical profile

compatible with myiasis. There were 9 cases of

myiasis, of which two were pediatric patients, one

adult and six elderly. Four of the nine patients were

male. The identified species were D. hominis and

237

Figure 2. Cochliomya hominivorax third stage larvae extracted from the patient's injury.

Neotropical Helminthology, 2018, 12(2), jul-dic Cutaneous myiasis by Cochliomyia hominivorax

238

A. Optical microscopy

B.Electron microscopy

Figure 3. Anterior end of the L of Cochliomyia hominivorax showing the detail of the hooks of the cephalopharyngeal skeleton.

Neotropical Helminthology, 2018, 12(2), jul-dic Castro-Hidalgo

239

A. Optical microscopy

B. Electron microscopy

Figure 4. Larva of third stage of Cochliomyia hominivorax showing the cuticular spines of one and two points.

Neotropical Helminthology, 2018, 12(2), jul-dic Cutaneous myiasis by Cochliomyia hominivorax

Figure 5. Posterior spiracular plates of the third instar larva of Cochliomyia hominivorax showing characteristic respiratory

stigmas and perithema.

Acha, P & Szyfres, B. 2003. Zoonosis y

enfermedades transmisibles comunes al

hombre y a los animales. 3ª ed. Washington

DC: Organización Panamericana de la

Salud. Vol III. Parasitosis. pp. 355-368.

Publicación Científica y Técnica Nº 580.

Wa s h i n g t o n , D C 2 0 0 3 7 , E U A .

BIBLIOGRAPHIC REFERENCES

Organización Panamericana de la Salud.

Batista da Silva, J, Borja, G & Queiroz, M. 2011.

Patient with tracheostomy parasitized in

Hospital by larvae of the screwworm,

Cochliomyia hominivorax. Journal of

Insect Science, vol.11 pp.163.

Botero, D & Restrepo, M. 2012. Parasitosis

Humanas. 5 ed. Ed. CIB Corporación para

Investigaciones Biológicas. Medellín. 575-

675 pp.

Becerril, MA. 2014. Parasitología Médica.

Capítulo 37: Artrópodos de importancia

médica. 4ª edición Editorial McGrawn-

Hill. México. pp. 283-305.

Calderón, O, Sánchez, C & Sandi, J. 1995. Miasis

oral por Cochlyomyia hominivorax

(Diptera: Calliphoridae) en una paciente

geriátrica. Revista Costarricense de

Ciencias Médicas, vol. 16: 61-66.

Carles-Tolrá, M. 2015. Manual de la Clase

Insecta: Orden Diptera. Revista de la

Sources of financing: Control Laboratory of

Arthropods and Vectors. National University of

San Marcos. Faculty of Biological Sciences. Lima-

Perú.

ACKNOWLEDGMENT

Neotropical Helminthology, 2018, 12(2), jul-dic Castro-Hidalgo

240

para la erradicación del gusano barrenador

del ganado. pp. 1-71.

Heizenreder, B, Fernández, R & Kulinka, L. 2009.

Un caso de miasis h u m a n a p o r

Cochliomyia hominivorax (Díptera:

Calliphoridae) asociado a varicela en Villa

Angela, provincia del Chaco, Argentina.

Revista de Posgrado de la Cátedra de

Medicina, vol. 192. pp.14- 16.

Maguiña-Vargas, C, Osores, F, Farías, H, Torrejón,

D & Alcorta, T. 2005. Enfermedades por

e c t o p a r á s i t o s : s e g u n d a p a r t e .

Dermatología Peruana, vol.15, pp. 38-50.

Mengarelli, R & Cevallos, M. 2012. Manejo de las

miasis en heridas agudas y crónicas.

Presentación de casos y revisión de la

bibliografía. Revista Argentina de

D e r m a t o l o g í a , v o l . 9 3 , I n :

http://www.scielo.org.ar/scielo.php

Miranda, H. 2007. Miasis en Trujillo, Perú:

observaciones clínicas y entomológicas.

Folia Dermatológica, vol.18 pp.13-17.

Olea, M, Centeno, N, Veggiani, C, Ortega, E,

Begoña, G, Olea, L & Dantur, J. 2014. First

report of myiasis caused by Cochliomyia

hominivorax (Diptera: Calliphoridae) in a

diabetic food ulcer patient in Argentina.

Korean Journal of Parasitology, vol.52 pp.

89-92.

Páez, R & Villa, L. 2017. Identificación de larvas

productoras de miasis obtenidas del

cepario de la Universidad Colegio Mayor

de Cundinamarca con importancia en salud

pública. Revista NOVA Publicación

Científica en Ciencias Biomédicas, vol.15,

pp. 79-91.

Pérez-Caballero, A, Garduño-Eseverri, E, Nicolás-

Olivera, R & Pérez-Bote, L. 2012. Lesión

cutánea de etiología poco frecuente.

Enfermedades Infecciosas y Microbiología

Clínica, vol.30, pp. 346–347.

Pereira, J, Sant'Ana dos Santos, F, Farias, A,

Salimon, F, Ferreira, F & Tadeu, A. 2015.

Oral myasis caused by Cochliomyia

hominivorax in a disabled person. Case

Reports in Pathology, vol. 2015, pp.1-3.

Reinoso, Q.S. & Aleman, I.J. 2016. Rara miasis

maxilar por Cochliomyia hominivorax.

Reporte de caso, actualidad y entomología.

Revista Española de Cirugía Oral y

M a x i l o f a c i a l , v o l . 3 8 , p p . 1 1 1 -

116.Seminario, M & Colán, E. 1990.

Sociedad Entomológica Aragonesa, vol. 63,

pp. 1–22.

Coronel, A, Sacta, B & Crespo, C. 2016. Caso

clínico: Miasis traumática. Revista Médica

del Hospital Jose Carrasco Arteaga (HJCA)

Cuenca-Ecuador, vol. 8, pp. 82-85.

Dale, W. 1985. Identidad de las moscas

Calliphoridae en la Costa Central de Perú.

Revista Peruana de Entomología, vol. 28,

pp. 63-70.

Domínguez, J, Cueva, J, Cusco, C, Rodríguez-

Hidalgo, R & Calvopiña, M. 2016. Miasis

orbitaria severa causada por Cochliomyia

hominivorax en la región andina de

E c u a d o r. R e v i s t a Me x i c a n a de

Oftalmología, vol. 90 pp. 43-47.

Espinoza, A, Quiñones-Silva, J & Garay, O. 2009.

Miasis en cavidad oral por Cochliomyia

hominivorax. Reporte de un caso. Revista

Peruana de Medicina Experimental y Salud

Pública. vol. 26, pp.573-576.

Failoc-Rojas, VE, Molina-Ayasta, Salazar-

Zuloeta, J, Samamé, A & Silva-Díaz, H.

2018. Case Report: Myiasis due to

Cochliomyia hominivorax and Dermatobia

hominis: clinical and pathological

differences between two species in Northern

Peru. American Journal of Tropical

Medicine and Hygiene, vol. 98 pp.150-153.

Florez, E & Wolff, M. 2009. Descripción y clave de

los estadios inmaduros de las principales

especies de Calliphoridae (Diptera) de

importancia forense en Colombia.

Neotropical Entomology, vol. 38, pp. 418-

429.

Forero, E.; Cortés, J. & Villamil, L. 2007. Ecologia

y Epidemiologia del gusano barrenador del

ganado, Cochliomyia hominivorax

(Coquerel, 1858). Revista de Medicina

Veterinaria, vol. 14, pp. 37-49.

Francesconi, F & Lupi, O. 2012. Myiasis. Clinical

Microbiology Reviews, vol. 25, pp.79-105.

Graham, O.H. 1985. Symposium erradication of

the screwworm from the United States and

Mexico. Miscellaneous. Publications of the

Entomological Society of Americana 62 pp.

Gomez, M, Alvarez, A & Bonilla, J. 2008. Manual

de identificación de gusano barrenador del

ganado Cochliomyia hominivorax

(Coquerel) Diptera: Calliphoridae y su

diferenciación de otras especies causantes

de miasis. Comisión México americana

241

Neotropical Helminthology, 2018, 12(2), jul-dic Cutaneous myiasis by Cochliomyia hominivorax

humana por Cochlyomyia hominivorax

(Diptera: Calliphoridae) asociado a

pediculosis en Mendoza, Argentina.

Parasitologia Latinoamericana, vol. 58,

pp.166-168.

Zumpt, F. 1965. Myiasis in man and animals in the

old world. Butterworths London. United

Kingdon. pp.267.

Dermatobia hominis en carúncula ocular.

Reporte de un caso en Iquitos Perú.

Diagnóstico, vol. 26 pp.95-96.

Trombetta L, Oliva A, Galache V, Bava J &

Troncoso A. 2009. Cutaneous myiasis due

to Cochliomyia hominivorax in a drug user.

Journal of Infection in Developing

Countries, vol. 3, pp. 873-876.

Villarreal, J, Agapito, J, Gutiérrez, J & Lavander, L.

1993. Miasis genital: A propósito de un

caso. Revista de la Sanidad de la Policía

Nacional del Peru, vol. 54. pp.72-75.

Visciarelli, E, García, S, Salomón, C, Jofré, C &

Costamagna, S. 2003. Un caso de miasis

242

Received September 21, 2018.

Accepted December 27, 2018.

Neotropical Helminthology, 2018, 12(2), jul-dic Castro-Hidalgo