Case Report: Re-Emergence of Cochliomyia hominivorax in Costa Rica: Report of a Human Myiasis Case 23 Years after Elimination

ABSTRACT.

The New World screwworm, Cochliomyia hominivorax Coquerel (Diptera: Calliphoridae), was officially eliminated from Costa Rica in 2000, but it was reintroduced in 2023. A myiasis by C. hominivorax in a 71-year-old man with a 4-month history of foot hyperkeratosis and interdigital ulcers is reported. The myiasis was detected before sampling for bacterial culture. Approximately 160 first- and second-instar larvae were recovered and identified as C. hominivorax. Morphological identification was based mainly on characteristics of the cephalopharyngeal skeleton, spiracles, and pigmented dorsal tracheal trunks. Sequencing of a cytochrome c oxidase subunit I gene fragment confirmed the identity. The ulcers healed after extraction of the larvae and ciprofloxacin treatment of a concurrent Staphylococcus aureus and Pseudomonas aeruginosa infection. Given the reintroduction of C. hominivorax in Costa Rica and the risk of northward expansion, this report highlights its impact on public health and calls for awareness among clinicians and healthcare practitioners.

INTRODUCTION

Myiasis is the infestation of organs and tissues in humans and vertebrate animals caused by fly larvae that feed on living or necrotic tissues. Larvae of some fly species are obligate parasites, as is the case of Cochliomyia hominivorax, in which larval development occurs exclusively in tissues of a living host.¹ Because of its impact on the economy and public health of both humans and animals, significant efforts have been made to control C. hominivorax, and elimination was successful in North and Central America.²

In Costa Rica, the Screwworm Eradication Program released approximately 60 million sterile flies per week from 1996 to 1999. The last case of screwworm myiasis at the time was reported in June 1999, and the country was officially certified as free of C. hominivorax in 2000.² After 23 years without screwworm outbreaks in Costa Rica, a case in a dog was reported on July 14, 2023 in the canton of Corredores, Puntarenas province, near the border with Panama. By June 5, a total of 2,014 cases had been reported throughout the country, predominantly in cattle, but also in dogs, goats, horses, cats, sheep, pigs, birds, and humans.³ Before its elimination, human cases of screwworm myiasis were reported frequently in the country.^4–7 In this report, we describe a case of myiasis by C. hominivorax, which, to the authors’ knowledge, was the first infestation to be observed in a human after the recent reintroduction of this species in Costa Rica.

CASE REPORT

On January 12, 2024, a 71-year-old male patient presented at the clinical laboratory of Hospital Juana Pirola (San Vito district of Coto Brus canton, Puntarenas province, Costa Rica) for bacterial and fungal culture. The patient had a history of hypertension, dyslipidemia, and cerebrovascular accident but no diabetes or any other significant comorbidities on record. The patient confirmed that he resided in a small rural settlement of Coto Brus (8.908652, –82.903399; elevation: 940 m), close to the geographic limit with Panama in the Talamanca mountain range. This location is surrounded by cloudy forest patches and farms dedicated to agriculture; the average temperature recorded from January 1 to 12, 2024 was 20.8°C, with a total precipitation of 5.6 mm, and an average humidity of 83.5% (data provided by the National Meteorological Institute of Costa Rica). The patient reported the presence of painful, purulent, and foul-smelling hyperkeratotic lesions in the interdigital area of both feet, with a 4-month evolution, which had not improved with topical aluminum acetate (powder) and 1% bifonazole cream, nor with oral trimethoprim-sulfamethoxazole or amoxicillin (Figure 1A). A deep lesion with numerous fly larvae was observed between the first and second toes of the right foot (Figure 1B; Supplemental Video 1). Approximately 160 first- and second-instar larvae were mechanically extracted; two were killed by immersion in hot water for 30 seconds for further microscopic observation, and the rest were directly preserved in 10% formaldehyde or 70% ethanol. Samples for bacterial and fungal cultures were taken from the lesions, with a subsequent positive result for Staphylococcus aureus and Pseudomonas aeruginosa isolates (reported 2 days later), both of which showed in vitro susceptibility to ciprofloxacin. The fungal culture was negative. After sample collection, the patient was taken to the emergency department for wound care, where a few more larvae were extracted. Oral ciprofloxacin (500 mg every 12 hours for 7 days) was prescribed, as well as topical twice daily treatments with 1% bifonazole cream and 1% silver sulfadiazine cream. Signs of improvement were noticed after 4 days, and the wounds on both feet had healed upon a follow-up visit 6 weeks later (Figure 1C).

Figure 1.

Clinical presentation of the affected feet. (A) Foot condition upon arrival at the hospital, showing hyperkeratosis and ulcers. (B) Site of the myiasis (arrow). (C) Foot condition 6 weeks after treatment.

The initial microscopic observation of larval characters, combined with the numerous larvae in the lesion and recent reports of screwworm myiases in animals from the area, raised suspicion of this myiasis being linked to C. hominivorax.⁸ As these were only first and second-instar larvae, and there had not been any reported screwworm myiasis cases in humans in Costa Rica for more than 2 decades, the preserved larvae were transported to the Medical Entomology Laboratory of the School of Microbiology, University of Costa Rica, for further analysis. All larvae were observed under a dissecting microscope to confirm that they were morphologically identical to each other. Six second-instar larvae were selected (based on slight variations in size, body transparency, and extent of tracheal trunk pigmentation), cleared in lactophenol, and mounted using Hoyer’s medium for microscopic observation. In all cases, larval morphology was compatible with C. hominivorax, according to characters that have been described previously for this instar (Figure 2): posterior spiracles with two straight respiratory slits, incomplete peritremes, and undifferentiated buttons; a band of dark spines that completely encircles the anterior portion of segments 2–10 but is dorsally incomplete in segment 11; and the distal pigmentation of the dorsal tracheal trunks extends to at least half of terminal segment 12.^9,10 In addition, the anterior spiracles of the second-instar larvae analyzed in this case had 9–11 openings each.

Figure 2.

Morphological characteristics of second-instar Cochliomyia hominivorax larvae. (A) Whole larva. (B) Cephalopharyngeal skeleton. (C) Posterior spiracles and pigmented tracheal trunks. (D) Anterior spiracle with 11 openings.

To support morphological identification of the larvae and completely exclude the possibility of other known Chrysomyinae species that may seem similar at the second-instar larval stage,^10,11 genomic DNA was extracted from a pool of five larvae using the NucleoSpin Tissue Kit (Macherey-Nagel). Subsequently, a 710 bp fragment of the cytochrome c oxidase subunit I (MT-CO1) gene was amplified by end-point polymerase chain reaction (PCR) using the LCO1490 and HCO2198 primers, as previously described.¹² The PCR product was purified with an enzymatic EXO/FastAP mixture (ThermoFisher Scientific) and sent to Macrogen Inc. (South Korea) for Sanger sequencing. The resulting sequence showed 100% homology with available MT-CO1 C. hominivorax reference sequences, such as GenBank accession number HM185574. Voucher specimens of the larvae were deposited in the University of Costa Rica’s Medical Entomology Collection, and the MT-CO1 sequence was deposited in GenBank with accession number PP713099.

To comply with all requirements for the publication of this case report, the patient provided a signed informed consent form, and approval was granted from the Center for Strategic Development and Information on Health and Social Security of the Costa Rican Social Security Fund, which is the public healthcare provider in Costa Rica.

DISCUSSION

To the authors’ knowledge, this case marks the return of human myiasis due to C. hominovorax in Costa Rica, more than 20 years after it had been eliminated from the country. On February 26, 2024, the Ministry of Health and the National Animal Health Service (SENASA) of Costa Rica publicly announced the first official report of a human screwworm myiasis case in the country, in which third-instar larvae were confirmed in a patient from the Pavón district of the Golfito canton, Puntarenas province.¹³ However, the myiasis described in the present case was detected more than 1 month before this (January 12), but the official species report to the local authorities was delayed due to the confirmation process.

New World screwworm myiases can occur in different warm-blooded animals and begin when female flies oviposit on or near open wounds or moist body openings.¹⁴ In this case report, purulent and foul-smelling hyperkeratotic lesions were present, which were coinfected with bacteria and had been present for several months. Dermatological conditions such as ulcers and hyperkeratosis have been identified as important predisposing factors for this type of myiasis.^15,16 Moreover, previous studies have reported that female C. hominivorax can be attracted to foul-smelling wounds, such as foot ulcers and those infected with bacteria, including P. aeruginosa.^17,18 In this patient, the wound-healing process was effective only after the correct antibiotic treatment was given, which highlights the importance of wound care and treatment to prevent possible recurrent screwworm infestations in endemic areas. Additional protective actions against myiases in humans include covering wounds, wearing appropriate clothing, and enhancing overall sanitation and personal hygiene.¹⁹

To identify fly species associated with myiasis, the observation of third-instar larvae is preferred due to their size and the availability of detailed descriptions and identification keys^10,20; however, descriptions of first and second-instar larvae of several species are also available.^9,21 In the present case, only second-instar larvae were used for morphological identification, and they showed expected character variations compared with third-instar larvae, such as two slits in each posterior spiracle and a shorter pigmented section of the dorsal tracheal trunks.^9,10 The only inconsistent characteristic in this case was that the anterior spiracles had nine to 11 openings, compared with the seven to nine openings that are commonly reported for second- and third-instar larvae of this species.^8,9,22 These phenotypic variations should be considered when identifying early-stage larvae, even though molecular identification can be useful when in doubt.^11,23 All other morphological and molecular characteristics were consistent with C. hominivorax.

Before its elimination from North and Central America, the New World screwworm distribution included warm temperate zones of the Southern United States and tropical areas of Central America, South America, and the Caribbean.^2,14 In this case report, the mean temperature where the patient lived (20.8°C) was slightly lower than the optimal temperature reported for egg production in laboratory studies with C. hominivorax (from 21.8°C to 37.8°C), although it was in the range of adult survival (12.3–47.2°C).²⁴ Therefore, the presence of C. hominivorax in this area confirms the adaptability of the fly to inhabit cool and dry areas within the tropics.

Currently in Costa Rica, the National Animal Health Service (SENASA) is conducting a series of actions aimed at controlling and preventing the northward spread of C. hominivorax, which includes intensifying passive surveillance by promoting the reporting and follow-up of all suspected cases, monitoring the extent and distribution of the fly, controlling the movement of all animals from the affected areas to prevent animals with wounds or myiasis from leaving the area, and implementing control checkpoints with police presence 24 hours a day.³ Considering the risk of re-emergence of New World screwworm in the rest of Central America and North America, measures for prevention, diagnosis, and general awareness of possible cases in both humans and animals are necessary.

Note: Supplemental materials appear at www.ajtmh.org.