Umbilical Myiasis by Cochliomyia hominivorax in an Infant in Colombia
Juan David Ruiz-Zapata1 
Luis Mauricio Figueroa-Gutiérrez1 Jaime Alberto Mesa-Franco1 
Paula Andrea Moreno-Gutierrez2*- 1Faculty of Health Sciences, Universidad Tecnológica de Pereira, Pereira, Colombia
- 2Grupo de Investigación en Biomedicina, Fundación Universitaria Autónoma de las Américas, Pereira, Colombia
Myasis is the infestation by fly larvae (Diptera) in live vertebrates including humans. Myasis has been reported most commonly in tropical and subtropical areas around the world with poor sanitation and presence of cattle. Neonatal umbilical myiasis is an important cause of death in bovines and produces major economic losses in the livestock industry. However, its presentation in humans is rare, with a few cases reported worldwide. Moreover, umbilical myasis can be life-treating due to the risk of larvae migration to deeper tissues of the abdomen, omphalitis, and sepsis. We describe the case of a 7-day-old infant admitted to the hospital due to umbilical cord myiasis. In total, 55 larvae were removed from the wound and identified as Cochliomyia hominivorax. The patient recovered satisfactorily after treatment with ivermectin and amoxicillin. A literature search was performed in Pubmed, Medline, Lilacs and Google Scholar, with 64 cases of myasis by C. hominivorax being reviewed. Oral cavity, wounds, scalp and natural orifices are the main affected anatomical areas. Risk factors include the extremes of age, male sex, poor hygiene, alcohol and drug use, cancer, and mental disability. Programs for human myiasis prevention and surveillance are needed in neotropical areas where living conditions make it difficult to implement control strategies.
Introduction
Myiasis is infestation by fly larvae (Diptera) in live vertebrates, including humans. Fly larvae feed on wound tissue of their host, causing a disease whose severity may depend on the larva species and anatomical sites affected (1, 2). It is widespread in neotropical areas around the world, causing economic and public health problems in low-income populations. Human infection is facilitated by poor hygienic conditions and close contact with wild or domestic animals (2, 3). Umbilical cord myiasis is a common type of wound myiasis in animals but it has been described only rarely in humans (2). We present the first report of neonatal umbilical myiasis in Colombia and review the most relevant aspects of this disease. Recent case reports of myiasis by C. hominivorax are reviewed in the discussion.
Case Report
The research procedures for this case were carried out in accordance with the recommendations of the guidelines of the Helsinki Committee. Written informed consent was obtained from the mother of the newborn for pictures and publication of this case.
A 7-day-old female neonate was taken to a primary health facility in June 2017 because something was coming out of her umbilicus. The patient was born full-term at the local hospital by vaginal delivery from a 17-year-old mother. At birth, the newborn had respiratory depression and mild perinatal asphyxia but without further complications. The umbilical cord was cut following standard care measures for in-hospital delivery. The patient lived on a farm with a cowshed next to the house in the rural area of the municipality of La Virginia (04°54′1.617″ N, 75°52′47.445″ W), in the state of Risaralda, located in the coffee region of Colombia. The mother practiced exclusive breastfeeding and used a fabric girdle, which is traditionally used in Colombia for protection of the umbilical stump during the first days of life.
The neonate was transferred to a tertiary care hospital. On admission, she was visibly irritated and jaundiced. On physical exam, weight was 3,300 g and vital signs (temperature, heart rate, respiratory rate, blood pressure, and blood oxygen levels) were normal. Umbilical stump inspection revealed numerous live larvae (Supplementary Figure 1) and foul-smelling serohaematic secretion. The rest of the examination was normal. Initial blood count showed 20,140 leukocytes/μl (52% neutrophils, 3% eosinophils, 4% lymphocytes, and 5% monocytes). Total serum bilirubin was 18.0 mg/dl (cutoff point to consider phototherapy: 20.5 mg/dl) (4). Wound and blood cultures on admission and 48 h later were negative.
Initial treatment included covering the umbilical stump with gauze soaked in ivermectin and nitrofurazone, followed by a single oral dose of ivermectin (0.15 mg/kg). To prevent late-onset sepsis, intravenous ampicillin (200 mg/kg/day) and gentamicin (4 mg/kg/day) were administered. On the second day, 39 live larvae were removed from the umbilical stump under aseptic conditions using a surgical clamp. One live and 15 dead larvae were extracted on the third day. A follow-up abdominal ultrasonography was normal and the patient was discharged 7 days after admission.
After extraction, seven larvae were preserved in a solution containing 80% alcohol. The specimens were sent to an entomologist and examined using a microscope with 10× magnification. Third instar larvae of C. hominivorax were identified by their smooth appearance with prominent spine bands and one body process in the last segments (Supplementary Figure 2). Pigmented dorsal tracheal trunks were present in two to three of the last segments. The posterior spiracular plates contained three oval-shaped slips pointing to the peritreme (5).
Discussion
Umbilical myiasis is a rare type of wound myiasis in humans, but the occurrence of cases in widely distributed areas shows that this may be a latent risk in all neotropic zones were myiasis has been reported (2). A handful of case reports of umbilical myiasis have been made, mainly in India (3, 6–13). One case was reported in the United States (14) and another in Argentina (15), the latter associated with C. hominivorax. The largest case collection of umbilical myiasis was carried out in Nigeria, where active detection in a region of the Niger Delta resulted in 55 cases of omphalitis (16). Other anatomical sites of myiasis in human neonates include the nostrils (17), ear (18), skin (19), and genitals (20).
The warm and moist environment of the umbilical stump attracts the female flies to lay their eggs on it (11). In our case, the use of an umbilical girdle could have retained moisture around the stump and delayed the separation, creating ideal conditions for larvae growth and also hiding the disease. Umbilical girdles were used traditionally to secure the navel of newborns (21) and remain a common practice in Colombia that goes against current recommendations to keep the stump uncovered to help dry out the base. The girdle also facilitates omphalitis, which in turn increases the size of the wound and creates a proper environment for egg hatching (11). Traditional methods for stump care, such as application of cow dung or herb leaves on the umbilicus of neonates, have been described in previous reports as sources of cross-contamination (16, 22).
Clinical signs of umbilical myiasis are hardly recognized by the caregiver. The disease is usually detected once the larvae are visible or clinical signs of omphalitis appear (11). Imaging and biopsy are rarely necessary for diagnosis but may be useful in umbilical myiasis to determine the extent of the infestation and any organ involvement. Leukocytosis along with neutrophilia and eosinophilia are common clinical findings (2). Hyperbilirubinaemia that resolved after larvae extraction was reported in one case of cutaneous myiasis by Drosophila in a newborn (23), but not in prior cases of neonatal umbilical myiasis.
Neonatal myiasis has been consistently attributed to conditions related to low socioeconomic status, such as poor hygiene, contact with farm animals, home delivery using unsterilized instruments and the use of traditional methods to take care of the stump (8, 9, 11, 24). Nonetheless, wound myiasis can also be an indicator of neglect or self-neglect (24). Thus, social counseling should be considered in these cases and newborn care must be reinforced. Adequate wound care, keeping the umbilicus covered with clean dressings and adequate hygienic habits in general should all be included in the recommendations given to the mother or caretaker before discharge (2, 14, 15).
The New World screwworm (C. hominivorax), is the most common species causing myiasis in Central and South America. The incidence of human myiasis by this species has been declining progressively since 1958 due to the implementation of programmes using the sterile insect technique (SIT) that have led to the eradication of C. hominivorax in Curacao, North and Central America and North Africa (25). Sixty-five case reports of human disease have been published from 2000 up to 30 September 2019 according to a literature search performed in Pubmed, Medline, Google Scholar and Lilacs (Table 1). Sixty of the cases (92%) occurred in South America, mainly in Brazil (n = 31, 48%) and Argentina (n = 7, 11%). There was one case report in India, but the species could have been mistakenly identified. Common anatomical sites of infection were the oral cavity, chronic or traumatic wounds, scalp and natural orifices (ear, nose, vagina). Risk factors for infection include the extreme ages, male gender, rural residency, poor hygienic conditions, cancer, alcohol and drug use, malnutrition, mental impairment, prolonged mouth opening, and prosthetic material. Myiasis in the scalp was facilitated by pediculosis or seborrheic dermatitis.
Table 1. Cases of myiasis by Cochliomyia hominivorax published since 2000 in Pubmed, Medline, Google Scholar, and Lilacs.
In Colombia, the geographic distribution and economic burden of C. hominivorax, as well as the epidemiology of myiasis in both animals and humans, is unknown but this species is recognized as in important cause of livestock loss (87). Human myiasis by this species has been reported in the states of Antioquia (88, 89), Atlantico (57), Cundinamarca (41), and Boyaca (90), however notification of cases is not mandatory. Research is needed on the biology, epidemiology and population dynamics of this species in order to assess the political, geographic and economic viability of the implementation of programs for insect control in the country (87). Thus, nationwide protocols and surveillance systems are urgently needed to control this ongoing threat to animal and human health.
During its larvae stage, C. hominivorax is an obligate parasite of warm-blooded animals, including humans. Once the female is gravid, it deposits an average of 200 eggs in open wounds or natural orifices (1). Egg hatching occurs in approximately 12 h and then it takes 5–7 days for larvae to reach the third instar of maturity inside bovine wounds. This means that the patient possibly was infected in the first 2 days of life. Larvae penetrate deeply into wounds, tearing tissue and making tunnels with their mouths to find a warm and moist place. Then, they hook and cause an extensive destruction of tissue known as traumatic myiasis, which provokes wound swelling that may facilitate bacterial infection (91). Umbilical myiasis is particularly dangerous because it might induce fistulation, penetration of deep layers of the abdomen wall and secondary sepsis associated with omphalitis (2, 92), although none of these were found in our patient.
As in our case, treatment of myiasis is based on the removal of all visible larvae, cleaning of the wound and debridement of remaining necrotic tissue. Irrigation is helpful if the lesions have holes and/or cavities. Local application of ivermectin paralyzes the parasite and kills the larvae, facilitating the extraction and relieving pain (31). Turpentine or ether is used to suffocate the larvae, but this practice is not recommended as it could lead to complications such as anaphylaxis and sepsis (22). Surgical treatment is required when larvae are dead, decomposing or laying in deep tissues (8). Topical anthelmintic medication, bactericides, tetanus toxoid vaccine and systemic antibiotics should also be considered to prevent secondary sepsis. In many reports, the use of systemic ivermectin showed positive results, but further studies are needed to consider this a standard therapy (2, 7, 8).
Correct identification by a trained entomologist is helpful to understand the infestation mechanism, to plan treatment and to consider preventive actions. For etiological diagnosis, the larvae should be immersed in hot water for 30 s to retain length and morphology and then preserved in a 70–90% ethanol solution or isopropyl alcohol. The regions where the patient has been, the climatic conditions and the endemic species are also important for accurate identification (2). The peak period of infestation by C. hominivorax has been reported to be between June and August, in humid and warm locations (5), such as the city where the patient lived.
Livestock is an important economic source in neotropical regions where poverty and inadequate health conditions make it difficult to implement control and eradication programs. Therefore, myiasis will continue to be a sanitary problem in many countries of America, Africa and Asia. Furthermore, global warming and internationalization are likely to influence the migration of screwworm and other myiasis-causing species into new geographic areas that were previously unaffected by this problem. Naïve livestock host are more susceptible to insect replication, increasing the likelihood of outbreaks (93). Groups of individuals at high risk of myiasis should be targeted in prevention programs for C. hominivorax infection in areas were insect eradication programs are not available.
Ethics Statement
Ethical review and approval was not required for the study on human participants in accordance with the local legislation and institutional requirements. Written informed consent to participate in this study was provided by the participants' legal guardian/next of kin. A written informed consent was obtained from the mother of the newborn for pictures and publication of this case.
Author Contributions
LF-G and JM-F contributed to the diagnosis and treatment of the patient. They also obtained informed consent and gathered clinical data. JR-Z and PM-G reviewed the literature and wrote the manuscript. All the authors discussed and analyzed the case.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Supplementary Material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmed.2019.00292/full#supplementary-material
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Keywords: screwworm infection, newborn, umbilicus, myiasis, ivermectin, Colombia
Citation: Ruiz-Zapata JD, Figueroa-Gutiérrez LM, Mesa-Franco JA and Moreno-Gutierrez PA (2020) Umbilical Myiasis by Cochliomyia hominivorax in an Infant in Colombia. Front. Med. 6:292. doi: 10.3389/fmed.2019.00292
Received: 22 July 2019; Accepted: 28 November 2019;
Published: 22 January 2020.
Edited by:
Matthew H. Collins, Emory University, United StatesReviewed by:
Mario Santoro, Stazione Zoologica Anton Dohrn, ItalyAna Afonso, University of São Paulo, Brazil
Copyright © 2020 Ruiz-Zapata, Figueroa-Gutiérrez, Mesa-Franco and Moreno-Gutierrez. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Paula Andrea Moreno-Gutierrez, paula.moreno@uam.edu.co