First confirmation of the chicken eyeworm, Oxyspirura mansoni, as a causative pathogen of human cutaneous larva migrans by morphological and molecular evidence

Abstract

Human larva migrans is a zoonotic disease caused by larvae of various nematode species, with all previously confirmed pathogens originating from mammalian reservoirs. In 2020, a case series in Vietnam reported instances of cutaneous larva migrans caused by avian eyeworm larvae of the Oxyspirura genus. This nematode genus, belonging to the Thelaziidae family, includes 84 species that mainly parasitize the eyes of various bird species. They utilize different arthropod intermediate hosts, such as cockroaches, grasshoppers, and crickets, in their life cycle. Although the 18S sequences of the larvae were analyzed, the precise identification of the pathogen at the species level remains inconclusive. This study aims to identify the exact causative agent at the species level by analyzing larvae from a patient and adult eyeworms collected from chickens raised in his family using morphological and molecular methods. Molecular analysis of 18S rDNA, ITS2, and cox1 sequences revealed genetic identity between the larva from the patient and adult eyeworms from chickens, as well as with Oxyspirura mansoni from Thailand and Bangladesh. Additionally, morphological examinations further confirmed the adult chicken eyeworms as Oxyspirura mansoni. These findings confirm that O. mansoni larvae are responsible for human larva migrans, marking the first confirmation of nematode larvae from birds (chickens) as a pathogen causing an emerging neglected tropical disease in humans. Given the widespread distribution of this nematode, further research is crucial to investigate this neglected disease, not only in Vietnam but also in other regions. Understanding appropriate treatments and transmission routes is essential to prevent infections in both chickens and humans.

Keywords: Oxyspirura mansoni; Chicken eyeworm; Larva migrans; Larvae.

Fig. 1

Microscopic images of Oxyspirura mansoni collected from eyes of chickens raised in the backyard by the man who suffered from a pruritic cutaneous nematodiosis in Son La Province, Vietnam. a Whole body of a female and a male; b anterior end of a male showing divided buccal capsule (Bc), nerve ring (Nr) and excretory pore (Ep); c anterior end of a female showing long esophagus (Es); d posterior end of a male showing unequal genital spicules, short spicule (S-sp) and long spicule (L-sp); e posterior end of a female showing vulva (Vu) and anus (An)

Fig. 2

Molecular phylogenetic tree reconstructed from the 18S rDNA sequences. The evolutionary history was inferred using the maximum likelihood method based on the Kimura 2-parameter model with a discrete Gamma distribution (K2 + G). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 12 nucleotide sequences. All positions containing gaps and missing data were eliminated. Bootstrap values greater than 70% are shown above branches. Red text indicates nucleotide sequences obtained in this study. Other sequences were retrieved from GenBank with accession numbers and country of origin provided for Oxyspirura sequences. The scale bar indicates nucleotide substitutions per site

Fig. 3

Molecular phylogenetic tree reconstructed from the cox1 sequences. The evolutionary history was inferred using the maximum likelihood method based on the Tamura-Nei model with a discrete Gamma distribution (TN93 + G). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. The analysis involved 14 nucleotide sequences. Codon positions included were 1st + 2nd + 3rd. All positions containing gaps and missing data were eliminated. Bootstrap values greater than 70% are shown above branches. Red text indicates nucleotide sequences obtained in this study, while other sequences were retrieved from GenBank with accession numbers and country of origin provided for Oxyspirura sequences. The scale bar indicates nucleotide substitutions per site