Molecular epidemiology of ascariasis: a global perspective on the transmission dynamics of Ascaris in people and pigs

Abstract

Background: The roundworm Ascaris lumbricoides infects 0.8 billion people worldwide, and Ascaris suum infects innumerable pigs across the globe. The extent of natural cross-transmission of Ascaris between pig and human hosts in different geographical settings is unknown, warranting investigation.

Methods: Adult Ascaris organisms were obtained from humans and pigs in Europe, Africa, Asia, and Latin America. Barcodes were assigned to 536 parasites on the basis of sequence analysis of the mitochondrial cytochrome c oxidase I gene. Genotyping of 410 worms was also conducted using a panel of microsatellite markers. Phylogenetic, population genetic, and Bayesian assignment methods were used for analysis.

Results: There was marked genetic segregation between worms originating from human hosts and those originating from pig hosts. However, human Ascaris infections in Europe were of pig origin, and there was evidence of cross-transmission between humans and pigs in Africa. Significant genetic differentiation exists between parasite populations from different countries, villages, and hosts.

Conclusions: In conducting an analysis of variation within Ascaris populations from pig and human hosts across the globe, we demonstrate that cross-transmission takes place in developing and developed countries, contingent upon epidemiological potential and local phylogeography. Our results provide novel insights into the transmission dynamics and speciation of Ascaris worms from humans and pigs that are of importance for control programs.

Keywords: Ascaris; barcode; giant roundworm; microsatellite; neglected tropical disease; population genetics; soil-transmitted helminth; zoonosis.

Figure 1.

Minimum spanning TCS network of all cox1 haplotypes identified. A line indicates 1 base change. A black dot indicates a nonsampled or extinct haplotype. The size of the ovals is representative of the number of samples with a particular haplotype. Blue ovals represent haplotypes only found in worms from humans, pink ovals indicate haplotypes only found in worms from pigs, and purple ovals indicate haplotypes identified in worms from both hosts. The haplotype number is displayed in bold. The host type and geographical location are also indicated. Numbers indicate number of samples from each host type and location with the specific haplotype. The 3 clusters are labeled cluster A, cluster B, and cluster C. Abbreviations: BA, Bangladesh; DK, Denmark; GT, Guatemala; H, humans; KE, Kenya; NP, Nepal; P, pigs; PH, Philippines; TZ, Tanzania; UG, Uganda; UK, United Kingdom; ZA, Zambia; ZZ, Zanzibar.

Figure 2.

A–B, Cavalli-Sforza and Edwards' chord distances between Ascaris populations from different host types and locations represented in consensus neighbor joining trees based on 8 microsatellite markers. A, Populations stratified by host type and country. B, Populations stratified by host type and by country, by village, or by individual host, depending on the number of worms sampled for each location and host and whether information on individual hosts was available. Names of villages are provided in panel B, and if a population corresponds to worms from only 1 host, this is indicated in brackets. Bootstrap values are displayed and are based on 1001 replications. C, Assignment of Ascaris samples to clusters on the basis of STRUCTURE analysis. Output from a representative STRUCTURE run is presented. One cluster is indicated in red (mostly worms from pigs) and green (mostly worms from humans). Each narrow column corresponds to 1 sample. Examples of cross-transmission between human and pig hosts are indicated with black arrows. In addition, most worms from humans in the United Kingdom and Denmark appear to have originated from pigs. Abbreviations: BA, Bangladesh; DK, Denmark; GT, Guatemala; H, humans; KE, Kenya; NP, Nepal; P, pigs; PH, Philippines; TZ, Tanzania; UG, Uganda; UK, United Kingdom; ZA, Zambia; ZZ, Zanzibar.