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Volume 17, Number 10—October 2011

Letter

Zoonotic Ascariasis, United Kingdom

Suggested citation for this article

To the Editor: Ascaris lumbricoides/suum is a complex of closely related enteric roundworms that mainly infect humans and pigs (1). Transmission occurs through ingestion of fecally excreted ova. A. lumbricoides worms usually infect humans, mainly in regions with poor sanitation, where the environment is contaminated with human feces. In industrialized countries, human ascariasis is uncommon and cases are generally believed to have been imported (2). By contrast, A. suum infection of pigs occurs worldwide; in the United Kingdom, 3.4%–6.5% of pigs at slaughter have evidence of infection (3). Sporadic zoonotic infection with A. suum in the industrialized world is described (46) but poorly quantified. We describe probable zoonotic transmission of Ascaris spp. roundworms in Cornwall, a rural county in southwestern England.

Incidence rates for ascariasis in Cornwall and the rest of England were calculated from local and national laboratory data. From 2004 through 2008, a total of 18 cases were identified in Cornwall, and 314 from the rest of England were reported to the Health Protection Agency; annual rates were 0.87 and 0.12 cases per 100,000 population, respectively.

From 1995 through 2010, a total of 63 ascariasis cases were identified in Cornwall, and details of patient age, sex, and place of residence were collected. Patients from Cornwall were younger (mean age 22 years) than those from other parts of England (mean age 31 years), and the proportion of patients <5 years of age in Cornwall (35.5%) was greater than that in the rest of England (19.7%). Similar proportions (61% vs. 65%) of patients from Cornwall and England were female.

The possibility of zoonotic transmission in Cornwall was investigated by comparing risk factors for ascariasis and enterobiasis (caused by an enteric helminth that infects only humans). From 1995 through 2010, the laboratory in Cornwall identified 38 cases of Enterobius infection. Patient mean age was 24 years (range 1–95 years); 2 (5.7%) patients were <5 years of age and 23 (60.5%) were female. The following risk factors were considered for statistical analysis: age <5 years, female sex, and residence near pig herds. Residence was determined by comparing the postcodes of case-patients with postcodes of pig holdings registered with the Department of Environment, Food and Rural Affairs. The UK postal service allots a maximum of 80 households to a postcode. In rural areas like Cornwall, the number is much smaller. Consequently, sharing a postcode with a pig holding implies proximity to pig herds. Of the 50 ascariasis patients with a Cornwall postcode, 11 (22%) shared that postcode with a pig holding. Of the 35 enterobiasis patients in Cornwall, only 2 (5.7%) shared a postcode with a pig holding.

Odds ratios were calculated for all 3 risk factors, and the Fisher exact test was used to determine their significance. We calculated p values by using 2-tailed models for age and sex and a 1-tailed model to test the association with residence near a pig holding (Table). Significant associations were found for age <5 years (odds ratio 6.42, p = 0.0037) and living near pigs (odds ratio 4.65, p = 0.036) but not for female sex.

Further evidence for zoonotic transmission comes from molecular analyses of DNA extracted from 11 Ascaris spp. worms recovered from patients in Cornwall. Results were compared by PCR-linked restriction fragment length polymorphism and sequence analysis with those from 35 reference worms from pigs in the United Kingdom, Denmark, Uganda, Guatemala, and the Philippines and from 20 worms from humans in Uganda, Tanzania, and Nepal. We used the PCR-linked restriction fragment length polymorphism method described by Nejsum et al. (5). Briefly, the ribosomal internal transcribed spacer region was amplified, and the products were digested with the restriction enzyme HaeIII and separated into bands by agarose gel electrophoresis. All worms from humans and pigs in the United Kingdom had 3- or 4-banded genotypes, typically found in worms from pigs (4,5,7). By contrast, a 2-banded genotype predominated in worms collected from humans living in A. lumbricoides–endemic areas. Similarly, sequence analysis, as described by Nejsum et al. (8), of amplified mitochondrial cox1 genes using primers by Peng et al. (9) showed that all worms from humans in Cornwall clustered with worms from pigs (i.e., had pig-like DNA sequences).

Compared with the rest of the United Kingdom, incidence of human ascariasis is high in Cornwall, especially among children <5 years of age. Because of the retrospective nature of our study, we have little travel or clinical information for these case-patients. However, because such young case-patients would probably not travel much and because postcode data identified place of residence as a risk factor, the data suggest a focus of locally acquired A. suum infection in humans in Cornwall. Molecular evidence implicates pigs as the source. Further studies are needed, but if pigs are confirmed to be the source, control and prevention of this emerging infection will probably depend more on modifications of animal husbandry and fecal waste disposal rather than on human sanitation.

Richard P. BendallComments to Author , Maggie Barlow, Martha Betson, J. Russell Stothard, and Peter Nejsum
Author affiliations: Royal Cornwall Hospital, Truro, UK (R.P. Bendall); Health Protection Agency, St. Austell, UK (M. Barlow); Natural History Museum, London, UK (M. Betson, J.R. Stothard); Liverpool School of Tropical Medicine, Liverpool, UK (M. Betson, J.R. Stothard); University of Copenhagen, Copenhagen, Denmark (P. Nejsum)

Acknowledgments

We thank Sofie Nissen, Ida-Hella Poulsen, Harriet Namwanje, Helena Ngowi, Tim J.C. Anderson, Salcedo Eduardo, and Sarah Williams-Blangero for providing the worms; the Travel and Migrant Health Section Health Protection Agency, Centre for Infections, London, UK, for providing laboratory notification data; and Animal Health, Department for Environment, Food and Rural Affairs, Worcester, UK, for providing pig-holding registrations.

The article is dedicated to the memory of Carole Fitzsimons, who was instrumental in planning this study and collecting the worms, but who died before the project was complete.

References

  1. Peng W, Yuan K, Hu M, Gasser RB. Recent insights into the epidemiology and genetics of Ascaris in China using molecular tools. Parasitology. 2007;134:32530. DOIPubMed
  2. Maguire J. Intestinal roundworms. In: Mandell GL, Bennett JE, Dolin R, editors. Principles and practice of infectious diseases. 6th ed. Philadelphia: Elsevier Inc.; 2005. p. 3260–7.
  3. Sanchez-Vazquez MJ, Smith RP, Kang S, Lewis F, Nielen M, Gunn GJ, Identification of factors influencing the occurrence of milk spot livers in slaughtered pigs: a novel approach to understanding Ascaris suum epidemiology in British farmed pigs. Vet Parasitol. 2010;173:2719. DOIPubMed
  4. Anderson TJC. Ascaris infections in humans from North America: molecular evidence for cross-infection. Parasitology. 1995;110:2159. DOIPubMed
  5. Nejsum P, Parker ED, Frydenberg J, Roepstorff A, Boes J, Haque R, Ascariasis is a zoonosis in Denmark. J Clin Microbiol. 2005;43:11428. DOIPubMed
  6. Phillipson RF, Race JW. Human infection with porcine Ascaris. BMJ. 1967;3:865. DOI
  7. Peng W, Anderson TJ, Zhou X, Kennedy MW. Genetic variation in sympatric Ascaris populations from humans and pigs in China. Parasitology. 1998;117:35561. DOIPubMed
  8. Nejsum P, Bertelsen MF, Betson M, Stothard JR, Murrell KD. Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes). Vet Parasitol. 2010;171:2736. DOIPubMed
  9. Peng W, Yuan K, Hu M, Zhou X, Gasser RB. Mutation scanning-coupled analysis of haplotypic variability in mitochondrial DNA regions reveals low gene flow between human and porcine Ascaris in endemic regions of China. Electrophoresis. 2005;26:431726. DOIPubMed

Table

Suggested citation for this article: Bendall RP, Barlow M, Betson M, Stothard JR, Nejsum P. Zoonotic ascariasis, United Kingdom [letter]. Emerg Infect Dis [serial on the Internet]. 2011 Oct [date cited]. http://dx.doi.org/10.3201/eid1710.101826

DOI: 10.3201/eid1710.101826

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Table of Contents – Volume 17, Number 10—October 2011

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Richard P. Bendall, Royal Cornwall Hospital, Clinical Microbiology, Treliske, Truro TR1 3LJ, UK





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