Multilocus genotyping and risk factor analysis of Giardia duodenalis in dogs in Korea

Highlights

• Multilocus Giardia sequence typing, including 18S rRNA, gdh, and β-giardin genes, was assessed in dogs in Korea.

• Of 640 dog stool samples, 99 (15.5%) were positive for G. duodenalis in sheltered, companion, and special-purpose dogs.

• Phylogenetic analysis revealed that all G. duodenalis-positive samples belonged to assemblages C and D.

• Assemblage C has the potential to be transmitted from dogs to humans.

• The living environment of dogs cannot be ignored and continuous follow-up monitoring is needed.

Abstract

Giardia duodenalis (syn. G. intestinalis, G. lamblia), a protozoan parasite that infects most mammals (including humans), has recently been classified into eight different groups/assemblages (A to H) based on host range and genetic characteristics. Assemblages A and B have been reported in humans and in many other animals, including dogs. This study analyzed Giardia infections, implementing multilocus genotyping, including the 18S rRNA, gdh, and β-giardin genes, in sheltered, companion, and special-purpose dogs throughout Korea. Of 640 dog stool samples, 99 (15.5%) were G. duodenalis-positive; this prevalence was similar to that previously reported in Korean calves. In addition, the prevalence was significantly higher in the southern region, and lower in non-sheltered dogs, older dogs, and in the autumn season. Phylogenetic analysis revealed that all G. duodenalis-positive samples belonged to assemblages C and D. Although no G. duodenalis assemblages A and B (mainly found in humans) were identified in this study, assemblage C was detected in the main types of dogs in contact with humans. Assemblage C, thought to be dog-specific, was recently identified in humans. As Giardia (including zoonotic assemblages) is distributed throughout Korea, dog living environments and the potential for dog-human transmission should be monitored.

Introduction

Giardia is a well-known, globally distributed protozoan parasite associated with gastrointestinal diseases. This genus includes several species that infect various hosts including mammals, birds, and amphibians (Mark-Carew et al., 2013). This parasite can cause abdominal pain, diarrhea, bloating, weight loss, and malabsorption. It is commonly detected in companion animals and livestock, and in particular, is frequently found in domestic dogs (Shin et al., 2015).

Giardia duodenalis (syn. G. intestinalis, G. lamblia) is the only human-infective Giardia species that can also infect most other mammals including dogs (Heyworth, 2016). Recent studies have reported that this species comprises at least eight different assemblages (A to H) based on genetic characteristics and host range (Li et al., 2013; Heyworth, 2016). Host-specific lineages are represented by assemblages C and D, which are infective in dogs; assemblage E in ruminants and pigs; assemblage F in cats; assemblage G in mice and rats; and assemblage H in marine mammals (Li et al., 2013; Mark-Carew et al., 2013). In contrast, assemblages A and B are infective not only in humans, but also in many other animals, including dogs. These assemblages are considered to have broad host specificity and, therefore, constitute potentially zoonotic assemblages (Ballweber et al., 2010).

Interestingly, a recent study reported the occurrence of dog-specific G. duodenalis assemblage C in humans (Štrkolcová et al., 2015). Several studies have examined G. duodenalis genotypes in dogs, including reports on their zoonotic potential in many parts of the world such as Trinidad and Tobago, China, the Americas, Cambodia, south-eastern European countries, and Taiwan (Mark-Carew et al., 2013; Li et al., 2013; Inpankaew et al., 2014; Tseng et al., 2014; Zheng et al., 2014; Sommer et al., 2015; Coelho et al., 2016). Of the 26 samples identified in the Trinidad and Tobago study, four were identified as assemblage C (15.4%), 21 as assemblage D (80.8%), and one as assemblage E (3.8%) (Mark-Carew et al., 2013). The Chinese study tested 205 fecal samples, and confirmed 27 as being positive for G. duodenalis (13.2%); of these, 25 were identified as assemblage A and two as assemblage C (Li et al., 2013).

Studies on Giardia in Korea have reported an outbreak of human giardiasis due to water contamination (Cheun et al., 2013) and the discovery of cysts in the Han River (Lee et al., 2011). A serological study on canine Giardia in Korea was published in 2008 (Liu et al., 2008). In 2015, molecular detection of G. intestinalis was undertaken in sheltered animals in the Daejeon and Gyeongbuk Provinces in Korea (Shin et al., 2015). Interestingly, studies of Giardia in Korean calves detected only assemblage A in normal feces, and only assemblage E in diarrheal feces (Lee et al., 2016, 2018). Several studies have investigated age, sex, health status, and seasonal change as risk factors (Wade et al., 2000; Mircean et al., 2012; Mohamed et al., 2014).

The present study broadens the scope of previous studies by conducting a nationwide analysis of Giardia infections and performing multilocus genotyping in companion and special-purpose dogs, as well as sheltered dogs. We examined fecal type as well as age, sex, region, and season as risk factors, and investigated whether the different types of dogs had similar assemblage involvement.