Skip to main content
NCBI home page
Veterinary Research Forum logoLink to Veterinary Research Forum
. 2023 Jun 15;14(6):335–340. doi: 10.30466/vrf.2022.545726.3336

Frequency and genotyping of Giardia duodenalis in dogs of Urmia, northwest of Iran

Reza Esmailzadeh 1, Farnaz Malekifard 1,*, Alaleh Rakhshanpour 2, Mousa Tavassoli 1
PMCID: PMC10298836  PMID: 37383654

Abstract

Giardia duodenalis is a zoonotic protozoan infecting various vertebrates such as humans and domestic animals. The aim of this study was to determine the frequency and genotypes of G. duodenalis using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) in dogs of Urmia, Iran. Overall, 246 stool specimens were collected from 100 pet, 49 stray, and 97 shelter dogs in the Urmia, Iran. Totally, seven samples (2.48%) were microscopically positive in terms of Giardia cyst. The PCR-RFLP analysis revealed that three (1.21%) and two (0.83%) samples have the C and D genotypes, respectively. In addition, two samples (0.83%) were belonged to the AI sub-group. A significant association was determined between the frequency of Giardia infection and life style, age, and stool form of dogs. The findings of the study showed the high frequency of Giardia infection in stray dogs and the dogs under one-year-old. Furthermore, the C and D genotypes of G. duodenalis were predominant in dogs of Urmia, Iran.

Introduction

Giardia duodenalis (also known as G. intestinalis or G. lamblia) is a protozoan parasite infecting human, and domestic and wild animals.1 Giardiosis results from ingesting cysts, which are transmitted through various sources such as contaminated water and food.2 There are reports regarding more than 280 million human cases of diarrhea caused by Giardia every year, and the Giardia infection has been noticed in more than 40 animal species all over the world.3 A former study has showed the significant role of dogs in Giardia transmission to human beings;4 however, this result was rejected by another study.5

The molecular genetic analysis of the conserved genes loci has shown that G. duodenalis parasite has at least seven major genotypes (A-H).6 Two genotypes of A and B are detected in different mammalian hosts and human beings; therefore, they are considered as genotypes with the highest zoonotic potential for public health.7 Genotypes of C and D have found only in dog isolates, E genotype infects hoofed livestock, F genotype infects cats, G genotype has the potential to infect rats, and H genotype has been found in marine mammals.8,9 The A genotype consists of isolates being classified into two clusters with distinct features. The AI includes a combination of closely related human and animal isolates being widespread in various parts of the world; most attention conducted on the zoonotic potential of the AI sub-group.9,10 However, the second sub-group (AII) is composed of human isolates. Furthermore, B genotype has two sub-groups named III and IV; IV sub-group seems to be specific for the humans.1,6

Direct wet-mount, staining, and concentration are parasitological procedures used for detecting Giardia.11,12 Furthermore, different polymerase chain reaction (PCR)-based molecular genetics methods have been used to detect G. duodenalis cysts in the feces of isolates originating from humans and animals. Several researchers have used the PCR- restriction fragment length polymorphism (RFLP) method to distinguish Giardia genotypes related to human and animals.1,13-15 Genotypes of G. duodenalis are based on the analysis of various parameters including small sub-unit ribosomal RNA, triosephosphate isomerise, glutamate dehydrogenase (gdh), elongation factor 1-alpha, β-giardin, and variant surface protein genes.16,17 The gdh gene is proven to be useful for determining the genotype of Giardia isolated from mammalian species.14

Several epidemiological studies in Iran have investigated the zoonotic intestinal parasites in canines.2,18,19 Recently, in a study by Homayouni et al.,20 D, C and A assemblages of G. intestinalis having sub-assemblage of AII were identified in dogs of Shiraz, southwestern Iran. However, there are limited data about the G. duodenalis assemblages distributions in dogs residing in Urmia, Iran. Hence, this study was designed to determine the frequency and genotypes of G. duodenalis isolates in dogs in Urmia, northwestern Iran, to evaluate these pathogens zoonotic potential.

Materials and Methods

Chemicals. All chemical compounds used in the present study were obtained from Sigma-Aldrich Company (St. Louis, USA).

Study area. The study was carried out from July 2018 to March 2019 in Urmia, West Azerbaijan province, northwestern Iran. The region of the study is an agriculturally fertile area being located between 37° 32´ N and 45° 04´ E, and the area is estimated to be around 8,000 km2. The temperature of the study area varies from – 3.80 ˚C to 23.40 ˚C during different seasons. The area is bordered with Iraq and Türkiye.21

Collection of Samples. For this study, a total of 246 dogs including 49 strays, 97 shelter, and 100 pet dogs were selected randomly. The majority of sampled dogs (228/ 246) had no symptoms. Various parameters including age, gender, keeping conditions (indoor/outdoor), and fecal consistency (diarrheic/non-diarrheic) of all selected dogs were recorded. An individual disposable latex glove was used to collect fecal samples from the rectum of all dogs. The collected samples were placed in plastic specimen cups equipped with a screw-on lid, labeled and sent to the Parasitology Laboratory of Faculty of Veterinary Medicine, Urmia University, Urmia, Iran, within 2 hr after collection. The samples were stored at 4.00 ˚C and examined within 24 hr. Sucrose flotation was utilized to isolate and partially purify the Giardia cysts.22,23 The semi-filtered and concentrated cysts were kept in sterile distilled water without adding any preservatives for up to two weeks at – 20.00 ˚C. Ethical approval for this study was obtained from Veterinary Ethic Committee of Urmia University, Urmia, Iran (Approval Number: IRR-UU-AEC-3-89-AD).

DNA extraction. The cyst wall was disrupted in fecal samples with freeze-thaw or glass beads. The following procedure was used to extract DNA by utilizing phenol-chloroform-isoamylalcohol (PCI) on purified and concentrated fecal samples by sucrose gradient and sedimentation of ethyl acetate samples. In the first step, 200 μL of sucrose gradient or sediment concentrated cysts sample was mixed with 200 μL 3.00% Triton X100 and incubated in a water bath for 1 hr at 75.00 ˚C. Next, 200 μL of lysis buffer and 10.00 μL of proteinase K were mixed with 200 μL of homogenate and incubated overnight at 37.00 ˚C. Genomic DNA was extracted from the cysts by PCI method. Then, PCI was mixed with the solution prior to centrifugation (Eppendorf, Hamburg, Germany) at 15,000 rpm for 10 min at 25.00 ˚C. Ethanol absolute (two or four equals) was used to precipitate the supernatant in a new tube for 24 hr at – 20.00 ˚C. The resulting solution was centrifuged at 15,000 rpm for 10 min at a temperature of 4.00 ˚C. The sediment was air-dried, and 100 mL deionized distilled water was added to it before storing at – 20.00 ˚C until PCR analysis.24

Polymerase chain reaction amplification. The gdh genes were amplified by a single PCR. Amplification of the 432 bp fragment during the PCR was done using the forward primer (GDHiF), 5´-CAGTACAACTCTGCTCTCGG-3' and the reverse primer (GDHiR), 5´-GTTGTCCTTGCA CATCTCC-3'.24 For this study, the amplification reaction was modified as follows: PCR mix had 1X buffer containing 1.50 mM MgCl2, each deoxynucleotide triphosphate at the concentration of 100 μM, each primer at a concentration of 0.50 μM, 10.00 ng of DNA, and 2.50 U of Taq DNA polymerase (Sinaclon, Tehran, Iran). Cycling parameters were 10 min at 94.00 ˚C (initial heat activation step), followed by 30 cycles of 35 sec at 94.00 ˚C, 35 sec at 61.00 ˚C, and 50 sec at 72.00 ˚C, with a final extension of 7 min at 72.00 ˚C.24 To validate the results, negative and positive controls were included in the PCR analysis. Cysts and distilled water were used as templates for positive and negative controls, respectively.

Restriction fragment length polymorphism of the gdh gene. The RFLP was conducted on all specimens being PCR-positive. Furthermore, RFLP was used for genotyping G. duodenalis according to the method described previously.1 The RFLP analysis was conducted by digesting 8.00 μL of PCR products with 1.50 U 0.80 U of NIaIV enzyme (Vivantis, Shah Alam, Malaysia) in 2.00 μL of 10X enzyme buffer in a final volume of 20.00 μL for 3 hr at 37.00 ˚C.1 Horizontal electrophoresis in 1.50 and 2.00% agarose gels and Ethidium Bromide were respectively used for the separation of PCR products and restriction fragments. Table 1 shows the expected fragments following digestion by specific restriction NlaIV enzymes.

Table 1.

Restriction fragment length polymorphism profiles of Giardia duodenalis assemblages after digesting with NlaIV.

Assemblages of G. duodenalis Diagnostic genotyping profile
AI 90, 120, 150
AII 70, 80, 90, 120
C 120, 70, 190
D 120, 250
Open in a new tab

Statistical analysis. The SPSS software (version 26.0; IBM Corp., Armonk, USA) was used to analyze the results. The association between the frequency of Giardia infection and various variables such as age, sex, and fecal consistency was analyzed by Chi-square test; values less than 0.05 were considered significant (p < 0.05).

Results

Of 246 fecal samples, the Giardia cysts were microscopically diagnosed in seven samples (2.84%), and GDHiF and GDHiR primers were used to amplify the gdh gene in the PCR as shown in Figure 1A. At the Table 2, the frequency of G. duodenalis in association with age, sex, fecal consistency, and keeping conditions is shown. As shown in Table 2, the frequency of Giardia infection was significantly higher in dogs less than one-year-old and stray and diarrheic dogs than other dogs (p < 0.05). The PCR-RFLP analysis showed that the AI, C and D genotypes were detected in PCR products samples (Fig. 1B).

Fig. 1.

Fig. 1

Open in a new tab

A) Electrophoretic separation of polymerase chain reaction (PCR) product from DNA amplified at the gdh locus of Giardia duodenalis on an Ethidium Bromide stained 1.50% agarose gel. Lane M: 100 bp gene ruler (fermentase); Lane 1: Negative control; Lane 2: Positive control; Lanes 3 and 4: PCR products from examined samples (432 bp fragment). B) The NIaIV digestion of polymerase chain reaction products on an Ethidium Bromide stained 2.00% high resolution agarose gel. Lane M: 100 bp gene ruler (fermentase); Lane1: AI assemblage of Giardia duodenalis; Lanes 2-4: C assemblage of G. duodenalis; Lane 5: D assemblage of G. duodenalis.

Table 2.

Frequency of Giardia duodenalis infection in dogs of Urmia, Iran.

graphic file with name vrf-14-335-g001.jpg
Open in a new tab

Discussion

The current study identified G. duodenalis cyst in 2.84% of the fecal samples using microscopic evaluation. Some other studies conducted in Iran have used microscopical examination; but, they have reported a lower prevalence of G. duodenalis. These studies found 0.07% G. duodenalis in 98 stray dogs and 0.09% G. duodenalis infection in 100 samples.25,26 Fazaeli et al. have conducted a study in Zanjan, Iran, and reported an infection rate of 1.60% in stray dogs.2 The G. duodenalis infection rate in dogs reported in different studies in various geographical locations after fecal examination ranged from 0.09 to 28.00%.27-30 The different results may be due to several factors including the type of climate, life style of dogs, and applied diagnostic methods.10,30 Diarrhea or loose stool is a significant symptom of giardiosis.31 Our study results showed that the dogs suffering from diarrhea had a higher prevalence of G. duodenalis compared to healthy ones, and this result was consistent with that of Shin et al.32 Uiterwijk et al.31 have showed that dogs diagnosed as positives for Giardia have loose stool and shed more cysts. Our study also added the young age as a risk factor for the G. duodenalis transmission in dogs, being consistent with the results obtained by other studies in different geographical areas. Gender did not have a significant role in the prevalence of Giardia infection in the present study, and this result is in line with other studies conducted in Korea, Brazil, and Australia.32-34

Giardiosis is considered as an infectious zoonotic disease that can be transmitted from infected dogs, cats, sheep, and cattle to human. Although A and B assemblages are the genotypes known to be zoonotic, more rarely human cases have been identified with C, D, and F assemblages.35-38 The zoonotic genotypes (A and B) and the host-related, non-zoonotic genotypes (C and D) lead to the dogs infection.39

Determination of G. duodenalis genotype is a way to determine the infection epidemiology and implement preventive measures.14 It is noteworthy to mention that gdh locus is stable in the isolates taken from various species and identified in different geographical locations. It is the reason of its application to differentiate G. duodenalis assemblages and their genetic diversity.16,40-43 Genotyping of Giardia is mainly done by PCR-RFLP due to its simple, rapid, and sensitive nature.25,44,45 It is also the best tool available for researchers to detect mixed genotypes.1,15

Most of samples in this study were C and D assemblages of G. duodenalis. Various other studies in different geo-graphical areas including Hungary, Brazil, China, and Japan have showed that C and D genotypes have the highest prevalence.46-48 It should also be noted that the fecal origin can influence the outcome of genotyping. The results obtained from this study indicated that stray dogs had a higher infection rate compared to the pet and shelter dogs. The results of a previous study being conducted on fecal samples from stray dogs have showed that the close contact between stray dogs living together is a reason for the transmission of dog-specific genotypes and the higher prevalence of G. duodenalis infection in stray dogs.2

In this study, AI zoonotic genotype was detected in positive animals. Previous studies have showed the prevalence of zoonotic genotypes in Australia, Thailand, and Belgium.49 A study in China conducted by Zheng et al.47 has showed that most dogs in this region are infected with the A zoonotic assemblage. A study done in Japan has also showed that out of 24 fecal samples analyzed, 14 are belonged to the A assemblage and three of the samples have the sequences related to both A and D assemblages.15 Transmission of zoonotic assemblages was studied by Adell-Aledón et al.50 in Spain, and the results reported A and B zoonotic assemblages as well as C and D host-specific assemblages. The results of a study conducted by Shin et al.32 have showed an assemblage of G. intestinalis in fecal samples collected from dogs in Korea. They have also noted the potential of Giardia transmission from dogs to humans and vice versa.

In conclusion, as far as we are concerned, this is the first molecular study regarding Giardia genotyping of dogs conducted in this region. The results of this analysis showed that C and D genotypes of G. duodenalis had the highest prevalence in this region. It should also be noted that A zoonotic genotype was reported in some cases. More studies are needed in other endemic regions of Iran to assess the effects of Giardia infection in dogs on public health.

Conflict of interest

None of the authors have any conflict of interest to declare.

Acknowledgments

The present work was extracted from the Doctor of Veterinary Medicine thesis of Dr. Reza Esmailzadeh conducted at Urmia University, Urmia, Iran. The authors would like to sincerely thank the members of the Faculty of Veterinary Medicine and Urmia University Research Council for the approval and support of this research.

References

  • 1.Read CM, Monis PT, Thompson RC. Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol. 2004;4(2):125–130. doi: 10.1016/j.meegid.2004.02.001. [DOI] [PubMed] [Google Scholar]
  • 2.Fazaeli A, Kohansal MH, Spotin A, et al. Infection rate and genetic diversity of Giardia duodenalis assemblage C in Iranian stray dogs, targeting the glutamate dehydrogenase gene. Vet World. 2021;14(2):419–425. doi: 10.14202/vetworld.2021.419-425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Horlock-Roberts K, Reaume C, Dayer G, et al. Drug-free approach to study the unusual cell cycle of Giardia intestinalis. mSphere. 2017;2(5):e00384–16. doi: 10.1128/mSphere.00384-16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Berrilli F, D’Alfonso R, Giangaspero A, et al. Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Côte d’Ivoire: occurrence and evidence for environmental contamination. Trans R Soc Trop Med Hyg. 2012;106(3):191–195. doi: 10.1016/j.trstmh.2011.12.005. [DOI] [PubMed] [Google Scholar]
  • 5.de Lucio A, Bailo B, Aguilera M, et al. No molecular epidemiological evidence supporting household transmission of zoonotic Giardia duodenalis and Cryptosporidium spp from pet dogs and cats in the province of Álava, Northern Spain. Acta Trop. 2017;170:48–56. doi: 10.1016/j.actatropica.2017.02.024. [DOI] [PubMed] [Google Scholar]
  • 6.Monis PT, Andrews RH, Mayrhofer G, et al. Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infect Genet Evol. 2003;3(1):29–38. doi: 10.1016/s1567-1348(02)00149-1. [DOI] [PubMed] [Google Scholar]
  • 7.Xiao L, Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol. 2008;38(11):1239–1255. doi: 10.1016/j.ijpara.2008.03.006. [DOI] [PubMed] [Google Scholar]
  • 8.Monis PT, Thompson RC. Cryptosporidium and Giardia-zoonoses: fact or fiction? Infect Genet Evol. 2003;3(4):233–244. doi: 10.1016/j.meegid.2003.08.003. [DOI] [PubMed] [Google Scholar]
  • 9.Thompson RC. Giardiasis as a re-emerging infectious disease and its zoonotic potential. Int J Parasitol. 2000;30(12-13):1259–1267. doi: 10.1016/s0020-7519(00)00127-2. [DOI] [PubMed] [Google Scholar]
  • 10.Olson ME, O’Handley RM, Ralston BJ, et al. Update on Cryptosporidium and Giardia infections in cattle. Trends Parasitol. 2004;20(4):185–191. doi: 10.1016/j.pt.2004.01.015. [DOI] [PubMed] [Google Scholar]
  • 11.Arani AS, Alaghehbandan R, Akhlaghi L, et al. Prevalence of intestinal parasites in a population in south of Tehran, Iran. Rev Inst Med Trop Sao Paulo. 2008;50(3):145–149. doi: 10.1590/s0036-46652008000300003. [DOI] [PubMed] [Google Scholar]
  • 12.Mohammed Mahdy AK, Surin J, Wan KL, et al. Giardia intestinalis genotypes: Risk factors and correlation with clinical symptoms. Acta Trop. 2009;112(1):67–70. doi: 10.1016/j.actatropica.2009.06.012. [DOI] [PubMed] [Google Scholar]
  • 13.Fallah E, Nahavandi KH, Jamali R, et al. Molecular identification of Giardia duodenalis isolates from human and animal reservoirs by PCR-RFLP. J Biol Sci. 2008;8(5):896–901. [Google Scholar]
  • 14.Hazrati Tappeh K, Manafi G, Asgharzadeh M, et al. Incidence of Giardia lamblia subspecies by PCR-RFLP in stool specimens of hospitalized children at Urmia Mutahhari hospital, West Azerbaijan province, Iran. Iran J Parasitol. 2014;9(4):541–547. [PMC free article] [PubMed] [Google Scholar]
  • 15.Itagaki T, Kinoshita S, Aoki M, et al. Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamete dehydrogenase gene sequencing. Vet Parasitol. 2005;133(4):283–287. doi: 10.1016/j.vetpar.2005.05.061. [DOI] [PubMed] [Google Scholar]
  • 16.Wielinga CM, Thompson RC. Comparative evaluation of Giardia duodenalis sequence data. Parasitology. 2007;134(Pt 12):1795–1821. doi: 10.1017/S0031182007003071. [DOI] [PubMed] [Google Scholar]
  • 17.Plutzer J, Ongerth J, Karanis P. Giardia taxonomy, phylogeny and epidemiology: Facts and open questions. Int J Hyg Environ Health. 2010;213(5):321–333. doi: 10.1016/j.ijheh.2010.06.005. [DOI] [PubMed] [Google Scholar]
  • 18.Kohansal MH, Fazaeli A, Nourian A, et al. Dogs’ gastrointestinal parasites and their association with public health in Iran. J Vet Res. 2017;61(2):189–195. doi: 10.1515/jvetres-2017-0024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Sarvi S, Daryani A, Sharif M, et al. Zoonotic intestinal parasites of carnivores: A systematic review in Iran. Vet World . 2018;11(1):58–65. doi: 10.14202/vetworld.2018.58-65. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Homayouni MM, Razavi SM, Shaddel M, et al. Prevalence and molecular characterization of Cryptosporidium spp and Giardia intestinalis in household dogs and cats from Shiraz, Southwestern Iran. Vet Ital. 2019;55(4):311–318. doi: 10.12834/VetIt.1710.9049.3. [DOI] [PubMed] [Google Scholar]
  • 21.Yakhchali M, Hosseini A. Prevalence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Vet Arh. 2006;76(5):431–442. [Google Scholar]
  • 22.Luchtel DL, Lawrence WP, DeWalle FB. Electron microscopy of Giardia lamblia cysts. Appl Environ Microbiol. 1980;40(4):821–832. doi: 10.1128/aem.40.4.821-832.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Bertrand I, Albertini L, Schwartzbrod J. Comparison of two target genes for detection and genotyping of Giardia lamblia in human feces by PCR and PCR-restriction fragment length polymorphism. J Clin Microbiol. 2005;43(12):5940–5944. doi: 10.1128/JCM.43.12.5940-5944.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Malekifard F, Ahmadpour M. Molecular detection and identification of Giardia duodenalis in cattle of Urmia, northwest of Iran. Vet Res Forum. 2018;9(1):81–85. [PMC free article] [PubMed] [Google Scholar]
  • 25.Mirzaei M. Prevalence of stray dogs with intestinal protozoan parasites. Am J Anim Vet Sci. 2010;5(2):86–90. [Google Scholar]
  • 26.Garedaghi Y, Karimi B. Prevalence of intestinal protozoan parasites in stray dogs of Tabriz city, Iran. Indian J Fundam Appl Life Sci. 2014;4(2):20–24. [Google Scholar]
  • 27.Silva MS, Uzêda RS, Costa KS, et al. Detection of Hammondia heydorni and related coccidia (Neospora caninum and Toxoplasma gondii) in goats slaughtered in Bahia, Brazil. Vet Parasitol. 2009;162(1-2):156–159. doi: 10.1016/j.vetpar.2009.02.007. [DOI] [PubMed] [Google Scholar]
  • 28.Tseng YC, Ho GD, Chen T TW, et al. Prevalence and genotype of Giardia duodenalis from faecal samples of stray dogs in Hualien city of eastern Taiwan. Trop Biomed. 2014;31(2):305–311. [PubMed] [Google Scholar]
  • 29.Qi M, Dong H, Wang R, et al. Infection rate and genetic diversity of Giardia duodenalis in pet and stray dogs in Henan Province, China. Parasitol Int. 2016;65(2):159–162. doi: 10.1016/j.parint.2015.11.008. [DOI] [PubMed] [Google Scholar]
  • 30.Upjohn M, Cobb C, Monger J, et al. Prevalence, molecular typing and risk factor analysis for Giardia duodenalis infections in dogs in a central London rescue shelter. Vet Parasitol. 2010;172(3-4):341–346. doi: 10.1016/j.vetpar.2010.05.010. [DOI] [PubMed] [Google Scholar]
  • 31.Uiterwijk M, Nijsse R, Kooyman FNJ, et al. Host factors associated with Giardia duodenalis infection in dogs across multiple diagnostic tests. Parasit Vectors. 2019;12(1):556 . doi: 10.1186/s13071-019-3810-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Shin JC, Reyes AW, Kim SH, et al. Molecular detection of Giardia intestinalis from stray dogs in animal shelters of Gyeongsangbuk-do (Province) and Daejeon, Korea. Korean J Parasitol. 2015;53(4):477–481. doi: 10.3347/kjp.2015.53.4.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Huber F, Bomfim TC, Gomes RS. Comparison between natural infection by Cryptosporidium sp Giardia sp in dogs in two living situations in the West Zone of the municipality of Rio de Janeiro. Vet Parasitol. 2005;130(1-2):69–72. doi: 10.1016/j.vetpar.2005.03.012. [DOI] [PubMed] [Google Scholar]
  • 34.Bugg RJ, Robertson ID, Elliot AD, et al. Gastrointestinal parasites of urban dogs in Perth, Western Australia. Vet J. 1999;157(3):295–301. doi: 10.1053/tvjl.1998.0327. [DOI] [PubMed] [Google Scholar]
  • 35.Liu J, Lee SE, Song KH. Prevalence of canine giardiosis in South Korea. Res Vet Sci. 2008;84(3):416–418. doi: 10.1016/j.rvsc.2007.06.003. [DOI] [PubMed] [Google Scholar]
  • 36.Broglia A, Weitzel T, Harms G, et al. Molecular typing of Giardia duodenalis isolates from German travellers. Parasitol Res. 2013;112(10):3449–3456. doi: 10.1007/s00436-013-3524-y. [DOI] [PubMed] [Google Scholar]
  • 37.Štrkolcová G, Maďar M, Hinney B, et al. Dog’s genotype of Giardia duodenalis in human: first evidence in Europe. Acta Parasitol. 2015;60(4):796–799. doi: 10.1515/ap-2015-0113. [DOI] [PubMed] [Google Scholar]
  • 38.Gelanew T, Lalle M, Hailu A, et al. Molecular characterization of human isolates of Giardia duodenalis from Ethiopia. Acta Trop. 2007;102(2):92–99. doi: 10.1016/j.actatropica.2007.04.003. [DOI] [PubMed] [Google Scholar]
  • 39.Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011;24(1):110–140. doi: 10.1128/CMR.00033-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Spotin A, Karamat M, Mahami-Oskouei M, et al. Genetic variability and transcontinental sharing of Giardia duodenalis infrapopulations determined by glutamate dehydrogenase gene. Acta Trop. 2018;177:146–156. doi: 10.1016/j.actatropica.2017.10.001. [DOI] [PubMed] [Google Scholar]
  • 41.Monis PT, Mayrhofer G, Andrews RH, et al. Molecular genetic analysis of Giardia intestinalis isolates at the glutamate dehydrogenase locus. Parasitology. 1996;112(Pt 1):1–12. doi: 10.1017/s0031182000065021. [DOI] [PubMed] [Google Scholar]
  • 42.Traub RJ, Monis PT, Robertson I, et al. Epidemiological and molecular evidence supports the zoonotic transmission of Giardia among humans and dogs living in the same community. Parasitology. 2004;128(Pt 3):253–262. doi: 10.1017/s0031182003004505. [DOI] [PubMed] [Google Scholar]
  • 43.Cacciò SM, Ryan U. Molecular epidemiology of giardiasis. Mol Biochem Parasitol. 2008;160(2):75–80. doi: 10.1016/j.molbiopara.2008.04.006. [DOI] [PubMed] [Google Scholar]
  • 44.Robertson LJ, Forberg T, Hermansen L, et al. Giardia duodenalis cysts isolated from wild moose and reindeer in Norway: genetic characterization by PCR-RFLP and sequence analysis at two genes. J Wildl Dis. 2007;43(4):576–585. doi: 10.7589/0090-3558-43.4.576. [DOI] [PubMed] [Google Scholar]
  • 45.Tan L, Wu S, Abdullahi AY, et al. PCR-RFLP method to detect zoonotic and host-specific Giardia duodenalis assemblages in dog fecal samples. Parasitol Res. 2016;115(5):2045–2050. doi: 10.1007/s00436-016-4948-y. [DOI] [PubMed] [Google Scholar]
  • 46.Szénási Z, Marton S, Kucsera I, et al. Preliminary investigation of the prevalence and genotype distribution of Giardia intestinalis in dogs in Hungary. Parasitol Res. 2007;101(Suppl 1):145–152. [Google Scholar]
  • 47.Zheng G, Alsarakibi M, Liu Y, et al. Genotyping of Giardia duodenalis isolates from dogs in Guangdong, China based on multi-locus sequence. Korean J Parasitol. 2014;52(3):299–304. doi: 10.3347/kjp.2014.52.3.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Souza SL, Gennari SM, Richtzenhain LJ, et al. Molecular identification of Giardia duodenalis isolates from humans, dogs, cats and cattle from the state of São Paulo, Brazil, by sequence analysis of fragments of glutamate dehydrogenase (gdh) coding gene. Vet Parasitol. 2007;149(3-4):258–264. doi: 10.1016/j.vetpar.2007.08.019. [DOI] [PubMed] [Google Scholar]
  • 49.Ballweber LR, Xiao L, Bowman DD, et al. Giardiasis in dogs and cats: update on epidemiology and public health significance. Trends Parasitol. 2010;26(4):180–189. doi: 10.1016/j.pt.2010.02.005. [DOI] [PubMed] [Google Scholar]
  • 50.Adell-Aledón M, Köster PC, de Lucio A, et al. Occurrence and molecular epidemiology of Giardia duodenalis infection in dog populations in eastern Spain. BMC Vet Res. 2018;14:26 . doi: 10.1186/s12917-018-1353-z. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Veterinary Research Forum are provided here courtesy of Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

RESOURCES