Intestinal Protists in Captive Non-human Primates and Their Handlers in Six European Zoological Gardens. Molecular Evidence of Zoonotic Transmission

We assessed the occurrence, genetic diversity, and zoonotic potential of four protozoan (Cryptosporidium spp., Entamoeba histolytica, Entamoeba dispar, Giardia duodenalis), one stramenopile (Blastocystis sp.), one microsporidia (Enterocytozoon bieneusi), and two ciliate (Balantioides coli, Troglodytella abrassarti) intestinal parasite or commensal protist species in captive non-human primates (NHP) and their zookeepers from six European zoological gardens in France (n = 1), Germany (n = 1), and Spain (n = 4). Faecal samples from NHP (n = 454) belonging to 63 species within 35 genera and humans (n = 70) were collected at two sampling periods in each participating institution between October 2018-August 2021. Detection and species identification was accomplished by PCR and Sanger sequencing of the ssu rRNA and/or ITS genes. Sub-genotyping analyses using specific markers were conducted on isolates positive for G. duodenalis (gdh, bg, tpi) and Cryptosporidium spp. (gp60). Overall, 41.0% (186/454) and 30.0% (21/70) of the faecal samples of NHP and human origin tested positive for at least one intestinal protist species, respectively. In NHP, Blastocystis sp. was the most prevalent protist species found (20.3%), followed by G. duodenalis (18.1%), E. dispar (7.9%), B. coli and T. abrassarti (1.5% each), and Cryptosporidium spp. and E. bieneusi (0.9% each). Occurrence rates varied largely among NHP host species, sampling periods, and zoological institutions. The predominant protist species found in humans was Blastocystis sp. (25.7%), followed by Cryptosporidium spp. (2.9%), E. dispar (1.4%), and G. duodenalis (1.4%). Sequencing of PCR-positive amplicons in human and/or NHP confirmed the presence of Cryptosporidium in six isolates (C. hominis: 66.7%, C. parvum: 33.3%), G. duodenalis in 18 isolates (assemblage A: 16.7%, assemblage B: 83.3%), Blastocystis in 110 isolates (ST1:38.2%, ST2:11.8%, ST3: 18.2%, ST4: 9.1%, ST5: 17.3%, ST8: 2.7%, ST13: 0.9%), and E. bieneusi in four isolates (CM18: 75.0%, Type IV: 25.0%). Zoonotic transmission events involving Blastocystis ST1–ST4 were identified in four zoological institutions. Zoonotic transmission of C. hominis was highly suspected, but not fully demonstrated, in one of them. Monitoring of intestinal protist species might be useful for assessing health status of captive NHP and their zookeepers, and to identify transmission pathways of faecal-orally transmitted pathogens.

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Occurrence and Genetic Diversity of Protist Parasites in Captive Non-Human Primates, Zookeepers, and Free-Living Sympatric Rats in the Córdoba Zoo Conservation Centre, Southern Spain

Animals ◽

10.3390/ani11030700 ◽

2021 ◽

Vol 11 (3) ◽

pp. 700

Author(s):

Pamela C. Köster ◽

Alejandro Dashti ◽

Begoña Bailo ◽

Aly S. Muadica ◽

Jenny G. Maloney ◽

...

Keyword(s):

Giardia Duodenalis ◽

Enterocytozoon Bieneusi ◽

Southern Spain ◽

Free Living ◽

Entamoeba Dispar ◽

High Exposure ◽

Faecal Samples ◽

Blastocystis Sp ◽

Leishmania Spp ◽

Protist Species

Little information is currently available on the epidemiology of parasitic and commensal protist species in captive non-human primates (NHP) and their zoonotic potential. This study investigates the occurrence, molecular diversity, and potential transmission dynamics of parasitic and commensal protist species in a zoological garden in southern Spain. The prevalence and genotypes of the main enteric protist species were investigated in faecal samples from NHP (n = 51), zookeepers (n = 19) and free-living rats (n = 64) by molecular (PCR and sequencing) methods between 2018 and 2019. The presence of Leishmania spp. was also investigated in tissues from sympatric rats using PCR. Blastocystis sp. (45.1%), Entamoeba dispar (27.5%), Giardia duodenalis (21.6%), Balantioides coli (3.9%), and Enterocytozoon bieneusi (2.0%) (but not Troglodytella spp.) were detected in NHP. Giardia duodenalis (10.5%) and Blastocystis sp. (10.5%) were identified in zookeepers, while Cryptosporidium spp. (45.3%), G. duodenalis (14.1%), and Blastocystis sp. (6.25%) (but not Leishmania spp.) were detected in rats. Blastocystis ST1, ST3, and ST8 and G. duodenalis sub-assemblage AII were identified in NHP, and Blastocystis ST1 in zookeepers. Giardia duodenalis isolates failed to be genotyped in human samples. In rats, four Cryptosporidium (C. muris, C. ratti, and rat genotypes IV and V), one G. duodenalis (assemblage G), and three Blastocystis (ST4) genetic variants were detected. Our results indicate high exposure of NHP to zoonotic protist species. Zoonotic transmission of Blastocysts ST1 was highly suspected between captive NHP and zookeepers.

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Molecular evidence for zoonotic transmission of Giardia duodenalis among dairy farm workers in West Bengal, India

Veterinary Parasitology ◽

10.1016/j.vetpar.2011.01.029 ◽

2011 ◽

Vol 178 (3-4) ◽

pp. 342-345 ◽

Cited By ~ 39

Author(s):

Shahbaz Manzoor Khan ◽

Chanchal Debnath ◽

Amiya Kumar Pramanik ◽

Lihua Xiao ◽

Tomoyoshi Nozaki ◽

...

Keyword(s):

West Bengal ◽

Giardia Duodenalis ◽

Dairy Farm ◽

Farm Workers ◽

Zoonotic Transmission ◽

Molecular Evidence

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Epidemiological and molecular evidence supports the zoonotic transmission ofGiardiaamong humans and dogs living in the same community

Parasitology ◽

10.1017/s0031182003004505 ◽

2004 ◽

Vol 128 (3) ◽

pp. 253-262 ◽

Cited By ~ 181

Author(s):

R. J. TRAUB ◽

P. T. MONIS ◽

I. ROBERTSON ◽

P. IRWIN ◽

N. MENCKE ◽

...

Keyword(s):

Giardia Duodenalis ◽

Elongation Factor ◽

Epidemiological Data ◽

Northeast India ◽

Ssu Rdna ◽

Zoonotic Transmission ◽

Molecular Evidence ◽

Multiple Loci ◽

Elongation Factor 1 Alpha ◽

Elongation Factor 1

Giardia duodenalisisolates recovered from humans and dogs living in the same locality in a remote tea-growing community of northeast India were characterized at 3 different loci; the SSU-rDNA, elongation factor 1-alpha (ef1-α) and triose phosphate isomerase (tpi) gene. Phylogenetic analysis of the SSU-rDNA and ef1-α genes provided poor genetic resolution of the isolates within various assemblages, stressing the importance of using multiple loci when inferring genotypes toGiardia. Analysis of the tpi gene provided better genetic resolution and placed canineGiardiaisolates within the genetic groupings of human isolates (Assemblages A and B). Further evidence for zoonotic transmission was supported by epidemiological data showing a highly significant association between the prevalence ofGiardiain humans and presence of aGiardia-positive dog in the same household (odds ratio 3·01, 95% CI, 1·11, 8·39,P=0·0000).

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Wildlife Is a Potential Source of Human Infections of Enterocytozoon bieneusi and Giardia duodenalis in Southeastern China

Frontiers in Microbiology ◽

10.3389/fmicb.2021.692837 ◽

2021 ◽

Vol 12 ◽

Author(s):

Yan Zhang ◽

Rongsheng Mi ◽

Lijuan Yang ◽

Haiyan Gong ◽

Chunzhong Xu ◽

...

Keyword(s):

Giardia Duodenalis ◽

Enterocytozoon Bieneusi ◽

Zoonotic Potential ◽

Nested Polymerase Chain Reaction ◽

Type Iv ◽

Genomic Dnas ◽

Polymerase Chain ◽

Human Infections ◽

A New Species ◽

Group 1

Wildlife is known to be a source of high-impact pathogens affecting people. However, the distribution, genetic diversity, and zoonotic potential of Cryptosporidium, Enterocytozoon bieneusi, and Giardia duodenalis in wildlife are poorly understood. Here, we conducted the first molecular epidemiological investigation of these three pathogens in wildlife in Zhejiang and Shanghai, China. Genomic DNAs were derived from 182 individual fecal samples from wildlife and then subjected to a nested polymerase chain reaction–based sequencing approach for detection and characterization. Altogether, 3 (1.6%), 21 (11.5%), and 48 (26.4%) specimens tested positive for Cryptosporidium species, E. bieneusi, and G. duodenalis, respectively. Sequence analyses revealed five known (BEB6, D, MJ13, SC02, and type IV) and two novel (designated SH_ch1 and SH_deer1) genotypes of E. bieneusi. Phylogenetically, novel E. bieneusi genotype SH_deer1 fell into group 6, and the other genotypes were assigned to group 1 with zoonotic potential. Three novel Cryptosporidium genotypes (Cryptosporidium avian genotype V-like and C. galli-like 1 and 2) were identified, C. galli-like 1 and 2 formed a clade that was distinct from Cryptosporidium species. The genetic distinctiveness of these two novel genotypes suggests that they represent a new species of Cryptosporidium. Zoonotic assemblage A (n = 36) and host-adapted assemblages C (n = 1) and E (n = 7) of G. duodenalis were characterized. The overall results suggest that wildlife act as host reservoirs carrying zoonotic E. bieneusi and G. duodenalis, potentially enabling transmission from wildlife to humans and other animals.

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Molecular characterization of the waterborne pathogens Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, Cyclospora cayetanensis and Eimeria spp. in wastewater and sewage in Guangzhou, China

Parasites & Vectors ◽

10.1186/s13071-020-04566-5 ◽

2021 ◽

Vol 14 (1) ◽

Author(s):

Yingying Fan ◽

Xinrui Wang ◽

Ruohong Yang ◽

Wentao Zhao ◽

Na Li ◽

...

Keyword(s):

Wastewater Treatment Plants ◽

Giardia Duodenalis ◽

Enterocytozoon Bieneusi ◽

Quantitative Microbial Risk Assessment ◽

Waterborne Pathogens ◽

Microbial Risk Assessment ◽

Cyclospora Cayetanensis ◽

Type Iv ◽

Eimeria Spp ◽

Wastewater Samples

Abstract Background The waterborne pathogens Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi and Cyclospora cayetanensis can cause intestinal diseases in humans. An understanding of their occurrence and transport in the environment is essential for accurate quantitative microbial risk assessment. Methods A total of 238 influent samples were collected from four wastewater treatment plants (WWTPs) and 88 samples from eight sewer locations in Guangzhou, China. PCR-based tools were used to detect and genetically characterize Cryptosporidium spp., G. duodenalis and E. bieneusi. Eimeria spp. and Cyclospora spp. were also analyzed to assess the sources of Cryptosporidium spp., G. duodenalis and E. bieneusi in wastewater. Results The overall occurrence rates in the WWTP and sewer samples were 14.3% (34/238) and 13.6% (12/88) for Cryptosporidium spp., 55.5% (132/238) and 33.0% (29/88) for G. duodenalis, 56.3% (134/238) and 26.1% (23/88) for E. bieneusi and 45.4% (108/238) and 47.7% (42/88) for Eimeria spp., respectively. Altogether, 11 Cryptosporidium species and genotypes, six G. duodenalis genotypes, 11 E. bieneusi genotypes and four C. cayetanensis were found, together with the presence of nine Eimeria species. The common occurrence of Cryptosporidium rat genotype IV, C. muris and Eimeria papillata and E. nieschulzi suggested that rodents were significant sources of the enteric pathogens detected in the wastewater samples. Conclusions While the dominant Cryptosporidium spp. detected in the raw wastewater sampled in this study are not pathogenic to humans, the widely detected G. duodenalis assemblage A and E. bieneusi genotypes D and Type IV are well-known zoonotic pathogens. Further studies are needed to monitor the occurrence of these waterborne pathogens in WWTPs to better understand their transmission and environmental transport in China.

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Multilocus genotyping of Giardia duodenalis isolates from breeding cattery cats in Japan

Journal of Feline Medicine and Surgery Open Reports ◽

10.1177/2055116917745237 ◽

2017 ◽

Vol 3 (2) ◽

pp. 205511691774523

Author(s):

Yoichi Ito ◽

Yuko Iijima ◽

Naoyuki Itoh ◽

Yuya Kimura

Keyword(s):

Glutamate Dehydrogenase ◽

Ribosomal Rna ◽

Specific Antigen ◽

Giardia Duodenalis ◽

Small Subunit ◽

Zoonotic Transmission ◽

Ssu Rrna ◽

Triose Phosphate ◽

Multilocus Genotyping ◽

Faecal Samples

Objectives The present study reports the multilocus genotyping of Giardia duodenalis isolates from cats maintained in breeding catteries in Japan and discusses their potential for zoonotic transmission. Methods A total of 41 faecal samples positive for Giardia-specific antigen were procured from cats maintained in five breeding catteries and subjected to PCR to amplify four gene loci, namely small subunit ribosomal RNA ( SSU rRNA), glutamate dehydrogenase ( gdh), beta-giardin ( bg) and triose phosphate isomerase ( tpi ). The PCR-amplified DNA fragments were sequenced to determine the G duodenalis genotypes (synonym for assemblages). Results The most commonly occurring single assemblage was assemblage F (68.3%; n = 28/41), followed by assemblage A (12.2%; n = 5/41) and assemblage C (2.4%; n = 1/41). The mixed assemblages were identified as follows: assemblages F and A (9.8%; n = 4/41), assemblages F and C (4.9%; n = 2/41) and assemblages C and D (2.4%; n = 1/41). Additional sub-genotyping of assemblage A isolates based on three of the sequenced loci ( gdh, bg and tpi ) revealed that all eight isolates were identified as sub-assemblage AI and/or AII. Conclusions and relevance The present study is the first to report the detection of dog-adapted assemblages C and D in feline isolates from Japan. In addition, zoonotic sub-assemblage AI and human-adapted sub-assemblage AII were also identified. Thus, we concluded that the risk of transmission of G duodenalis from breeding cattery cats to humans is considerable and cannot be ignored.

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Burden of major diarrheagenic protozoan parasitic co-infection among amoebic dysentery cases from North East India: a case report

Parasitology ◽

10.1017/s0031182015000669 ◽

2015 ◽

Vol 142 (10) ◽

pp. 1318-1325 ◽

Cited By ~ 6

Author(s):

JOYOBRATO NATH ◽

GULZAR HUSSAIN ◽

BABY SINGHA ◽

JAISHREE PAUL ◽

SANKAR KUMAR GHOSH

Keyword(s):

Monsoon Season ◽

False Negative ◽

Parasitic Infection ◽

Giardia Duodenalis ◽

Enterocytozoon Bieneusi ◽

Dot Blot ◽

Entamoeba Dispar ◽

Amoebic Dysentery ◽

North East ◽

Stool Specimens

SUMMARYIntestinal diarrheagenic polyparasitic infections are among the major public health concerns in developing countries. Here we examined stool specimens by microscopy, DNA dot blot and polymerase chain reaction (PCR) to evaluate the co-infection of four principal protozoans among amoebic dysentery cases from Northeast Indian population. The multiplex PCR confirmedEntamoeba histolytica(8·1%),Entamoeba dispar(4·8%) and mixed infection of both the parasites (3·4%) in 68 of 356 stool specimens that were positive in microscopy and/or HMe probe based DNA dot blot screening. The prevailing parasite that co-exists withE. histolyticawasGiardia duodenalis(34·1%), followed byEnterocytozoon bieneusi(22·0%),Cryptosporidium parvum(14·6%) andCyclospora cayetanensis(7·3%,P= 0·017). Symptomatic participants (odds ratio (OR) = 4·07; 95% confidence interval (CI) = 1·06, 15·68;P= 0·041), monsoon season (OR = 7·47; 95% CI = 1·40, 39·84;P= 0·046) and participants with family history of parasitic infection (OR = 4·50; 95% CI = 1·16, 17·51;P= 0·030) have significant association with overall co-infection rate. According to molecular consensus, comprehensive microscopy yielded 3·4% (12/356) false-negative and 7·6% (27/356) false-positive outcome, suggesting an improved broad-spectrum PCR-based diagnostic is required to scale down the poor sensitivity and specificity as well as implementation of integrated control strategy.

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Molecular characterization of Giardia duodenalis isolated from Semai Pahang Orang Asli (Peninsular Malaysia aborigines)

Parasitology ◽

10.1017/s0031182009990527 ◽

2009 ◽

Vol 136 (11) ◽

pp. 1237-1241 ◽

Cited By ~ 20

Author(s):

A. K. MOHAMMED MAHDY ◽

JOHARI SURIN ◽

A. MOHD-ADNAN ◽

K.-L. WAN ◽

Y. A. L. LIM

Keyword(s):

Ribosomal Rna ◽

Giardia Duodenalis ◽

Small Subunit ◽

Peninsular Malaysia ◽

Rrna Gene ◽

Orang Asli ◽

Faecal Samples ◽

Staining Techniques ◽

Assemblage B

SUMMARYThis study was conducted to determine the genotypes of Giardia duodenalis isolated from human faecal samples at Pos Betau, Pahang, Malaysia. Faecal specimens were collected and examined for G. duodenalis cysts using Trichrome staining techniques. Molecular identification was carried out by the amplification of a region of the small subunit of the nuclear ribosomal RNA (SSU rRNA) gene using nested PCR and subsequent sequencing. The sequences from 15 isolates from G. duodenalis were subjected to phylogenetic analysis (including appropriate outgroups) using the neighbor-joining and maximum parsimony methods. The trees identified G. duodenalis assemblages A and B, with a predominance of assemblage B. The predominance of anthroponotic genotypes indicates the possibility of anthroponotic transmission of these protozoa in this Semai Pahang Orang Asli community.

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