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
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Area
2.2. Sampling
2.3. Epidemiological Questionnaire
2.4. DNA Extraction and Purification
2.5. Molecular Detection and Characterization of Giardia Duodenalis
2.6. Molecular Detection and Characterization of Cryptosporidium spp.
2.7. Molecular Detection and Characterization of Blastocystis sp.
2.8. Molecular Detection and Characterization of Enterocytozoon bieneusi
2.9. Molecular Differential Detection of Entamoeba histolytica and Entamoeba dispar
2.10. Molecular Detection of Balantioides coli
2.11. Molecular Detection of Troglodytella spp.
2.12. Molecular Detection of Leishmania spp.
2.13. Statistical Analysis
3. Results
3.1. Prevalence and Molecular Characterization of Enteroparasites in Captive Non-Human Primates
3.2. Prevalence and Molecular Characterization of Enteroparasites in Humans
3.3. Prevalence and Molecular Characterization of Enteroparasites and Leishmania spp. in Rats
3.4. Molecular-Based Evidence of Zoonotic Transmission
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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First Sampling Campaign | Second Sampling Campaign | All | ||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Frequency Positive Results (%) | Frequency Positive Results (%) | Frequency Positive Results (%) | ||||||||||||||||
Species | No. | Bl | Ed | Gd | Bc | Eb | No. | Bl | Ed | Gd | Bc | Eb | No. | Bl | Ed | Gd | Bc | Eb |
Cebuella pygmaea | 1 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 2 | 0.0 | 0.0 | 50.0 | 0.0 | 0.0 | 3 | 0.0 | 0.0 | 33.3 | 0.0 | 0.0 |
Cercocebus lunulatus | 3 | 100 | 0.0 | 100 | 0.0 | 0.0 | 3 | 33.3 | 100 | 66.7 | 0.0 | 0.0 | 6 | 66.7 | 50.0 | 83.3 | 0.0 | 0.0 |
Cercopithecus neglectus | 2 | 50.0 | 0.0 | 50.0 | 0.0 | 0.0 | 3 | 66.7 | 66.7 | 0.0 | 0.0 | 0.0 | 5 | 60.0 | 40.0 | 20.0 | 0.0 | 0.0 |
Eulemur fulvus | 2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 |
Hylobates leucogenys Ogilby | 4 | 75.0 | 100 | 25.0 | 0.0 | 0.0 | 3 | 33.3 | 33.3 | 0.0 | 0.0 | 33.3 | 7 | 57.1 | 71.4 | 14.3 | 0.0 | 14.3 |
Lemur catta | 2 | 100 | 0.0 | 0.0 | 0.0 | 0.0 | 0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 2 | 100 | 0.0 | 0.0 | 0.0 | 0.0 |
Macaca sylvanus | 5 | 40.0 | 0.0 | 0.0 | 0.0 | 0.0 | 3 | 33.3 | 100 | 100 | 0.0 | 0.0 | 8 | 37.5 | 37.5 | 37.5 | 0.0 | 0.0 |
Mandrillus leucophaeus | 5 | 40.0 | 0.0 | 0.0 | 20.0 | 0.0 | 3 | 33.3 | 33.3 | 0.0 | 33.3 | 0.0 | 8 | 37.5 | 12.5 | 0.0 | 25.0 | 0.0 |
Saimiri sciureus | 2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 3 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 5 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 |
Varecia variegata variegata | 2 | 50.0 | 0.0 | 0.0 | 0.0 | 0.0 | 3 | 100 | 0.0 | 0.0 | 0.0 | 0.0 | 5 | 80.0 | 0.0 | 0.0 | 0.0 | 0.0 |
Total | 28 | 50.0 | 14.3 | 17.9 | 3.6 | 0.0 | 23 | 39.1 | 43.5 | 26.1 | 4.3 | 4.3 | 51 | 45.1 | 27.5 | 21.6 | 3.9 | 2.0 |
Species Combination | No. of Faecal Samples |
---|---|
Blastocystis sp. Only | 10 |
E. dispar only | 4 |
G. duodenalis only | 1 |
Blastocystis sp. + E. dispar | 5 |
Blastocystis sp. + G. duodenalis | 4 |
G. duodenalis + E. dispar | 3 |
Blastocystis sp. + B. coli | 1 |
E. dispar + E. bieneusi | 1 |
G. duodenalis + Blastocystis sp. + E. dispar | 3 |
Total | 32 |
Species | Genotype | Sub-Genotype | Host Species | No. of Isolates | Locus | Reference Sequence | Stretch | Single Nucleotide Polymorphisms | GenBank ID |
---|---|---|---|---|---|---|---|---|---|
Giardia duodenalis | A | AII | C.t. | 1 | bg | AY072723 | 205–539 | None | MW417420 |
Blastocystis sp. | ST1 | Allele 1 | M.l., H.l., C.t. | 4 | ssu rRNA | MK357786 | 4–602 | None | MW414634 |
Allele 2 | C.t. | 1 | ssu rRNA | MT094302 | 36–539 | None | MW414635 | ||
Allele 2 | C.n. | 1 | ssu rRNA | MT094302 | 32–539 | C57A, 65InsG, A112G, C128A, C237T, C272T, A458C | MW414636 | ||
Alleles 1 + 2 | C.t., M.l. | 3 | ssu rRNA | MK357786 | 1–603 | G128R, A474W | MW414637 | ||
ST3 | Allele 34 | H.l., M.c., C.n. | 7 | ssu rRNA | MK801359 | 1–581 | G114A, A115T, A116G, A159G, T160A, A161T | MW414638 | |
Alleles 32 + 34 | C.n. | 1 | ssu rRNA | MK801359 | 1–586 | G114A, A115T, A116G, A159K, T160R, A161K, A162R | MW414639 | ||
ST8 | Allele 21 | V.v.v., L. c. | 6 | ssu rRNA | MT509451 | 1–525 | None | MW414640 | |
Balantioides coli | Unknown | - | M.l. | 2 | ITS | - | - | - | - |
Enterocytozoon bieneusi | D | - | H.l. | 1 | ITS | AF101200 | 31–419 | None | MW414645 |
Variable | Subject 38 | Subject 79 | Subject 86 |
---|---|---|---|
Sociodemographic factors | |||
Sex | Male | Male | Female |
Age (years) | 56 | 58 | 49 |
Protist infection/carriage | |||
Giardia duodenalis | Negative | Positive | Positive |
Blastocystis sp. | Positive | Negative | Positive |
Clinical factors | |||
Diarrhoea in the last 7 days | No | No | No |
Contact with children <5-years | No | No | No |
Diarrhoea in family members/relatives | Yes | No | No |
Work-related factors | |||
Activity | Veterinarian | Zookeeper | Zookeeper |
Exposure to faeces from NHP | Yes | Yes | Yes |
Exposure to faeces from animals other than NHP | Yes | Yes | Yes |
Any of these animal species with diarrhoea | Yes | Yes | Yes |
Food handler | Yes | Yes | Yes |
Behavioural factors | |||
Recent travel | Yes | No | No |
Contact with pet dogs | Yes | Yes | Yes |
Contact with pet cats | Yes | No | Yes |
Main drinking source—tap | Yes | Yes | Yes |
Main drinking source—bottled | No | No | No |
Swimming | No | No | No |
Handwashing | Frequently | Always | Always |
Vegetable washing | Always | Always | Always |
Species/Genotype | No. of Isolates | Reference Sequence | Stretch | Single Nucleotide Polymorphisms | GenBank ID |
---|---|---|---|---|---|
C. muris | 3 | AB089284 | 504–1012 | None | MW406908 |
C. rattia | 6 | MT504541 | 293–751 | None | MW406909 |
Rat genotype IV | 3 | JN172970 | 377–775 | None | MW406910 |
1 | JN172970 | 332–798 | C342T, C410T, C423T, 448DelT, G493A | MW406911 | |
1 | JN172970 | 332–752 | C342T, C410T, C423T, 490_491DelTT, G493A | MW406912 | |
1 | JN172970 | 328–814 | A428G, 448DelT, G493A | MW406913 | |
1 | JN172970 | 328–767 | A445G, 448DelT, G493A, T541A, T542A | MW406914 | |
1 | JN172970 | 348–776 | A445G, 448DelT, G493A, T541W, T542W | MW406915 | |
5 | JN172970 | 375–814 | 448DelT, G493A | MW406916 | |
1 | JN172970 | 454–678 | A459T, A475T, G493A | MW406917 | |
1 | JN172970 | 332–788 | A472G, 492InsT, G493A | MW406918 | |
3 | JN172970 | 341–814 | 490_491DelTT, G493A | MW406919 | |
1 | JN172970 | 481–814 | 490_491DelTT, G493A, G635A | MW406920 | |
Rat genotype V | 1 | MT504543 | 306–699 | A667G | MW406921 |
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Köster, P.C.; Dashti, A.; Bailo, B.; Muadica, A.S.; Maloney, J.G.; Santín, M.; Chicharro, C.; Migueláñez, S.; Nieto, F.J.; Cano-Terriza, D.; et al. 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 2021, 11, 700. https://doi.org/10.3390/ani11030700
Köster PC, Dashti A, Bailo B, Muadica AS, Maloney JG, Santín M, Chicharro C, Migueláñez S, Nieto FJ, Cano-Terriza D, et al. 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. 2021; 11(3):700. https://doi.org/10.3390/ani11030700
Chicago/Turabian StyleKöster, Pamela C., Alejandro Dashti, Begoña Bailo, Aly S. Muadica, Jenny G. Maloney, Mónica Santín, Carmen Chicharro, Silvia Migueláñez, Francisco J. Nieto, David Cano-Terriza, and et al. 2021. "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 11, no. 3: 700. https://doi.org/10.3390/ani11030700
APA StyleKöster, P. C., Dashti, A., Bailo, B., Muadica, A. S., Maloney, J. G., Santín, M., Chicharro, C., Migueláñez, S., Nieto, F. J., Cano-Terriza, D., García-Bocanegra, I., Guerra, R., Ponce-Gordo, F., Calero-Bernal, R., González-Barrio, D., & Carmena, D. (2021). 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, 11(3), 700. https://doi.org/10.3390/ani11030700