Molecular detection and characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi infections in dromedary camels (Camelus dromedaries) in Egypt

Ehab Kotb Elmahallawy; Pamela C Köster; Alejandro Dashti; Samia Qasem Alghamdi; Amira Saleh; Ahmed Gareh; Barakat M Alrashdi; Carolina Hernández-Castro; Begoña Bailo; Maha S Lokman; Eman A A Hassanen; David González-Barrio; David Carmena

doi:10.3389/fvets.2023.1139388

Molecular detection and characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi infections in dromedary camels (Camelus dromedaries) in Egypt

Front Vet Sci. 2023 Apr 20:10:1139388. doi: 10.3389/fvets.2023.1139388. eCollection 2023.

Authors

Affiliations

¹ Department of Zoonoses, Faculty of Veterinary Medicine, Sohag University, Sohag, Egypt.
² Parasitology Reference and Research Laboratory, National Centre for Microbiology, Madrid, Spain.
³ Department of Biology, Faculty of Science, Al-Baha University, Alaqiq, Al-Baha Province, Saudi Arabia.
⁴ Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Zagazig, Egypt.
⁵ Department of Parasitology, Faculty of Veterinary Medicine, Aswan University, Aswan, Egypt.
⁶ Biology Department, College of Science, Jouf University, Sakaka, Saudi Arabia.
⁷ Parasitology Group, Faculty of Medicine, Academic Corporation for the Study of Tropical Pathologies, University of Antioquia, Medellín, Colombia.
⁸ Department of Biology, College of Science and Humanities in Al-Kharj, Prince Sattam Bin Abdulaziz University, Al-Kharj, Saudi Arabia.
⁹ Department of Zoology and Entomology, Faculty of Science, Helwan University, Cairo, Egypt.
¹⁰ Department of Parasitology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt.
¹¹ CIBER Infectious Diseases (CIBERINFEC), Health Institute Carlos III, Madrid, Spain.

Abstract

Introduction: Few studies have investigated the occurrence of microeukaryotic gut parasites in dromedary camels in Egypt, and the majority of these investigations are based on microscopic analysis of fecal material.

Methods: Herein, we assessed the occurrence, molecular diversity, and zoonotic potential of protozoan (Cryptosporidium spp. and Giardia duodenalis) and microsporidian (Enterocytozoon bieneusi) pathogens in individual fecal samples (n = 102) of dromedary camels with (n = 26) and without (n = 76) diarrhea from Aswan Governorate, Upper Egypt. Other factors possibly associated with an increased risk of infection (geographical origin, sex, age, and physical condition) were also analyzed. The SSU rRNA or ITS genes were targeted by molecular (PCR and Sanger sequencing) techniques for pathogen detection and species identification.

Results and discussion: The most abundant species detected was G. duodenalis (3.9%, 4/102; 95% CI: 1.1-9.7), followed by Cryptosporidium spp. (2.9%, 3/102; 95% CI: 0.6-8.4). All samples tested negative for the presence of E. bieneusi. Sequence analysis data confirmed the presence of zoonotic C. parvum (66.7%, 2/3) and cattle-adapted C. bovis (33.3%, 1/3). These Cryptosporidium isolates, as well as the four Giardia-positive isolates, were unable to be amplified at adequate genotyping markers (Cryptosporidium: gp60; Giardia: gdh, bg, and tpi). Camels younger than 2 years old were significantly more likely to harbor Cryptosporidium infections. This connection was not statistically significant, although two of the three cryptosporidiosis cases were detected in camels with diarrhea. The spread of G. duodenalis infections was unaffected by any risk variables studied. This is the first report of C. parvum and C. bovis in Egyptian camels. The finding of zoonotic C. parvum has public health implications since camels may function as sources of oocyst pollution in the environment and potentially infect livestock and humans. Although preliminary, this study provides useful baseline data on the epidemiology of diarrhea-causing microeukaryotic parasites in Egypt. Further research is required to confirm and expand our findings in other animal populations and geographical regions of the country.

Keywords: Zoonoses; epidemiology; genotyping; microsporidia; protists; transmission.

Grants and funding

This study was partially funded by the Health Institute Carlos III (ISCIII), Spanish Ministry of Economy and Competitiveness under project PI19CIII/00029. EE is the recipient of a postdoctoral fellowship funded by the Ministry of the Higher Education of the Arab Republic of Egypt. DG-B is the recipient of a Sara Borrell Research Contract (CD19CIII/00011) funded by the Spanish Ministry of Science, Innovation, and Universities. AD is the recipient of a PFIS contract (FI20CIII/00002) funded by the Spanish Ministry of Science and Innovation and Universities. CH-C is the recipient of a fellowship funded by the Fundación Carolina (Spain) and the University of Antioquia, Medellín (Colombia).