Occurrence of Giardia, Cryptosporidium , and Entamoeba in wild rhesus macaques ( Macaca mulatta ) living in urban and semi-rural North-West India

Abstract

Giardia duodenalis, Cryptosporidium spp., and Entamoeba spp. are intestinal protozoa capable of infecting a range of host species, and are important causes of human morbidity and mortality. Understanding their epidemiology is important, both for public health and for the health of the animals they infect. This study investigated the occurrence of these protozoans in rhesus macaques (Macaca mulatta) in India, with the aim of providing preliminary information on the potential for transmission of these pathogens between macaques and humans. Faecal samples (n = 170) were collected from rhesus macaques from four districts of North-West India. Samples were analysed for Giardia/Cryptosporidium using a commercially available direct immunofluorescent antibody test after purification via immunomagnetic separation. Positive samples were characterised by sequencing of PCR products. Occurrence of Entamoeba was investigated first by using a genus-specific PCR, and positive samples further investigated via species-specific PCRs for Entamoeba coli, Entamoeba histolytica, Entamoeba dispar and Entamoeba moshkovskii. Giardia cysts were found in 31% of macaque samples, with all isolates belonging to Assemblage B. Cryptosporidium oocysts were found in 1 sample, however this sample did not result in amplification by PCR. Entamoeba spp. were found in 79% of samples, 49% of which were positive for E. coli. Multiplex PCR for E. histolytica, E. dispar and E. moshkovskii, did not result in amplification in any of the samples. Thus in 51% of the samples positive at the genus specific PCR, the Entamoeba species was not identified. This study provides baseline information on the potential for transmission of these zoonotic parasites at the wildlife-human interface.

Occurrence and multilocus genotyping of Giardia duodenalis in captive non-human primates from 12 zoos in China

“…The infection rate in Changsha Zoo was similar to that detected in Wuhan Zoo (7.6%, 5/66) [8] and Guangxi Zoo (2.4%, 5/205) [21]. The various infection rates in different zoos may relate to geographic distribution [8,11,12,[14][15][16].…”

“…Average infection rate in this study was 8.3% (25/ 302), which was lower than a previous study in captive NHPs from seven zoos (18.6%, 92/496) (Shijiazhuang Zoo, Wuhan Zoo, Taiyuan Zoo, Changsha Wild Animal Zoo, Beijing Zoo, Shanghai Zoo and Shanghai Wild Animal Zoo) and also lower than our previous study from three zoos (17.7%, 15/85) in southwestern China (Guiyang Zoo, Bifengxia Zoo and Chengdu Zoo) [8,15]. Compared with other countries, the average infection rate in this study was closed to that in Thailand (7.0%, 14/200) [9] and Uganda (11.1%, 9/81) [10], but lower than that in North-West India (31.2%, 53/170) [11]. The differences of infection rates in NHPs may be related to animal health status, detection methods, or geo-ecological conditions [2,8,15,16,[22][23][24][25][26][27][28][29].…”

“…To date, there have been numerous studies about the Giardia duodenalis infection for nonhuman primates in the world, such as in Thailand (7.0%, 14/200) [9], Uganda (11.1%, 9/81) [10], India (31.2%, 53/170) [11], Netherlands/Belgium (61.6%, 159/258) [12], Italy (50.0%, 5/ 10) [13] and Spain (70.0%, 14/20) [14]. In China, Giardia duodenalis infection rates in ten zoos are reported between 0% to 44.0%, including Changsha Wild Animal Zoo (44.0%, 33/75), Guiyang Zoo (30.0%, 15/50), Beijing Zoo (22.2%, 16/72), Shanghai Wild Animal Zoo (20.9%, 14/ 67), Taiyuan Zoo (13.6%, 9/66), Wuhan Zoo (7.6%, 5/66), Shijiazhuang Zoo (11.2%, 10/89), Shanghai Zoo (8.2%, 5/61), Bifengxia Zoo (0%, 0/24) and Chengdu Zoo (0%, 0/11) [8,15].…”

“…In China, Giardia duodenalis infection rates in ten zoos are reported between 0% to 44.0%, including Changsha Wild Animal Zoo (44.0%, 33/75), Guiyang Zoo (30.0%, 15/50), Beijing Zoo (22.2%, 16/72), Shanghai Wild Animal Zoo (20.9%, 14/ 67), Taiyuan Zoo (13.6%, 9/66), Wuhan Zoo (7.6%, 5/66), Shijiazhuang Zoo (11.2%, 10/89), Shanghai Zoo (8.2%, 5/61), Bifengxia Zoo (0%, 0/24) and Chengdu Zoo (0%, 0/11) [8,15]. Giardia duodenalis has at least eight assemblages (A-H), only assemblages A, B, and E have been detected in NHPs, with assemblage B dominating [8][9][10][11][12][13][15][16][17][18][19][20]. Assemblages A and B, which are consider potentially zoonotic, were reported in NHPs from zoos [8][9][10][11][12][13][14][15][16], thus, NHPs may play a role in the transmission of G. duodenalis to humans.…”

Giardia duodenalisin primates: Classification and host specificity based on phylogenetic analysis of sequence data

“…Because the SSU gene is a multicopy locus, which increases the assay sensitivity (Stensvold, Lebbad, & Verweij, ), for some isolates, it may be the only marker for which amplification is achieved, despite other loci also being targeted (e.g. Debenham, Tysnes, Khunger, & Robertson, ). In addition, the most commonly used SSU primers only amplify a small fragment of the gene (<300 bp), making it less suitable to differentiate between Assemblages and/or subgenotypes.…”