Trichinella infections in wildlife in the Greater Kruger National Park, South Africa: unravelling epidemiological gaps with special emphasis on infectivity of Trichinella zimbabwensis in selected tropical fishes.
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Date
2020
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Abstract
Trichinella species are widely distributed on all continents with the exception of
Antarctica, although the full spectrum of Trichinella species found in sub-Saharan African
countries and their hosts has not been fully documented. This study was conducted to review
reports on Trichinella infections in wildlife in the Kruger National Park and also to identify
species and/or genotypes of Trichinella larvae isolated from muscle tissues of wildlife from
Kruger National Park and adjacent areas of the Limpopo and Mpumalanga provinces, South
Africa referred to as the Greater Kruger National Park using molecular techniques. A review
of Trichinella spp. isolates and their wildlife hosts from the Greater Kruger National Park
covering the period 1964–2011 was conducted and the results were compared with recent
findings where isolates collected between 2012 and 2016 were identified to genotype/species
level using molecular techniques. In the first 15 years the prevalence of infection was only
reported twice in scientific publications and the reports included only four carnivorous
mammal species and one rodent species. However, since the last report of Trichinella in an
African civet (Civettictis civetta) other wildlife species were tested in the KNP and one new
host was identified. Advances in molecular techniques allowed scientists to identify two
isolates, collected in 1966 and 1988 respectively as Trichinella T8. Another isolate collected
in 1991 was described as T. nelsoni. All of the other isolates found before 1991 were
erroneously identified as T. spiralis. Ninety samples collected during the 2012–2016 period
representing 15 mammalian, two avian- and three reptilian species were screened for
Trichinella infection using artificial digestion. Isolates detected were identified using a
multiplex polymerase chain reaction amplification of the ITS1, ITS2 and ESV regions of
ribosomal DNA followed by molecular analysis of the sequences. Twenty (20) samples from
seven wildlife species were positive for Trichinella spp. larvae with an overall prevalence of
21.1% (20/90). The prevalence was higher in carnivores (18.9%, 18/90) than in omnivores
(2.2%, 2/90). Analysis of sequences showed that eight of the isolates; two from spotted hyaena
(Crocuta crocuta) (2/8), three from lion (Panthera leo) (3/13), one from leopard (Panthera
pardus) (1/6), one from small spotted genet (Genetta genetta) (1/2) and one Nile monitor lizard
(Varanus niloticus) (1/2) conformed to Trichinella zimbabwensis. One isolate from a hyaena
was grouped under the encapsulated species clade comprising T. nelsoni and genotype
Trichinella T8 reported to be present in South Africa. This is the first report confirming natural
infection of T. zimbabwensis in hyaena, leopard, genet and Nile monitor lizard, adding to the
body of knowledge on the epidemiology of Trichinella infections in the Greater Kruger
National Park, South Africa. Ten Trichinella-like larvae recovered after digestion from four wildlife species in this study (2012–2016) revealed inconclusive results due to DNA
degradation from poor storage or too few larvae for analysis in comparison to 20 isolates from
five wildlife species not identified to species during the 1964–2011 period.
Knowledge on factors influencing the infectivity, epidemiology and survival of
Trichinella spp. in different climatological environments is scanty. Availability of this
knowledge will allow for the elucidation of epidemiology of Trichinella infections and the
prediction of probable host-parasite cycles within specific ecological niches. The recent
identification of new host species infected with three Trichinella taxa within the Greater Kruger
National Park prompted a revision of previously published hypothetical transmission cycles
for these species. Using data gathered from surveillance studies spanning the period 1964–
2016, and the recently obtained data from molecular identification of isolates from the Greater
Kruger National Park, the previously hypothesized transmission cycles were revised. The new
hypothesized transmission cycles were established in consideration of epidemiological factors
and prevalence data gathered from both the Greater Kruger National Park and similar wildlife
protected areas in Africa where the same host- and parasite species are known to occur. The
anecdotal nature of some of the presented data in the hypothesized transmission cycles
confirms the need for more intense epidemiological surveillance in the rest of South Africa and
continued efforts to unravel the epidemiology of Trichinella infections in this unique and
diverse protected landscape.
Furthermore, to determine the role of fish in the epidemiology of T. zimbabwensis in
the Greater Kruger National Park, experimental infections were conducted to assess the
infectivity of this species to catfish (Clarias gariepinus) and tigerfish (Hydrocynus vittatus).
Twenty-four catfish (581.7 ± 249.7 g) were randomly divided into 5 groups and experimentally
infected with 1.0 ± 0.34 T. zimbabwensis larvae per gram (lpg) of fish. Results showed no adult
worms or larvae in the gastrointestinal tract and body cavities of catfish euthanized at day 1, 2
and 7 post-infection (p.i.). These results suggest that African sharp tooth catfish does not play
a role in the epidemiology of the parasite irrespective of the fact that the fish cohabit with
crocodiles and Nile monitor lizards in the Greater Kruger National Park.
Forty-one tigerfish (298.6 ± 99.3 g) were randomly divided into three separate trials
(T). Each trial (T) was divided into groups (G) as follows; Trial 1 (T1G1); Trial 2 (T2G1, T2G2)
and Trial 3 (T3G1, T3G2, T3G3) infected with 2.12 ± 1.12 lpg of fish. An additional 7 tigerfish
were assessed for the presence of natural infection.
Two tigerfish from T1G1 yielded T. zimbabwensis larvae in muscle tissues on day 26
p.i. (0.1 lpg) and 28 p.i. (0.02 lpg), respectively. No adult worms or larvae were detected in the
fish from trials 2 or 3 on days 7, 21, 28, 33 or 35 p.i. or from the control group. Results from this study suggest tigerfish to be generally unsuitable hosts for T.
zimbabwensis. However, results from this study suggest that some individuals could, under
very specific, and as yet to be elucidated circumstances, maintain the larvae of T. zimbabwensis
but it could not be confirmed whether the parasite can fully develop and reproduce in this host.
These results preclude any definitive conclusion in respect of the potential of African
sharp tooth catfish and tiger fish to serve as potential hosts for T. zimbabwensis. The influence
of temperature on T. zimbabwensis larval development and survival in fish remains
inconclusive. It is possible that these fish could only become infected during warmer seasons
and in warmer climates. It is also not clear whether potentially infected fish would retain the
infection in subsequent colder seasons. Variability of temperatures between different
geographic regions may additionally influence the susceptibility of these fish to T.
zimbabwensis infection.
However, the plethora of biological-, geographical- and climatic factors that could
potentially influence the infectivity of T. zimbabwensis to certain fish host species precludes
any definitive conclusion on the role of fish in the parasite’s natural ecosystem. Results from
this study do suggest that tigerfish could, under very specific and as yet unknown
circumstances, sustain the development and establishment of T. zimbabwensis.
Description
Doctoral Degree. University of KwaZulu-Natal, Durban.