Helminths as heirlooms and souvenirs: a review of new world paleoparasitology

Evidence from studies on ancient human feces, intestinal contents and organs of preserved bodies has established that Enterobius vermicularis, Trichuris trichiura, Diphyllobothrium spp and probably Trichinella spiralis infected humans in the pre-Columbian New World. These species, and perhaps other common human helminths for which there is not yet convincing evidence, probably accompanied transberingeal immigrants and their dogs, and thus can be seen as heirloom parasites. Early humans on the American continents were affected by helminths of native animals such as Paragonimus and Cryptocotyle, and these have also been found in precontact human remains. Michael Kliks considers that the indigenous parasites infecting early Americans may be viewed as zoonotic souvenirs of some 50 millennia of migrations from Alaska to Patagonia. Among the most serious zoonoses would have been infection by cystic hydatid larvae of echinococcid tapeworms, the many enzootic filarial worms, and a variety of larval trematodes and nematodes.     

Helminth communities of pademelons, Thylogale stigmatica and T. thetis from eastern Australia and Papua New Guinea

Gastrointestinal helminths were collected from pademelons of the genus Thylogale (Marsupialia: Macropodidae) in eastern Australia and Papua New Guinea. Examined were 12 Thylogale stigmatica stigmatica and 13 T. s. wilcoxi, the latter subdivided into eight specimens from the northern limit of their distribution and five from southern areas, all from eastern Queensland, Australia, one T. s. oriomo from Papua New Guinea and ten T. thetis from southeastern Queensland and northern New South Wales, Australia. Six species of cestodes and 40 species of nematodes were found. The helminth community of T. s. stigmatica was similar to that found in northern specimens of T. s. wilcoxi, while differences from the helminth community present in southern T. s. wilcoxi could be accounted for by parasites acquired from sympatric T. thetis. Thylogale thetis harboured a community of helminths distinct from but related to that in T. stigmatica. The evidence suggests that all subspecies of T. stigmatica examined share a common helminth community, but that in areas of sympatry, T. stigmatica and T. thetis share some of their parasites.     

Parasites and associated pathology of the swamp wallaby, Wallabia bicolor (Marsupialia)

Thirty-five swamp wallabies from Victoria, New South Wales and Queensland, Australia were examined for parasites. Thirty-nine species of nematodes, five species of cestodes and eight species of arthropods were found. Wallabies from Queensland and northern New South Wales had a less diverse helminth fauna (23 species) than did wallabies from southern New South Wales and Victoria (32 species). Rugopharynx spp. and Cloacina spp. occurred in large numbers in the stomach but provoked no pathological changes. Known pathogenic species (Globocephaloides trifidospicularis and Hypodontus macropi) were encountered in small numbers only and did not produce any lesions. Pathological changes associated with parasites were: gastric nodules associated with Labiostrongylus clelandi and Parazoniolaimus collaris, bronchopneumonia due to Marsupostrongylus spp., biliary fibrosis associated with Progamotaenia festiva and fibrous peritonitis, pleuritis, pericarditis and eosinophilic splenitis due to Breinlia mundayi. Echinococcus granulosus was the only parasite found which also occurs in domestic animals.     

Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. I. The Colorado checkered whiptail (Cnemidophorus tesselatus)

Eleven of 27 (41%) parthenogenetic Colorado checkered whiptails (Cnemidophorus tesselatus) from four counties of western and southwestern Texas were infected with one or more helminths. These included a linstowiid cestode (Oochoristica sp.), a larval spirurid nematode (Physaloptera sp.) and two species of oxyurid nematodes (Parathelandros texanus and Pharyngodon warneri). This note, the first in a series of reports on helminths of Cnemidophorus spp., represents the first record of parasites from C. tesselatus.     

Gastrointestinal parasites of the grasscutter (Thryonomys swinderianus, Temminck 1827) on the Accra Plains of Ghana

The gastrointestinal parasites of the grasscutter were investigated between 1996 and 2006 using 180 grasscutters from the Accra Plains. The aim of the study was to develop strategies for the control of the parasites under captive management. The gastrointestinal tracts of the animals were examined for the presence of both helminth and protozoan parasites with the aid of a hand lens, the direct smear and Willis Flotation techniques. In all, fourteen species of helminths were found including twelve nematodes and two cestodes. Trichuris muris was the most common nematode encountered, whilst Hepatocola hepatica was the least commonly encountered nematode. Three genera of protozoans, viz, Trichomonas spp, Giardia spp and Eimeria spp were also encountered, with Giardia spp and Trichomonas spp being reported for the first time in the grasscutter. Eimeria spp were the most prevalent protozoa. The widespread occurrence of protozoal and helminthic parasites in the grasscutter suggests that routine treatment of grasscutters with coccidiostats, anti-flagellates and anthelminthics such as dimetridazole and albendazole may contribute significantly to improve productivity of animals and reduce the pressure on wild populations.     

Zoonotic and human parasites of inhabitants of Cueva de los Muertos Chiquitos, Rio Zape Valley, Durango, Mexico

We present the first reconstruction of the parasitoses among the people of the Loma San Gabriel culture, as represented by 36 coprolites excavated from the Cueva de los Muertos Chiquitos in Durango, Mexico. The coprolites date to approximately 1,400-yr-ago. Species identified based on eggs recovered include the trematode Echinostoma sp., the tapeworms Hymenolepis sp. and Dipylidium caninum , and the nematodes Ancylostoma duodenale, Enterobius vermicularis, and Trichuris trichiura. After rehydration and screening, 2 methods were used to recover eggs from these samples including spontaneous sedimentation and flotation. Samples were analyzed by 3 different laboratories for independent verification and comparison of methods. Spontaneous sedimentation resulted in the discovery of hymenolepidid eggs that were not found with flotation. Sedimentation was a more-sensitive indicator of prevalence as well. The modified method of flotation permitted estimation of egg concentration and resulted in the detection of a few specimens not found by sedimentation. The results of both methods showed that 19 (of 36) coprolites contained helminth eggs. Our results detected the presence of pathogenic helminths including hookworms and whipworms. The cestodes found do not cause severe pathology in humans. The early dates of hookworm and whipworm, relative to other findings in the southwest United States, indicate that these parasites arrived relatively late in prehistory in Arizona and New Mexico, probably moving into the area with travelers from Mesoamerica.     

A comparative analysis of the helminth fauna of kittiwake Rissa tridactyla (Linnaeus, 1758) and glaucous gull Larus hyperboreus Gunnerus, 1767 from different parts of the Barents Sea

The article is based on the results of helminthological observations made on kittiwake Rissa tridactyla and glaucous gull Larus hyperboreus in 1991-2001 in different areas of the Barents Sea (Eastern Murman coast, Franz Josef Land, Novaya Zemlya, Spitzbergen). 18 helminth species (2 trematodes, 11 cestodes, 4 nematodes, and 2 acanthocephalans) were recorded in the kittiwakes and 19 (3 trematodes, 9 cestodes, 5 nematodes and 2 acanthocephalans) species were recorded in the glaucous gulls. Trematodes were absent in the birds collected at the Franz Josef Land and the northern island of Novaya Zemlya. 3 trematode species, namely Gymnophallus sp. (somateria?), Microphallus sp. 1 (M. pseudopygmaeus), and Cryptocotyle lingua were found in the glaucous gulls of western Spitzbergen. It was supposed that the life cycles of these parasites can be completed there. On the other hand, coastal ecosystems of Arctic archipelagoes turn out to be favourable for the transmission of some cestodes. This is closely connected with the regional traits in the marine bird diet, namely the increase of the amphipod (intermediate hosts of hymenolepidids and some dilepidids) and polar cod (supposed second intermediate host for some tetrabothriids) portion in Arctic. As a result, cestodes are the base of the helminth fauna of kittiwakes and glaucous gulls of the Barents Sea, by their species richness, prevalence and abundance. Nematodes and acanthocephalans were represented by a few species with low infection intensity. The main ecological factors affected the regional difference in the species richness and abundance of the helminths parasitising kittiwakes and glaucous gulls in the Barents Sea are proposed. Those are regional climatic features and regional traits in the behaviour and food priorities of birds, and also the distribution of the helminths intermediate hosts, invertebrates and fishes. The phenomenon of host specificity lowering with respect to the definitive host was recorded in some cestode species (Microsomacanthus diorchis, M. microsoma, and Arctotaenia tetrabothrioides) on the border of their distribution ranges, the coastal ecosystems of Arctic.     

A gastropod scavenger serving as paratenic host for larval helminth communities in shore crabs

The whelk Cominella glandiformis is an important predator-scavenger of New Zealand intertidal ecosystems; a few whelks can quickly eat all the soft tissues of recently dead crabs. In this study, we demonstrate that whelks can also ingest and act as paratenic hosts for at least 4 helminth species that use crabs as intermediate hosts: metacercariae of the trematode Maritrema sp. and of another unidentified trematode, larval acuariid nematodes, and cystacanths of the acanthocephalans Profilicollis spp. Large whelks ingest disproportionately more helminth larvae than small whelks, but the survival of parasites during their short stay in the whelks is not affected by whelk size. The majority of metacercariae and nematodes are passed out in whelk feces within 3 days of ingestion, whereas the few cystacanths found did not leave whelks until after that time; no parasite was left in whelks 5 days postingestion. Survival of all 4 helminth species was generally very high, though it decreased day by day in 2 species. Given that the avian definitive hosts of all 4 helminths also eat whelks, our results indicate that alternative transmission pathways exist and that parasites can take routes through food webs that are too often ignored.     

A survey in Louisiana of intestinal helminths of ponies with little exposure to anthelmintics

Ponies reared with minimal or no exposure to anthelmintics were surveyed for intestinal helminths in order to estimate prevalence and intensity of parasite populations unaltered by frequent exposure to anthelmintics. Thirty-seven mixed breed ponies of varying ages were examined. Thirty-four species of nematodes and 2 species of cestodes were found. Twenty-four of the nematode species (including 1 new species) were in the subfamily Cyathostominae (small strongyles). Eighty-seven percent of the total burden of adult small strongyles in the large intestine was composed of 10 species. By comparing the results of the present survey with those of recent surveys of horses from herds which had been subjected to treatments with anthelmintics, the effect of prolonged usage of anthelmintic treatment on the prevalence of individual species possibly can be estimated. The general ranking of the 10 most common cyathostome species was similar to those described in recent surveys of horses, suggesting that anthelmintic pressure does not affect the prevalence of most cyathostome species. The lack of anthelmintic treatment appeared not to affect prevalence rates for Anoplocephala perfoliata and Anoplocephala magna when compared to other studies. Conversely, prevalence rates for Strongylus spp., Triodontophorus spp., Craterostomum acuticaudatum, Oxyuris equi, and Parascaris equorum were higher than those reported for these species in recent studies of horses.     

Parasites in social subterranean Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia)

Three out of 18 examined common mole-rats ( Cryptomys sp., Xkaryotype 2n = 58) from Zambia were infested with cestodes ( Inermicapsifer nmdagascariensis and an undetermined species) and a nematode ( Protospirura muricola ). Four out of 14 examined Zambian giant mole-rats ( Cryptomys mechowi ) hosted cestodes ( Raillietina (R) sp. and an undetermined species) and nematodes ( Protospirura muricola, Capillaria sp.). Helminths and circumstances of findings are briefly described. No ectoparasites were found. The influences of subterranean and social way of life and feeding habits upon occurrence of parasites in mole-rats are discussed. Burrow conditions and social behaviour seem not to favour infestation by parasites.     

Gastrointestinal parasites of the colobus monkeys of Uganda

From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of Uganda-the endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (C. angolensis)--to identify and determine the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Coprocultures facilitated identification of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes.     

The prevalence and diversity of intestinal parasitic infections in humans and domestic animals in a rural Cambodian village

In Cambodia, intestinal parasitic infections are prevalent in humans and particularly in children. Yet, information on potentially zoonotic parasites in animal reservoir hosts is lacking. In May 2012, faecal samples from 218 humans, 94 dogs and 76 pigs were collected from 67 households in Dong village, Preah Vihear province, Cambodia. Faecal samples were examined microscopically using sodium nitrate and zinc sulphate flotation methods, the Baermann method, Koga Agar plate culture, formalin-ether concentration technique and Kato Katz technique. PCR was used to confirm hookworm, Ascaris spp., Giardia spp. and Blastocystis spp. Major gastrointestinal parasitic infections found in humans included hookworms (63.3%), Entamoeba spp. (27.1%) and Strongyloides stercoralis (24.3%). In dogs, hookworm (80.8%), Spirometra spp. (21.3%) and Strongyloides spp. (14.9%) were most commonly detected and in pigs Isospora suis (75.0%), Oesophagostomum spp. (73.7%) and Entamoeba spp. (31.6%) were found. Eleven parasite species were detected in dogs (eight helminths and three protozoa), seven of which have zoonotic potential, including hookworm, Strongyloides spp., Trichuris spp., Toxocara canis, Echinostoma spp., Giardia duodenalis and Entamoeba spp. Five of the parasite species detected in pigs also have zoonotic potential, including Ascaris spp., Trichuris spp., Capillaria spp., Balantidium coli and Entamoeba spp. Further molecular epidemiological studies will aid characterisation of parasite species and genotypes and allow further insight into the potential for zoonotic cross transmission of parasites in this community.     

Helminth associations in white-toothed shrews Crocidura russula (Insectivora: Soricidae) from the Albufera Natural Park, Spain

The helminths of 218 white-toothed shrews from 29 sites in 2 biotopes in the Albufera Natural Park (Valencia, Spain) were examined from July 1990 to August 1991. An association analysis of helminths occurring at a prevalence of more than 4% was carried out for 4 species of cestodes located in the intestine (Hymenolepis pistillum, H. scalaris, H. tiara, and Pseudhymenolepis redonica) and 3 species of nematodes (Pseudophysaloptera sp. located in the stomach, Stammerinema rhopocephala larvae in the intestine and abdominal cavity, and Porrocaecum sp. in the thoracic and abdominal cavities). Bivariate (species pairs) versus multivariate analyses (associations within the entire set of species) were performed of presence-absence and of quantitative records (influence of intensity on associations). The associations were evaluated with respect to the sex and age of the host and to the sampling date and sites. The host and environment played a limited role, and the major determinant of species assemblage was phylogenetic. Positive associations were found among both the cestodes and the nematodes, whereas negative associations were found between cestodes and nematodes. The type of life cycle was probably the second greatest determinant of species associations. Nematodes using shrews as a paratenic host or as their definitive host were both positively associated.     

Parasites with zoonotic potential found in commercially important fish in Tamaulipas,Northeastern Mexico

Human population is exposed to numerous parasitic ichthyozoonoses. Although Tamaulipas state (northeastern Mexico) is well known for its fishing and aquaculture industry, there are few reports of this type of zoonosis. Therefore, it is imperative to investigate whether the parasites that affect these fish may represent a zoonotic risk for the inhabitants of the area.The objective of this study was to identify molecular and/or morphologically muscle parasites of fish from coastal locations in Tamaulipas, Mexico, and assess the risk of infection for humans. Between 2017 and 2018, 764 individual fish belonging to 28 species were examined for parasites. Collected worms were processed for their identification using morphological characteristics. In addition, partial sequences of the large subunit (28S) ribosomal RNA gene were obtained from some species to corroborate their identity. Prevalence and mean intensity of all registered infections were calculated. A total of seven species of parasites were found: cestodes (Poecilancistrium caryophyllum), trematodes (Clinostomum tataxumui, Clinostomum cichlidorum), nematodes (Eustrongylides sp., Contracaecum sp.) and pentastomids (Sebekia purdieae, Sebekia sp.). Parasites infected 10 species belonging to different fish families (Ariidae, Centrarchidae, Centropomidae, Cichlidae, Eleotridae, Ictaluridae, Mugilidae and Sciaenidae). Congeneric species of parasites or related to those registered in this study have been identified as zoonotic agents in other regions of the world. Despite the low levels of infection (2.6–16.6% prevalence and 1–5.5 parasites per infected host), there is a latent risk of transmission to humans, so it is recommended to avoid eating raw or undercooked fish meat.     

Studies of disease in the Red fox (Vulpes vulpes) in Northern Ireland

Some 720 foxes were examined for signs of disease and parasites, incidental to an intensive ecological study. The epifauna, skin infections, intestinal helminths and lesions of internal organs are described and rates of infection given. Important diseases included sarcoptic mange, which is a major debilitating factor and probably a fatal infection. Leptospirosis was common, antibodies were recorded in the blood, and chronic interstitial nephritis was a frequent condition of the kidneys. The nematodes Uncinaria stenocephala and Toxocara spp. were often present as parasites of the alimentary canal and may be a mortality factor in cubs. The cestodes and ectoparasites alone would appear to be of little importance and largely reflect the diet of the fox.     

Molecular characterization of Trichuris spp. from captive animals based on mitochondrial markers

Monoxenous parasites may easily infect animals in captivity, and nematodes belonging to the genus Trichuris are commonly reported in zoological gardens worldwide. Infections in captive animals should be accurately monitored and the characterization of pathogens is highly advisable, as a tool to infer possible routes of intra- and interspecific transmission pathways and to assess the related zoonotic potential. Whipworms are usually identified on the basis of few morphological features of adults males and eggs and by an host-affiliation criterion. Given the strong morphological convergence of adaptive traits and the possible occurrence of hybridization and/or cross-infections events, the use of molecular methods is of great utility.Here, we analysed two partial mitochondrial loci, the cytochrome c oxidase I and the cytochrome b regions, in Trichuris spp. infecting four animal species hosted in the Bioparco Zoological Garden of Rome. Results from molecular systematics, compared to previous data, suggested that the five Trichuris taxa recovered were well separated, showing a significant degree of host affiliation (herbivorous, primates/swine and rodents/canids). The screw horn antelopes and the camels were infected with two variants of Trichuris ovis; Trichuris sp. similar to those observed in rodents from South America was infecting the Patagonian maras. Moreover, Trichuris from the ring-tailed lemur showed a great similarity to Trichuris infecting the Japanese macaque previously analysed from the same zoological garden, and clustering together with Trichuris trichiura, posing a potential zoonotic threat for visitors and workers.     

Molecular phylogenetic analysis of the genus Strongyloides and related nematodes

Strongyloides spp., parasitic nematodes of humans and many other terrestrial vertebrates, display an unusual heterogonic lifecycle involving alternating parasitic and free-living adult reproductive stages. A number of other genera have similar lifecycles, but their relationships to Strongyloides have not been clarified. We have inferred a phylogeny of 12 species of Strongyloides, Parastrongyloides, Rhabdias and Rhabditophanes using small subunit ribosomal RNA gene (SSU rDNA) sequences. The lineage leading to Strongyloides appears to have arisen within parasites of terrestrial invertebrates. Inferred lifecycle evolution was particularly dynamic within these nematodes. Importantly, the free-living Rhabditophanes sp. KR3021 is placed within a clade of parasitic taxa, suggesting that this species may represent a reversion to a non-parasitic lifecycle. Species within the genus Strongyloides are very closely related, despite the disparity of host species parasitised. The highly pathogenic human parasite Strongyloides fuelleborni kelleyi is not supported as a subspecies of the primate parasite S. fuelleborni fuelleborni, but is most likely derived from a local zoonotic source.     

Helminths of California quail (Callipepla californica) and mountain quail (Oreortyx pictus) in western Oregon

Eighty California quail (Callipepla californica), collected from the E. E. Wilson Wildlife Area near Monmouth, Oregon (USA) during a 22 mo period, were examined for gastrointestinal helminths. Eight birds were infected with three species of nematodes, Heterakis isolonche, Dispharynx nasuta, and Capillaria sp., and two species of cestodes, Rhabdometra odiosa and Davainea sp. Except for D. nasuta, prevalence did not exceed 5% despite mesic conditions in the collection area. Two mountain quail (Oreortyx pictus) were collected from Lane County, Oregon (USA), near Blue River Reservoir; both were infected with the nematode Trichostrongylus tenuis.     

Studies of endoparasites of the mourning dove (Zenaida macroura) in the southeast United States.

From September, 1973, through November, 1974, 255 mourning doves (Zenaida macroura) were collected in the southeastern United States and examined for endoparasites. Thirteen species of endoparasites were found and included six species of protozoans, one trematode, two cestodes, and four nematodes. New host records included Sarcocystis sp., Echinostoma revolutum, Hymenolepis sp., Aproctella stoddardi, Ascaridia columbae, and Dispharynx nasuta.