First evidence of enterobiasis in ancient Egypt

The oldest and most common parasite for which we have direct evidence, in the New World, is Enterobius vernicularis. Numerous archaeological sites, especially in the arid American southwest, have yielded fecal samples positive for pinworm ova, some of these dating back 10,000 yr. Reports of pinworm from the Old World are scarce. This article reports the first evidence of pinworm infection from Roman-occupied (30 BC-AD 395) Egypt.     

SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites

Enterobius vermicularis, pinworm, is one of the most common helminths worldwide, infecting nearly a billion people at all socio-economic levels. In prehistoric populations the paleoparasitological findings show a pinworm homogeneous distribution among hunter-gatherers in North America, intensified with the advent of agriculture. This same increase also occurred in the transition from nomad hunter-gatherers to sedentary farmers in South America, although E. vermicularis infection encompasses only the ancient Andean peoples, with no record among the pre-Colombian populations in the South American lowlands. However, the outline of pinworm paleoepidemiology has been supported by microscopic finding of eggs recovered from coprolites. Since molecular techniques are precise and sensitive in detecting pathogen ancient DNA (aDNA), and also could provide insights into the parasite evolutionary history, in this work we have performed a molecular paleoparasitological study of E. vermicularis. aDNA was recovered and pinworm 5S rRNA spacer sequences were determined from pre-Columbian coprolites (4110 BC-AD 900) from four different North and South American archaeological sites. The sequence analysis confirmed E. vermicularis identity and revealed a similarity among ancient and modern sequences. Moreover, polymorphisms were identified at the relative positions 160, 173 and 180, in independent coprolite samples from Tulán, San Pedro de Atacama, Chile (1080-950 BC). We also verified the presence of peculiarities (Splicing leader (SL1) RNA sequence, spliced donor site, the Sm antigen biding site, and RNA secondary structure) which characterise the SL1 RNA gene. The analysis shows that the SL1 RNA gene of contemporary pinworms was present in pre-Columbian E. vermicularis by 6110 years ago. We were successful in detecting E. vermicularis aDNA even in coprolites without direct microscopic evidence of the eggs, improving the diagnosis of helminth infections in the past and further pinworm paleoepidemiological studies.     

Transmission of Dientamoeba fragilis: evaluation of the role of Enterobius vermicularis

The role of Enterobius vermicularis in the transmission of Dientamoeba fragilis has been evaluated in two groups of patients admitted to the Parasitology Laboratory of Celal Bayar University: one group with E. vermicularis infection (n=187, Pinworm Group), and the other with D. fragilis infection (n=126, Dientamoeba Group). The presence of the other parasite, pinworm or Dientamoeba, was investigated with the microscopic examination of cellophane tape and stool samples for three consecutive days. In the Pinworm Group, 9.6% of the patients were found to be coinfected with D. fragilis, while 25.4% of the patients in the Dientamoeba Group were found to be coinfected with pinworms. The coincidence rates of D. fragilis and E. vermicularis, higher than the prevalence of each parasite in similar populations, suggest a common relation between these two parasites, possibly in entering the human body. E. vermicularis infection was found to be significantly more common in younger children (p<0.001), indicating that younger children may also be at higher risk for D. fragilis infection. These findings also raise the question of whether the unrelated symptoms of the pinworm infected patients such as abdominal pain and diarrhea may actually be due to overlooked Dientamoeba infections.     

Negligible Egg Positive Rate of Enterobius vermicularis and No Detection of Head Lice among Orphanage Children in Busan and Ulsan,Korea (2014)

To determine whether pinworm infections and head lice infestations spread among children in orphanages, 117 children from 4 orphanages in Busan-si and Ulsan-si, Korea, were examined for enterobiasis and head lice infestation between January and February 2014. The overall rate of Enterobius vermicularis egg positivity was 0.85%, whereas none of the children had head lice infestations. The rate of pinworm infection was much lower among the orphanage children compared to the rates observed in previous studies among kindergarten and primary school students. Moreover, the risk factors for enterobiasis were less frequent among these subjects than previously reported. The personal hygiene and health of the orphanage children were supervised by a regular, employed nurse through a health education program. In conclusion, pinworm infection was efficiently controlled among the children in orphanages, and this might be related to good personal hygiene practices in Korea.     

Growth of Enterobius vermicularis in a chimpanzee after anthelmintic treatment

The growth of Enterobius vermicularis in a chimpanzee was investigated by observing worms discharged in feces after administration of pyrantel pamoate. Just after the final molting, immature adult male pinworms developed to a fully mature stage in 2 wk, after passing through a stage corresponding to the so-called Enterobius gregorii, which was surmised to be a younger adult form of E. vermicularis. The frequency distribution of body length forms 2 peaks in both male and female pinworms, with a depression in the transitional forms from the immature to the fully mature stage.This depression seems to be the result of more rapid growth or lower susceptibility to the drug in this transitional stage. Pyrantel pamoate effectively eradicated mature males, but gravid females were continuously observed in the feces after treatment. The complete eradication of pinworm infection by pyrantel pamoate could be achieved by repeated treatment at intervals shorter than 2 wk. This treatment would eradicate male worms first, resulting in females producing only unfertilized eggs, from which only males might hatch.     

Prevalence of Enterobius vermicularis Infection among Preschool Children in Kindergartens of Taipei City, Taiwan in 2008

The prevalence of Enterobius vermicularis infection among preschool children was reported to be low based on a 5-year screening program in Taipei City, Taiwan. The Taipei City government intended to terminate the E. vermicularis screening program among preschool children. Thus, we were entrusted with confirming whether pinworm infections among preschool children in Taipei City had truly declined. From each of 12 administrative districts 2-3 kindergartens were randomly selected for investigation. In total, 4,349 children were examined, of which 2,537 were boys and 1,812 were girls. The cellophane tape adhered to a glass slide was used, and all examinations were done by certified medical technologists. Results indicated that the overall prevalence rate of pinworm infections was 0.62% (27/4,349). Although the infection rate was higher among boys (0.67%, 17/2,537) than in girls (0.55%, 10/1,812), no significant difference was found (χ² = 0.399, P = 0.62). According to the administrative district, the infection rate ranged from no positive cases of E. vermicularis infection in the Xinyi, Zhongzhen, and Wanhua Districts (0%; 0/299, 0/165, and 0/358, respectively), to 0.26% (1/131) in Songshan District, with the highest rate of 1.88% (7/373) in Wenshan District. Because the overall infection rate (0.62%, 27/4,349) in the present study was unchanged compared to that (0.40%, 197/49,541) previously reported in 2005, we propose that regular pinworm screening and treatment programs should be continued in some parts of Taipei City.     

Egg positive rate of Enterobius vermicularis among preschool children in Cheongju, Chungcheongbuk-do, Korea

In an attempt to determine the prevalence of pinworm infection, the egg positive rate of Enterobius vermicularis was examined using the adhesive cello-tape anal swab method in 1,512 preschool children sampled from a total of 20 kindergartens in Cheongju city, in November to December of 2004 (951 children from 13 kindergartens) and September to October of 2005 (561 from 7 kindergartens). The overall egg positive rate was found to be 7.9% (119/1,512); 9.3% (73/784) for boys and 6.3% (46/728) for girls, respectively. The 5-year age group evidenced the highest egg positive rate (10.9%, 47/430) among the examined age groups. As compared to those reported from previous works (ranged from 9.2 to 26.1%), the prevalence of E. vermicularis in the Cheongju city area is relatively low.     

Enterobius vermicularis eggs discovered in coprolites from a medieval Korean mummy

While the presence of pinworm eggs in archaeological samples has been reported by many researchers in the New World, those have been detected very scarcely in the Old World, especially in East Asian countries. In fact, many parasite species were recovered from the archeological remains in Korea, eggs of Enterobius vermicularis had not been found. Recently, a female mummy buried in the 17th century was discovered in the Joseon tomb from Dangjin-gun, Chungcheongnam-do, Korea. After rehydration process for 12 days, investigations were carried on the luminal surface of the colon. From them, 3 eggs of E. vermicularis were recovered. They were elliptical, transparent with a thin egg shell, 50.3±5.2 μm (length) and 28.2±3.9 μm (width) in size. This is the first discovery of E. vermicularis eggs in East Asia.     

The finding of Enterobius vermicularis eggs in pre-Columbian human coprolites

Enterobius vermicularis eggs were found in human coprolites collected in the archaeological site of Caserones, Tarapaca Valley, Chile, dating from 400 BC to 800 AD. The human pinworm had already been found in other pre-historic archaeological sites in America, and its introduction in this continent is discussed.     

Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park,Tanzania

The release of any species into a novel environment can evoke transmission of parasites that do not normally parasitize the host as well as potentially introducing new parasites into the environment. Species introductions potentially incur such risks, yet little is currently known about the parasite fauna of introduced primate species over the long term. We describe the results of long‐term monitoring of the intestinal parasite fauna of an unprovisioned, reproducing population of chimpanzees introduced 40 years earlier (1966–1969) onto Rubondo Island in Lake Victoria, Tanzania, a non‐native habitat for chimpanzees. Two parasitological surveys (March 1997–October 1998 and October 2002–December 2005) identified Entamoeba spp. including E. coli, Iodamoeba buetschlii, Troglodytella abrassarti, Chilomastix mesnili, Trichuris sp., Anatrichosoma sp., Strongyloides spp., Strongylida fam. gen. sp., Enterobius anthropopitheci, Subulura sp., Ascarididae gen. sp., and Protospirura muricola. The parasite fauna of the Rubondo chimpanzees is similar to wild chimpanzees living in their natural habitats, but Rubondo chimpanzees have a lower prevalence of strongylids (9%, 3.8%) and a higher prevalence of E. anthropopitheci (8.6%, 17.9%) than reported elsewhere. Species prevalence was similar between our two surveys, with the exception of Strongyloides spp. being higher in the first survey. None of these species are considered to pose a serious health risk to chimpanzees, but continued monitoring of the population and surveys of the parasitic fauna of the two coinhabitant primate species and other animals, natural reservoir hosts of some of the same parasites, is important to better understand the dynamics of host–parasite ecology and potential long‐term implications for chimpanzees introduced into a new habitat. Am. J. Primatol. 72:307–316, 2010. © 2009 Wiley‐Liss, Inc.     

Redescription of Enterobius anthropopitheci (Gedoelst, 1916) (Nematoda,Oxyurida), a parasite of chimpanzees

Enterobius anthropopitheci (Gedoelst, 1916), a parasite of the chimpanzees Pan troglodytes and P. paniscus, is redescribed. E. anthropopitheci can be distinguished from the two closely related species parasitic in man, E. vermicularis (L., 1758) and E. gregorii Hugot, 1983, by the following characters: in the males, the cuticular pericloacal ornamentation, and the size and shape of the spicule; in the females, the lateral alae, which are simple in the pinworms of man, are simple only anteriorly and divided into two crests at the mid-oesophageal level in the parasite of chimpanzees. Enterobius anthropopitheci (Gedoelst, 1916), parasite des chimpanzés, Pan troglodytes et P. paniscus, dans toute leur aire de répartition est redécrite. E. anthropopitheci est très proche par sa morphologie des deux oxyures de l'Homme, E. vermicularis (L., 1758) et E. gregorii Hugot, 1983, dont il diffère toutefois par les caractères suivants: chez le mâle, ornementation cuticulaire péricloacale, taille et forme du spicule; chez la femelle, aile latérale simple sur toute sa longuer chez les oxyures de l'Homme, simple dans la région antérieure se dédoublant en deux crêtes au milieu de l'oesophage, chez l'oxyure parasite des chimpanzés.     

Intestinal parasite infections at an institution for the handicapped in Korea

Stool and cellotape anal swab examinations were carried out in August 1997 on handicapped people at an institution located in Chorwon-gun, Kangwon-do, Korea. A total of 112 stool samples (78 males and 34 females) revealed three cases of Trichuris trichiura infection and one case of Enterobius vermicularis infection. Other helminth eggs were not detected. The overall prevalence rate was 35.7% (38.5% for males and 29.4% for females). More than two different kinds of parasites were found in 42.0% of the positive stool samples (17 cases). The infection rates for protozoan cysts are as follow: Entamoeba coli (25.0%), E. histolytica (1.8%), Endolimax nana (21.4%), Iodoamoeba bütschlii (1.8%) and Giardia lamblia (0.9%). In cellotape anal swab examinations (165 samples), the prevalence rate of E. vermicularis was 20.6% (25.7% of males and 9.6% of females). In conclusion, the handicapped people in the institution showed higher infection rates of protozoan parasites and E. vermicularis, possibly due to more accessibility to the infection.     

A case of maxillary sarcoma in a chimpanzee (Pan troglodytes)

Oral malignancy is rare in chimpanzees. A 34‐year‐old female chimpanzee (Pan troglodytes) at Kumamoto Sanctuary, Japan, had developed it. Treatment is technically difficult for chimpanzees while malignant neoplasm is seemingly rising in captive populations. Widespread expert discussion, guidelines for treatment, especially for great apes in terminal stages is urgently needed.     

Effects of repeated anthelmintic treatment on Enterobius vermicularis infection in chimpanzees

Effects of repeated treatment with pyrantel pamoate on Enterobius vermicularis infection in chimpanzees were assessed by observing worms discharged in the feces after administration of anthelmintic treatment. Three of 9 chimpanzees reared in a zoological garden in Japan were subjected to fecal worm count and morphometric observation, and all were given oral pyrantel pamoate 6 times at 10-day intervals simultaneously. Following the first and second treatments, more than 30,000 pinworms were discharged from 1 chimpanzee. The number of discharged worms abruptly decreased after the third treatment, and only a few worms were recovered after the fifth treatment, indicating that repeated treatment at short intervals was very effective. Complete eradication was not achieved, however, presumably because of reinfection. The female proportion among discharged worms tended to increase as the treatment was repeated.     

Egg positive rate of Enterobius vermicularis of primary school children in Geoje island

The status of pinworm (Enterobius vermicularis) egg positive rate of primary school children in Geoje island was investigated by using adhesive cellotape anal swap method, in September, 2002. Total egg positive rates of E. vermicularis were 9.8% (74/754) and those of male and female were 10.8% and 8.7%, respectively. Among three schools examined, Myeongsa primary school showed the highest egg positive rate (12.6%) followed by Yeoncho [9.8% (26/266)] and Geoje [9.1% (35/385)]. As for the age groups, the 2nd grade had the highest egg positive rate (15.3%), whereas the 5th grade showed the lowest egg positive rate (2.6%). The above result led us to confirm that the egg positive rates of E. vermicularis in primary school children in Geoje island were not significantly different from the those in the whole country including urban and rural areas, showing more than 10%.     

Temporal and Spatial Distribution of Enterobius vermicularis (Nematoda: Oxyuridae) in the Prehistoric Americas

Investigations of Enterobius sp. infection in prehistory have produced a body of data that can be used to evaluate the geographic distribution of infection through time in the Americas. Regional variations in prevalence are evident. In North America, 119 pinworm positive samples were found in 1,112 samples from 28 sites with a prevalence of 10.7%. Almost all of the positive samples came from agricultural sites. From Brazil, 0 pinworm positive samples were found in 325 samples from 7 sites. For the Andes region, 22 pinworm positive samples were found in 411 samples from 26 sites for a prevalence of 5.3%. Detailed analyses of these data defined several trends. First, preagricultural sites less frequently show evidence of infection compared to agricultural populations. This is especially clear in the data from North America, but is also evident in the data from South America. Second, there is an apparent relationship between the commonality of pinworms in coprolites and the manner of constructing villages. These analyses show that ancient parasitism has substantial value in documenting the range of human behaviors that influence parasitic infections.     

野生太行猕猴肠道寄生虫感染的初步调查

为了解野生太行猕猴(Macaca mulatta tcheliensis)肠道寄生虫感染情况,采用饱和蔗糖溶液漂浮法、改良抗酸染色法和卢戈碘液染色法对194份粪便样品进行检查,结果共检查出阿米巴原虫(Amoebasp.)、等孢球虫(Isospora sp.)、鞭虫(Trichuris sp.)、圆线虫(Strongylid sp.)、泡翼线虫(Physaloptera sp.)、蛲虫(Enterobius叩.)、蛔虫(Ascarid sp.)7种寄生虫.寄生虫总感染率为97.4%,线虫感染率为93.8%.其中,鞭虫感染率最高,为91.2%;阿米巴原虫和圆线虫次之,分别为67.5%和60.8%.寄生虫混合感染率为87.1%;鞭虫、泡翼线虫、圆线虫3种线虫混合感染率为71%,同时感染其中2种的占42%,同时感染3种的占29%.对鞭虫卵、圆线虫卵和泡翼线虫卵进行感染强度测定,92%以上阳性样品线虫卵的EPG值在2 000以下.等孢球虫为非人灵长类国内新发现种;所检出寄生虫中,阿米巴原虫、鞭虫、泡翼线虫、蛲虫、蛔虫均可感染人,因此具有重要的公共卫生意义.     

The mitochondrial genome sequence of Enterobius vermicularis (Nematoda: Oxyurida)--an idiosyncratic gene order and phylogenetic information for chromadorean nematodes

The complete mitochondrial genome sequence was determined for the human pinworm Enterobius vermicularis (Oxyurida: Nematoda) and used to infer its phylogenetic relationship to other major groups of chromadorean nematodes. The E. vermicularis genome is a 14,010-bp circular DNA molecule that encodes 36 genes (12 proteins, 22 tRNAs, and 2 rRNAs). This mtDNA genome lacks atp8, as reported for almost all other nematode species investigated. Phylogenetic analyses (maximum parsimony, maximum likelihood, neighbor joining, and Bayesian inference) of nucleotide sequences for the 12 protein-coding genes of 25 nematode species placed E. vermicularis, a representative of the order Oxyurida, as sister to the main Ascaridida+Rhabditida group. Tree topology comparisons using statistical tests rejected an alternative hypothesis favoring a closer relationship among Ascaridida, Spirurida, and Oxyurida, which has been supported from most studies based on nuclear ribosomal DNA sequences. Unlike the relatively conserved gene arrangement found for most chromadorean taxa, E. vermicularis mtDNA gene order is very unique, not sharing similarity to any other nematode species reported to date. This lack of gene order similarity may represent idiosyncratic gene rearrangements unique to this specific lineage of the oxyurids. To more fully understand the extent of gene rearrangement and its evolutionary significance within the nematode phylogenetic framework, additional mitochondrial genomes representing a greater evolutionary diversity of species must be characterized.