Hymenolepis nana: Survival in the immunized mouse

Mice initially infected with Hymenolepis nana eggs became completely immune to challenge with mouse-derived cysticercoids (cysts) after more than 10 days. The host possessed at least two separated immune responses, one directed exclusively against reinfection with eggs (early response) and the other against cyst infection (late response). In two different mouse strains the responses showed markedly different duration both for the time lag prior to acquisition of the late response and for the survival of the initially infected worms, but were otherwise similar. The mice became immune to adult tapeworms and expelled the initially infected, destrobilated worms; this third immune response determines the longevity of H. nana in the mouse host. Thus, there is a strong indication that H. nana successively changes its immunogenicity during development, each stage stimulating immunity after a time lag. It is possible that the longevity of H. nana in a mouse strain depends on the length of time prior to acquisition of immune responses directed not against the tissue stage (early response), but against the lumen stages (late response and worm expulsion response).     

Development of human and mouse strain of Hymenolepis nana in mice

Ferretti G., Gabriele F. and Palmas C. 1981. Development of human and mouse strain of Hymenolepis nana in mice. International Journal for Parasitology11: 425–430. An Hymenolepis nana strain isolated from human faeces was transferred in the mouse. At first, the q ratio (the number of parasites to the number of eggs used) was very low. After 10 passages adaptation was complete: when mice of different age and strain (CD₁ and BDF₁) were infected with eggs of the above strain and eggs of 2 different murine strains, no differences emerged in the q ratio or in the parasite mean dry weight. Survival also appeared the same in the 3 parasite strains, however, human and murine strains live for a shorter time in BDF₁ than in CD₁ mice. Discussion bears on the hypothesis that the difficulties that emerge during the first passages may be connected to the adult and not to the larval phase.     

Interactions between Trichinella spiralis and Hymenolepis nana in the intestine of the mouse

Ferretti G., Gabriele F., Palmas C. and Wakelin D. 1984. Interactions between Trichinella spiralis and Hymenolepis nana in the intestine of the mouse. International Journal for Parasitology14: 29–33. The rejection of the intestinal phase of Trichinella spiralis in outbred CD₁ mice is associated with an inflammatory response. The effects of this inflammation were studied in mice concurrently infected with an unrelated parasite, Hymenolepis nana, which stimulates a slight inflammation but is also immunologically rejected by this strain of mice. Moreover though Cd(In)1 mice seem to be ‘slow responders’, in concurrent infections with T. spiralis and H. nana there was a marked effect upon the cesode survival. At the highest level of T. spiralis infection, H. nana failed to establish at all. On the other hand, if 300 T. spiralis were administered 10 weeks earlier, H. nana become established in all mice and the distribution of parasites suggests that immunodepression is involved. An accelerated loss of the nematode, when H. nana was present, was also demonstrated. There was no evidence of any reciprocal or specific cross-immunity between the two parasites.     

Hymenolepis nana: Protective immunity against mouse-derived cysticercoids induced by initial inoculation with eggs

Mice were almost completely resistant to a mouse-derived cysticercoid (cyst) challenge after 6 to 10 months following an initial immunizing inoculation with eggs of Hymenolepis nana. Previously uninfected control mice of the same age became infected with the cyst-derived tapeworms. There was no age resistance to H. nana in mice. Immunity against the cyst challenge was acquired by initial egg inoculation and blocked by injecting cortisone acetate just prior to the challenge. However, the number of worms recovered from mice given cortisone was significantly less than that from nonimmunized controls. Unexpected evidence was obtained that a few of the egg-derived tapeworms can survive for 6 or more months in some of the immunized mice, which are resistant to both egg and cyst challenges. The relative immunogenicity of oncospheres and cysts is discussed. It is strongly suggested that the cysts are different from the oncospheres in their immunogenicity, and, because of this, H. nana can complete its life cycle in the same immunized host. It is also suggested that the host possesses at least two separate immune responses: One is an early response directed exclusively against the oncosphere and/or the early postoncospheral stage (s) acquired within 2 days of egg inoculation, and the other is a late response against the cyst acquired after a time lag of unknown duration.     

Growth and development of Hymenolepis nana in mice maintained at different environmental temperatures

Growth and development of Hymenolepis nana in mice maintained at different environmental temperatures. International Journal for Parasitology16: 13–17. On days 3 and 4 post infection (p.i.) the number of Hymenolepis nana cysticercoids in the villi of male mice kept at 5°C did not differ from those in controls (21°C), but fewer larvae were observed in hosts at 35°C. However, on day 10 and 14 p.i. in cysticercoid and egg-induced infections respectively, the incidence of infection was higher and significantly more worms per host were found in mice at 5°C than in those kept at 21 or 35°C. Also, worms from mice maintained at 5°C were significantly heavier and became patent 1 day earlier than those from 21°C, which, in turn, were significantly heavier than those grown in hosts at 35°C.     

Intestinal Parasites among Wild Rodents in Northern Gangwon-do,Korea

To determine geographical patterns of natural parasite infections among wild rodents, a total of 46 wild rodents from 3 different localities in northern Gangwon-do (Province), Korea were examined for intestinal parasite infections. Along with nematodes such as hookworms and Syphacia spp., Plagiorchis muris (2 specimens) (Trematoda) were collected from striped field mice, Apodemus agrarius. In a Korean wood mouse, Apodemus peninsulae, the overall nematode infections were similar to A. agrarius, but an adult worm of Echinostoma hortense (Trematoda) was collected. In addition, 2 species of cestodes, i.e., Hymenolepis nana and Hymenolepis diminuta, were collected from A. agrarius. Through this survey, A. agrarius and A. peninsule were confirmed as the natural definite hosts for zoonotic intestinal helminths, i.e., P. muris, E. hortense, H. nana, and H. diminuta, in northern Gangwon-do, Korea. Considering increased leisure activities around these areas, seasonal and further comprehensive surveys on wild rodents seem to be needed to prevent zoonotic parasite infections.     

Complement-mediated lysis in vitro of newly excysted tapeworms: Hymenolepis diminuta, Hymenolepis microstoma, Hymenolepis nana and Hymenolepis citelli

Bøgh H., Christensen J.P.B. and Andreassen J. 1986. Complement-mediated lysis in vitro of newly excysted tapeworms: Hymenolepis diminuta, Hymenolepis microstoma, Hymenolepis nana and Hymenolepis citelii. International Journal for Parasitology16: 157–161. Newly excysted worms of Hymenolepis diminuta were lysed in 50% normal serum from all 13 animal species tested, including man. Since H. diminuta was neither lysed in complement inactivated serum—by heat or adding EDTA, LPS or CVF—nor in C5-deficient mouse serum, it is concluded that the lysis was associated with the complement cascade. It is shown that H. diminuta can activate the complement system via both the classical and alternative pathway. Furthermore, it is indicated that the lysis is independent of serum antibodies. Hymenolepis nana and H. citelli were also lysed in all normal sera tested, eight and six respectively, while newly excysted worms of H. microstoma were lysed in normal sera from 10 mammals and birds, but not in sera from its hosts, the mouse, rat and golden hamster. This indicates that the complement system of these three species differs from that of the other species tested in such a way that H. microstoma is able to avoid lysis in these sera.     

Hymenolepis nana: Immunogenicity of a lumen phase of the direct cycle and failure of autoinfection in BALBc mice

When $\text{BALB}\text{c}$ mice were given $\text{BALB}\text{c}$ mouse-derived cysticercoids (cysts) of Hymenolepis nana, only $\text{1}\text{43}$ mice became autoinfected, whereas most ($\text{31}\text{38}$) of dd mice given the same infection became massively autoinfected with mature worms. When $\text{BALB}\text{c}$ mice initially given cysts were challenged with eggs on Day 7, just before the patency of the primary infection, there was normal development into cysts, but almost none of them developed into adult worms. Thus, the failure of autoinfection of H. nana in $\text{BALB}\text{c}$ mice was not a result of failure of eggs to differentiate into cysts in the intestinal tissue, but a result of failure of these cysts to develop into adult worms in the lumen. The reasons why autoinfection does occur in dd and other strains of mice and not in the $\text{BALB}\text{c}$ strain are discussed in terms of the difference in onset of the late response in these strains of mice, ie., the response that is acquired after egg inoculation, and is directed against the lumen phase of cyst challenges. It is strongly suggested that (1) the lumen phase which follows cyst inoculation is highly immunogenic, but clearly differs from tissue phase which follows egg inoculation, (2) the autoinfection which occurs in some strains of mice is therefore not a result of no or poor immunogenicity of the lumen phase but is due to a delay of onset of the late response with the result that a secondary generation may mature, and (3) in other strains of mice, including $\text{BALB}\text{c}$, which acquire the late response within 15 days of initial egg inoculation, autoinfection normally does not occur after cyst infections.     

Immunization of mice against infection with Trypanosoma cruzi. Cross-immunization between five strains of the parasite using freeze-thawed vaccines containing epimastigotes of up to five strains.

McHardy N. and Elphick J. P. 1978. Immunization of mice against infection with Trypanosoma cruzi. Cross-immunization between five strains of the parasite using freeze-thawed vaccines containing epimastigotes of up to five strains. International Journal for Parasitology8: 25–31. Groups of male CD-1 mice were immunized with two doses of vaccines containing 10⁸ freeze-thawed cultured epimastigotes of Trypanosoma cruzi of five strains—Y, M, BG, Peru and Tulahuen, with saponin as adjuvant. Each vaccine contained 1, 2, 3 or 5 strains of the parasite. The mice were challenged with each of the five strains. All the single-strain vaccines gave good protection against both homologous and heterologous challenges, with the exception of the strain Y vaccine, which gave poor protection against homologous challenge, but good protection against all four heterologous challenges. The inclusion of more than one strain of epimastigote in the vaccine failed to increase protection, and in some instances appeared to reduce it, in comparison with vaccines containing only one of the component strains. It is suggested that this is due to antigenic competition.     

Mouse strain variation and effects of oocyst dose in infection of mice with Eimeria falciformis, a coccidian parasite of the large intestine

Stockdale P. G. H., Stockdale M. J., Rickard M. D. and Mitchell G. F. 1985. Mouse strain variation and effects of oocyst dose in infection of mice with Eimeria falciformis, a coccidian parasite of the large intestine, International Journal for Parasitology15: 447–452. Five inbred strains of mice and three hypothymic (nude) strains were infected orally with different doses of E. falciförmis oocysts. After resolution of primary infection as determined by faecal oocyst output, mice were challenged orally with a second dose of E. falciformis. Amongst the intact mice, BALB/c proved the most resistant to primary infection, while C3H/He mice were most susceptible, in terms of faecal oocyst production. Resistance was far more dramatic in BALB/c mice given high numbers of challenge oocysts. In terms of mortality at high oocyst doses, CBA/H were the most susceptible. All of the strains of mice were highly resistant to reinfection. In the case of nude mice, BALB/c. nu/nu were more susceptible than CBA/H.nu/nu or C57BL/6.nu/nu both in terms of faecal oocyst production and mortality. Thus the most resistant inbred mouse strain (BALB/c) is the least resistant in the absence of T cells. Unlike intact mice, nude mice showed no resistance to reinfection, this result being in line with previous work on this and other Eimeria spp. in nude mice.     

Primary infection with mouse-derived cysticercoids of Hymenolepis nana prepared from baby or adult mice and secondary infections with eggs or cysticercoids

Oral infection with mouse-derived cysticercoids (cysts) of Hymenolepis nana on day 0 did not make the 5 ± 1 week old mouse host immune to egg challenge by day 7 of the prepatent period, although the number of cyst-derived tapeworms was 1000 times greater than that of egg-derived tapeworms sufficient to make the host immune by day 7. Neither cysts recovered from immunologically competent 5 ± 1 week old donor mice, which should have become immune within 2 days of egg inoculation, nor those from incompetent 5–7 day-old baby mice given eggs when 0–2 days old made the host immune. The time course of differentiation of cysts in baby mice was not different from that in 5 ± 1 week-old mice. Mice infected twice with cysts on days 0 and 4 did not become immune either. Rapid protective immunity against egg challenge was acquired by inoculation exclusively with eggs but not with cysts. Apparently cysts differ from oncospheres in their immunogenicity. The importance of cysts for analysing the mouse—H. nana system from the immunological point of view is discussed.     

Correlation between protective antibody response and patent infection with Hymenolepis nana in mice

Correlation between protective antibody response and patent infection with Hymenolepis nana in mice. International Journal for Parasitology16: 197–203. Mice inoculated with mouse-derived cysticercoids of Hymenolepis nana, as well as with eggs, produced IgG and IgE antibodies that were detected by double diffusion (DD) and passive cutaneous anaphylaxis (PCA), respectively. When mice inoculated with eggs (day 0) were challenged with eggs (day 66), all were resistant to the challenge (assessed by the failure of cysticercoid recovery in the intestinal tissue) and produced protective antibodies evidenced by passive transfer, as well as IgG and IgE isotypes. When mice inoculated with eggs (day 0) were treated with a highly efficacious cestocide, praziquantel on day 6 at the beginning of the lumen phase, all were also resistant to the egg challenge on day 66, however, IgE, IgG, and protective antibodies were not detected. When mice treated with praziquantel before patent infection were repeatedly challenged with high doses of eggs, some of them produced IgG and IgE antibodies. From these results, it is suggested that (1) the production of protective antibody is a secondary response after patency (which may be ascribed to eggs released from mature worms), and (2) mice initially given eggs are highly resistant to egg challenge showing that an effector mechanism of acquired resistance to egg challenge may be expressed without high titres of protective antibody, at least in the serum.     

Heavy Hymenolepis nana Infection Possibly Through Organic Foods: Report of a Case

We encountered a patient with heavy Hymenolepis nana infection. The patient was a 44-year-old Korean man who had suffered from chronic hepatitis (type B) for 15 years. A large number of H. nana adult worms were found during colonoscopy that was performed as a part of routine health screening. The parasites were scattered throughout the colon, as well as in the terminal ileum, although the patient was immunocompetent. Based on this study, colonoscopy may be helpful for diagnosis of asymptomatic H. nana infections.     

Egg production of Clonorchis sinensis in different strains of inbred mice.

In order to compare the intraspecific variation in host-parasite relationship of Clonorchis sinensis, six strains of inbred mice, ICR, DDY, GPC, BALB/c, nude and DS, were infected orally with 20 metacercariae of C. sinensis. The biologic incubation period of C. sinensis was the shortest in DDY mice, 21.2 days in average, followed by GPC 21.4, BALB/c and DS 23.2, ICR and nude 23.4 days, respectively. The fertile period of the fluke was also the longest in the DDY strain, 164 days on average, followed by GPC 132, BALB/c 97, nude 37, DS 32 and ICR 28 days. The egg-laying capacity of the fluke in DDY and GPC was relatively high and stable compared with the other four strains of mice. It was found that there are intraspecific variations in biologic incubation period, fertile period, and fecundity of C. sinensis. The DDY mouse is likely to be the most suitable experimental animal among the six strains of the mice tested.     

Cryptic diversity in hymenolepidid tapeworms infecting humans

An adult hymenolepidid tapeworm was recovered from a 52-year-old Tibetan woman during a routine epidemiological survey for human taeniasis/cysticercosis in Sichuan, China. Phylogenetic analyses based on sequences of nuclear 28S ribosomal DNA and mitochondrial cytochrome c oxidase subunit 1 showed that the human isolate is distinct from Hymenolepis diminuta and Hymenolepis nana, the common parasites causing human hymenolepiasis. Proglottids of the human isolate were unfortunately unsuitable for morphological identification. However, the resultant phylogeny demonstrated the human isolate to be a sister species to Hymenolepis hibernia from Apodemus mice in Eurasia. The present data clearly indicate that hymenolepidid tapeworms causing human infections are not restricted to only H. diminuta and H. nana.     

A comparative study of the susceptibility of inbred strains of mice to infection with Mesocestoides corti

White T. R., Thompson R. C. A. and Penhale W. J. 1982. A comparative study of the susceptibility of inbred strains of mice to infection with Mesocestoides corti. International Journal for Parasitology12: 29–33. The susceptibility of 6 strains of inbred mice to infection with Mesocestoides corti was studied following both intraperitoneal and oral inoculation of tetrathyridia. The greatest degree of resistance was seen in C57BL/6 mice and this resistance was independent of route of inoculation. The proliferation of the parasite in C57BL/6 mice was compared with a more susceptible strain (CBA/H) on 7, 14, 21, 35 and 60 days post-infection. Although both strains harboured significantly different parasite burdens during the initial period following infection, these differences were no longer apparent by day 60.     

Morphological and molecular identification of hymenolepidid cestodes in children and synanthropic rodents from rural Mexico

Hymenolepidid cestodes of synanthropic rodents represent a risk for public health. In order to describe the occurrence of hymenolepidids in children and the role of rodents as a potential source of infection, we conducted a morphological and molecular survey on cestodes in two rural villages from Yucatan, Mexico. One hundred and thirty-five stool samples from children (64 from Paraíso and 71 from Xkalakdzonot), 233 Mus musculus (159 from Paraíso and 74 from Xkalakdzonot) and 125 Rattus rattus (7 from Paraíso and 118 from Xkalakdzonot) were analyzed for the presence of cestodes. Three hymenolepidid species were identified morphologically: Hymenolepis nana in 7.8% of children from Paraíso, Hymenolepis microstoma in 4.4% of M. musculus from Paraíso and Hymenolepis diminuta in 15.3% of R. rattus from Xkalakdzonot. The molecular characterization and phylogenetic analysis based on mitochondrial cytochrome c subunit 1 (CO1) gene and ribosomal internal transcribed spacer 1 (ITS1) region, confirmed the identity of the three cestodes isolated from Yucatan. Phylogeny of the CO1 gene identified intraspecific genetic differences within H. nana ranging from 0 to 5%, in H. microstoma from 0 to 0.4%, and in H. diminuta ranged from 0 to 6.5% which suggests, the presence of complex species within H. nana and H. diminuta infecting humans and rodents, as reported by other authors. Based on the morphological and molecular results, and the epidemiological evidence, infections with H. nana suggest a non-zoonotic transmission; however, the presence of H. microstoma and H. diminuta in synanthropic rodents serve as a possible source for human infection.     

Circulating immunoglobulins and complement in mice with Hymenolepis nana infection

Changes in the circulating immunoglobulins and complement in ddY mice were assayed at various times after immunizing and challenge infections with Hymenolepis nana eggs. The levels of IgG1 and IgG2a consistently increased during 3–4 weeks after immunizing infection. The increase of these immunoglobulins after challenge infection was quicker and more intense than that following immunization. It was not possible to correlate increased levels of IgG1 and IgG2a with the onset of destruction of challenge larvae in immunized mice. IgM concentrations increased slightly during 4 days after immunization but challenge infection did not further increase IgM levels. IgA and IgG2b levels showed no significant change during the course of the infection. Serum C3 levels showed no discernible change after either immunizing or challenge infections. An attempt to specifically suppress the acquisition of resistance by administration of the complement-depleting agent, cobra venom factor (CoF), before immunization failed and depletion of complement activity with CoF that was administered just before challenge infection also failed to affect resistance. These results suggest that complement has no critical role in either induction of the response nor in the anamnestic response to H. nana infection in mice.     

Hymenolepis nana: Maturation in an immunosuppressed unnatural rat host

When eggs of the dwarf tapeworm Hymenolepis nana, cycled exclusively and directly through mice for more than 10 years, were inoculated into previously uninfected inbred Fischer (F344) strain rats, they failed to mature in the rat intestinal lumen. Eggs of H. nana inoculated into the rat developed normally into cysticercoids (cysts) in the intestinal tissue, but thereafter failed to mature in the lumen except when the host was treated with cortisone acetate from the day of cyst maturation. The Fischer rat initially given eggs of H. nana became completely immune to egg challenge within 2 days of egg inoculation; no cysts derived from challenge eggs were found in the immunized rat. Immunosuppression, assessed by the success of cyst recovery in the tissue 4 days after egg challenge, had no promotive effect on the recovery of adult worms derived from eggs initially inoculated. Rats initially given eggs and immunosuppressed by cyclophosphamide or antithymocyte serum did not harbor any adult worms. Cortisone acetate treatment which was sufficient for eggs inoculated to mature (a total of 75 or even 200 mg, from Day 5 of egg inoculation) had no effects of immunosuppression, whereas cortisone acetate treatment which was sufficient for immunosuppression (a total of 150 mg from Day -2, two days prior to the initial egg inoculation) induced some adult formation as well. In addition, when mouse-derived cysts were inoculated into the rat instead of eggs, they also failed completely to mature even when the rat was treated with cyclophosphamide or antithimocyte serum. However, when the rat was treated with cortisone acetate from the day of cyst inoculation, the cysts developed into adult worms. Therefore, these results indicate that the Fischer rat clearly differs in its susceptibility to the tissue phase of egg inoculation and to the lumen phase of cyst inoculation of H. nana, and strongly suggest that the failure of maturation of H. nana in the unnatural host Fischer rat is not attributed to innate and/ or acquired immunity of the rat but to other nonimmunological mechanisms.     

Prevalence of Intestinal Parasitic Infections among Children under Five Years of Age with Emphasis on Schistosoma mansoni in Wonji Shoa Sugar Estate,Ethiopia

Intestinal parasite infections are major public health problems of children in developing countries causing undernutrition, anemia, intestinal obstruction and mental and physical growth retardation. This study was conducted to assess the prevalence of intestinal helminthic infections among children under five years of age with emphasis on Schistosoma mansoni in Wonji Shoa Sugar Estate, Ethiopia. A cross-sectional parasitological survey was conducted in under-five children living in Wonji Shoa Sugar Estate Ethiopia, April, 2013. Stool samples were collected and examined for intestinal parasites using single Kato-Katz and single Sodium acetate-acetic acid-formalin (SAF) solution concentration methods. Out of 374 children examined using single Kato-Katz and single SAF-concentration methods, 24.3% were infected with at least one intestinal parasite species. About 10.4%, 8.8%, 4.6%, 2.9%, 1.6% and 0.8% of the children were infected with Hymenolepis nana, Schistosoma mansoni, Ascaris lumbricoides, Trichuris trichiura, Enterobius vermicularis and hookworm, respectively. Prevalence of double, triple and quadruple intestinal helminthic infection was 6.4%, 0.54% and 1.1%, respectively. A significant increase in prevalence of S. mansoni (8.3% versus 3.2%) and T. trichiura (2.7% versus 0.5%) infection was observed when determined via the single Kato-Katz method compared to the prevalence of the parasites determined via the single SAF-concentration method. On the other hand, the single SAF-concentration method (9.1%) revealed a significantly higher prevalence of H. nana infection than the single Kato-Katz (1.6%) does. In conclusion, intestinal helminths infections particularly S. mansoni and H. nana were prevalent in under-five children of Wonji Shoa Sugar Estate. Including praziquantel treatment in the deworming program as per the World Health Organization guidelines would be vital to reduce the burden of these diseases in areas where S. mansoni and H. nana infections are prevalent among under-fives. Kato-Katz can be used in estimating the prevalence of S. mansoni and other helminth infections.