Endemicity of Paragonimus and paragonimiasis in Sub-Saharan Africa: A systematic review and mapping reveals stability of transmission in endemic foci for a multi-host parasite system.

Paragonimiasis is caused by zoonotic trematodes of Paragonimus spp., found in Asia, the Americas and Africa, particularly in tropical regions. These parasites have a complex, multi-host life cycle, with mammalian definitive hosts and larval stages cycling through two intermediate hosts (snails and freshwater decapod crustaceans). In Africa, paragonimiasis is particularly neglected, and remains the only human parasitic disease without a fully characterised life cycle. However paragonimiasis has potentially significant impacts on public health in Africa, and prevalence has likely been underestimated through under-reporting and misdiagnosis as tuberculosis due to a similar clinical presentation. We identified the need to synthesise current knowledge and map endemic foci for African Paragonimus spp. together with Poikilorchis congolensis, a rare, taxonomically distant trematode with a similar distribution and morphology. We present the first systematic review of the literature relating to African paragonimiasis, combined with mapping of all reported occurrences of Paragonimus spp. throughout Africa, from the 1910s to the present. In human surveys, numerous reports of significant recent transmission in Southeast Nigeria were uncovered, with high prevalence and intensity of infection. Overall prevalence was significantly higher for P. uterobilateralis compared to P. africanus across studies. The potential endemicity of P. africanus in Côte d'Ivoire is also reported. In freshwater crab intermediate hosts, differences in prevalence and intensity of either P. uterobilateralis or P. africanus were evident across genera and species, suggesting differences in susceptibility. Mapping showed temporal stability of endemic foci, with the majority of known occurrences of Paragonimus found in the rainforest zone of West and Central Africa, but with several outliers elsewhere on the continent. This suggests substantial under sampling and localised infection where potential host distributions overlap. Our review highlights the urgent need for increased sampling in active disease foci in Africa, particularly using molecular analysis to fully characterise Paragonimus species and their hosts.

Paragonimiasis.

Paragonimiasis is a zoonotic disease caused by lung flukes of the genus Paragonimus. Humans usually become infected by eating freshwater crabs or crayfish containing encysted metacercariae of these worms. However, an alternative route of infection exists: ingestion of raw meat from a mammalian paratenic host. Adult worms normally occur in pairs in cysts in the lungs from which they void their eggs via air passages. The pulmonary form is typical in cases of human infection due to P. westermani, P. heterotremus, and a few other species (Table 5.1). Worms may occupy other sites in the body, notably the brain, but lung flukes have made their presence felt in almost every organ. Ectopic paragonimiasis is particularly common when infection is due to members of the P. skrjabini complex (Table 5.1). Human paragonimiasis occurs primarily in the tropics and subtropics of Asia, Africa, and the Americas, with different species being responsible in different areas (Table 5.1).

Inactivation of Paragonimus westermani metacercariae in soy sauce-marinated and frozen freshwater crabs.

Soy sauce-marinated freshwater crabs (Eriocheir japonicus) are a source of human paragonimiasis. The viability of Paragonimus westermani metacercariae (PwMc) in marinated crabs was investigated in an experimental setting. The PwMc collected from freshwater crayfish were inoculated into freshwater crabs, which were then frozen or marinated in soy sauce. All PwMc in the freshwater crabs were inactivated after freezing for 48 h at -20 °C and after freezing for 12 h at -40 °C. After marinating for 32 days, the survival rate of PwMc in 5% NaCl soy sauce was 50%, in 7.5% NaCl soy sauce it was 33.3%, and in 10.0% NaCl soy sauce it was 31.3%. When marinated for 64 days, all PwMc were inactivated in all experimental groups. These results revealed that freezing and soy sauce marination were detrimental to the survival of PwMc in freshwater crabs. Specifically, freezing crabs for more than 48 h or soaking them in soy sauce containing at least 5.0% NaCl for 64 days can inactivate PwMc. These results can inform the production of the traditional Korean soy sauce-marinated freshwater crabs known as gejang.

Paragonimiasis in KwaZulu-Natal Province, South Africa.

Nine cases of paragonimiasis have been reported from cats (4), dogs (2) and children (3) in South Africa, with an additional suspected case in an adult female patient. Details of these cases are reviewed. All nine cases, and perhaps the adult case as well, were from the province of KwaZulu-Natal but locality data are only available for six of them. These six cases represent four localities which all lie below 100 m above sea level in the province's lowlands, suggesting that there may be a focus of transmission here. The molluscan first intermediate host must be one of the two prosobranch snail species present in the area, Melanoides tuberculata or Tomichia natalensis, and the decapod second intermediate host the common river crab Potamonautes sidneyi. All infected cats and dogs had pulmonary infections, while two human cases for which there is sufficient information had extrapulmonary infections. Transmission appears to be ongoing but the invasive snail Tarebia granifera may be competing with both M. tuberculata and T. natalensis. If so, this may bring transmission to an end.

Epidemiology of Paragonimiasis in Oban Community of Cross River State; Nigeria

The epidemiology and perception of Paragonimus infection were investigated in Oban community of Cross River State; Nigeria between January and June; 2006. Sputum samples collected on each of three consecutive days from 311 participants with productive cough were examined using standard parasitological procedures for the detection of ova of Paragonimus Spp. The samples were also processed and stained using the Ziehl-Neelsen technique to exclude Mycobacterium tuberculosis infection. Crabs collected from the village streams were dissected and examined for the presence of metacercariae of Paragonimus Spp. A questionnaire was also administered to test the perception of the disease. Paragonimus uterobilateralis was confirmed as the aetiologic agent of paragonimiasis with a prevalence of 4.2. Peak prevalence of 7.7was found among children aged between 1 to 10 years. More males (4.5) were infected than females (3.9) (P 0.05). The mean egg count was high (222 egs/5ml of sputum). The intensity of infection was found to correlate moderately and strongly with haemoptysis (r = 0.6) and chest pain (r=0.8) respectively. Only 1.6of the subjects had tuberculosis and presented with symptoms which mimic paragonimiasis. Sudanonautes africanus is the suspected vector of the disease in this locality. The disease; its vector and mode of transmission were poorly perceived by the respondents. The study has confirmed the endemicity of paragonimiasis in Oban community as well as provides comprehensive information on the disease and its transmission in this locality. There is urgent need to initiate the control of this disease in this community

[Paragonimosis in the peri-urban zone of Medellín, Antioquia]. / Estudio de foco de paragonimosis en Fuente Clara, Robledo, área periurbana de Medellín, Antioquia.

INTRODUCTION: Human paragonimosis in Colombia was assumed to be restricted to the sylvatic areas. However, in 2005, crabs infected with Paragonimus were found in Fuente Clara, an urban sector in Medellín. OBJECTIVE: A study was designed to understand the ecoepidemiology of paragonimosis. Programs were initiated to educate the community in the suitable use of wetland ecosystems. MATERIALS AND METHODS: Infection rates of Paragonimus in human and wild hosts was documented in the Fuente Clara sector. The presence of larvae and digenic adult worms was detected in mollusks (1,312), crabs (27) and mammals (4). Sputum diagnosis was performed on samples from 18 volunteer individuals. The following determinants of water quality were measured in the stream La Puerta: total fecal/coliform, pH, conductivity and dissolved oxygen were measured. Recreational workshops were conducted with children and teenagers for educational purposes. RESULTS: The percentage of infections found in hosts was as follows: snails, 0.07%; crabs, 55.5%; (wild) mammals, 25%; humans, 0%. During the workshops, children and teenagers identified the Paragonimus hosts and the risk factors for acquiring the disease. The water of the stream was found to be unsuitable for consumption and recreation (the most probable number of total coliforms/100 ml was in a scale of 104). CONCLUSIONS: Fuente Clara is the first urban locality in Colombia where a focus of Paragonimus was found. Exposure to and consumption of crabs may constitute a risk for human infection.

First findings on the seroepidemiology of human paragonimosis at the anti-tuberculosis centre of Divo, Repubuc of Ivory Coast (West Africa).

An epidemiological study was carried out in 2004-2005 at the anti-tuberculosis centre of Divo (Ivory Coast) to collect sera from patients who consulted for tuberculosis suspicion and to estimate the seroprevalence of human paragonimosis in the context of a systematic screening. No Paragonimus egg was found in the stools and/or sputa of the 167 persons investigated. In contrast, 41 sera were ascertained with antibodies against Paragonimus africanus using ELISA testing. As the optical density (OD) values related to seropositive findings were found under 0.6 (the minimal OD to detect an active paragonimosis), the above antibody titres might originate from patients in chronic or in convalescent stages, or might result of cross reactions with trematodes. Concomitantly, dissection of local crabs (Callinectes marginatus) demonstrated the presence of Paragonimus metacercariae in six out of 34 examined. The parasite burdens in crabs ranged from two to 35 cysts with a mean diameter of 302 microm. In Ivory Coast, the locality of Divo must be considered an at-risk zone in reason of the presence of anti-Paragonimus antibodies in several human sera and the presence of infected crabs at the local market.

Paragonimiasis: an important food-borne zoonosis in China.

The lung fluke, Paragonimus westermani, is of major socioeconomic importance in Asia. The parasite is transmitted via snails to freshwater crabs or crayfish, then to humans and other mammals, such as cats and dogs, and causes paragonimiasis. This review provides a background on the parasite and its life cycle; summarizes key aspects regarding the pathogenesis, diagnosis and treatment of paragonimiasis; describes the geographic distribution and prevalence of paragonimiasis; and makes some recommendations for future research and the control of this important disease in China.

Paragonimiasis and its intermediate hosts in a transmission focus in Lao People's Democratic Republic.

Human cases of paragonimiasis have been reported in Lao People's Democratic Republic from several provinces, however, detailed descriptions of a focus of transmission including parasites species and intermediate hosts are lacking. Field investigations were carried out between February and July 2004 in three neighboring villages of the province of Vientiane. Persons with chronic cough (more than three weeks) were identified during a door-to-door survey and three sputum samples were examined for Paragonimus spp. and tuberculosis on two consecutive days. Potential intermediate snail and crustacean hosts were sampled among the populations' water-contact sites and examined for metacercarial infections or cercarial shedding. Four dogs were infected with metacercaria and the species of the subsequently retrieved adult parasites were identified. 12.7% (15 cases) of all chronic cough patients (0.6% of the total population) suffered from paragonimiasis. Samples of five species of freshwater snails, two species of crabs and one species of prawn were collected from the Nam Sêt River. None of the snails were infected. Metacercariae of P. harinasutai, P. bangkokensis and P. heterotremus were found in Potamon lipkei crabs while an infection with P. westermani was observed in a Chulathelphusa brandti crab. No paragonimid metacercaria was found in the Macrobrachium dienbienphuense prawns Dang and Nguyen 1972. This study demonstrates the importance of Paragonimus spp. as an etiological agent in patients with chronic cough and suggests that similar transmission might be widespread in Lao People's Democratic Republic. We document herein the transmission of several Paragonimus species indicating that paragonimiasis is an active zoonosis in Lao People's Democratic Republic.

[Pleuro-pulmonary paragonimiasis]. / La paragonimose pleuropulmonaire.

Paragonimiasis is a food borne zoonosis due to a trematode belonging to the genus Paragonimus. Although present throughout the world, about 90% of the cases occur in Asia where around 20 million people are infected. The parasitic cycle is complex with two different intermediate hosts. Man is infected by ingesting the raw or undercooked flesh of the second host - a freshwater crab or prawn - or possibly of a paratenic mammal host (wild boar), which contains the infective larval stage metacercariae that reaches the lung which is the main target organ. Epidemiological, pathological, and clinical aspects are reviewed. The main symptoms are protracted cough, and recurrent "benign" hemoptysis. Abnormal pleuro-pulmonary imaging features are constant, but protean and non-specific, leading to frequent confusion with tuberculosis. Diagnosis is easily achieved by ova search in the sputum or pleural fluid, or by serology. Evolution is usually considered benign, although not well known. Finally, praziquantel is the effective first choice treatment. Some paradoxical aspects of this disease are underlined such as: underdiagnosis despite a very simple diagnostic procedure, or opposite tendencies according to location, either extinction or re-emergence.

[Familial infestation of Paragonimus westermani with peritonitis and pleurisy].

Human paragonimiasis was endemic in Korea until the 1960's, and nowadays, the prevalence is decreasing. However, it is still one of the important helminthic diseases. Though it is essentially a pulmonary disorder, it may involve brain, muscle, mesentery, genital tract, pleura, peritoneum, spinal cord, spleen, and liver. We experienced two cases of paragonimiasis in a family who had ingested raw crabs together for 7 months. A 57-year-old female patient was admitted due to abdominal pain, diarrhea and tenesmus for 6 months. And, her 35-year-old son complained of cough, chest discomfort and dyspnea. The definite diagnosis for paragonimiasis could be made by the detection of the egg and adult worm from stool, sputum and involved lesion. Neither an egg or worm was detected. However, they were diagnosed based on the food history, laboratory data including serum eosinophilia, ELISA for specific IgG, pleural and peritoneal fluid examination, radiological findings, and intradermal tests. They were treated with praziquantel and their symptoms improved rapidly over 2 days. Both patients were asymptomatic at a follow-up visit 2 months later.

Erhaia (Gastropoda: Rissooidea): phylogenetic relationships and the question of Paragonimus coevolution in Asia.

The human lung fluke Paragonimus is transmitted by gastropod taxa of two superfamilies: Ceritheoidea and Rissooidea. The question whether or not Paragonimus shows the same specificity of host-parasite coevolved relationship as the human blood fluke Schistosoma was inspired by the finding of two sympatric snail species as hosts for Paragonimus skrjabini in Fujian Province, China: Gammatricula and Erhaia. The former species can clearly be classified as Pomatiopsidae: Triculinae. The latter has previously been classified as Pomatiopsidae: Pomatiopsinae. However, this classification based on anatomical characteristics is uncertain. In order to obtain a robust phylogenetic hypothesis for Erhaia, we have studied three gene fragments from this taxon as well as from twelve related taxa. The data show that the species involved represent four families: Pomatiopsidae, Hydrobiidae, Cochliopidae (here raised to family status), and Amnicolidae. Erhaia fits securely into the Amnicolidae. This indicates that P. skrjabini has not coevolved with snail lineages. However, P. skrjabini has so far only been reported from rissooidean snails, whereas members of the Paragonimus westermani complex have only been found in ceritheoidean snails. The implication is that there is a host specificity on the superfamily level. However, Asian freshwater species of the Ceritheoidea and Rissooidea usually are not sympatric and often prefer different habitats. It is therefore possible that ecological niche partitioning plays the primary role for Paragonimus evolution.

[Epidemiological observations on the first case of human paragonimiasis and potential intermediate hosts of Paragonimus sp. in Benin]. / Observations épidémiologiques sur le premier cas de paragonimose humaine et les hôtes intermédiaires potentiels de Paragonimus sp. au Bénin.

Parasitological investigations were carried out for four months in 1998 in two Beninese centres of pneumo-phtisiology (Akpakpa, at Cotonou, and Akron, at Porto-Novo) to detect the patients harbouring eggs of Paragonimus sp. amongst the persons consulting for tuberculosis and showing a broncho-pneumopathy without mycobacteria. Eggs of Paragonimus sp. were detected in the sputum of a single patient out of 369 persons examined (prevalence, 0.2%). This patient had eaten crabs in the months preceding the date of diagnosis. A treatment using praziquantel has improved clinical symptomatology and biological signs found in this patient. These studies have been completed by visiting markets located in the coastal plain of Benin to identify the crabs that were sold and to find metacercariae of Paragonimus sp. Negative results were obtained when 126 Cardisoma armatum ("hole crab") were dissected. In contrast, the dissection of 176 Callinectes marginatus ("swimming crab") was successful, with 5% of crabs harbouring metacercariae of probably Paragonimus sp. Further studies are necessary to confirm these first results and to determine the global prevalence of Paragonimus infection in these definitive and intermediary hosts.

[Paragonimiasis: a rare little known disease]. / La paragonimose: une affection rare à ne pas méconnaître.

BACKGROUND: Paragonimiasis, caused by a lung fluke, is an parasitic disease rarely encountered in France. CASE REPORT: A 52-year-old man developed dyspnea, cough, mild fever and chest pain. Pleural effusion suggested possible pulmonary embolism or tuberculosis. Cell counts in blood and pleural effusion fluid revealed major eosinophila in this patient who had recently returned from a trip to Japan. Paragonimiasis was confirmed by ELISA. Treatment with praziquantel led to complete clinical and radiographic recovery. DISCUSSION: The clinical and radiographic features of paragonimiasis are often similar to tuberculosis with pleuropneumopathy, mild fever and dyspnea. ELISA has now replaced parasitologic diagnosis. Cure is achieved with praziquantel.

[A case of paragonimiasis westermani].

A 45-year-old man, who had eaten fried fresh water crabs (Geothelphusa dehaani), was admitted to our hospital because of productive cough and bloodysputum. Blood chemistry showed increased levels of white blood cells and C-reactive protein, but peripheral blood eosinophil counts and serum IgE values were not elevated. Chest roentgenogram and chest computed tomographic scan revealed infiltration of the right middle and left upper lung fields. He was diagnosed as having pneumonia, but his symptoms and radiological examination findings did not improve with antibiotics. The diagnosis of paragonimiasis was confirmed by immunoserological examination and detection of ova in sputum, stool and bronchoalveolar lavage fluid samples. Transbronchial lung biopsy showed infiltration and degranulation of eosinophils. The patient was treated with praziquantel for 3 days at a daily dosage of 75 mg/kg. After uneventful completion of treatment all clinical symptoms and radiological abnormalities disappeared. This is the first case in which ova of paragonimiasis westermani were identified in Nagano prefecture.

An outbreak of paragonimiosis in Zhengzhou city, China.

An outbreak of paragonimiosis occurred in the city of Zhengzhou, Central China, in May 1995. Of seven exposed urban inhabitants, four were seropositive for Paragonimus and had clinical symptoms consistent with acute paragonimiosis. All of four cases treated were cured with praziquantel. The P. skrjabini adult worm was obtained from the rats experimentally infected with the crabs collected in the mountainous area where the urban inhabitants had got the infection. The outbreak was attributed to the intake of raw freshwater crabs while on tourist trips in a mountainous area.

[Endemic area of paragonimiasis in Vietnam]. / Un foyer de paragonimose au Viet Nam.

We studied 155 patients with chronic pulmonary disease from a mountainous area in north-west Vietnam, in March, 1993. Sputum was collected from patients and examined for the presence of Paragonimus eggs using a light microscope. Forty four of the patients (approximately 28%) were diagnosed with and treated for human paragonimiasis. Forty two of these cases were purely pleural-pulmonary forms whereas the remaining two cases also involved problems with the central nervous system. Most of the patients had eaten freshwater crabs (Ranguna luangprabangensis) which had been insufficiently cooked. This appears to be the main source of infection as these crustaceans are often highly contaminated with metacercariae. Most of the patients were children (aged 11 +/- 5 years) and male (30 of the 44). Sputum samples were also collected from 225 healthy people from the same area during the period March 1993 to April 1996. The samples were examined using a light microscope and 11 (approximately 5%) were found to contain Paragonimus eggs. A number of animals were also tested. Three pet dogs (of 14 tested), 2 wild dogs (of 2 tested) and 2 domestic pigs (of 15 tested) were found to be infected with the fluke. This is the first report of an area with endemic paragonimiasis in Vietnam. Human infections probably also occur in other areas. They are a threat to public health and may be confused with tuberculosis.