An emerging public health problem in India

Paragonimiasis: an emerging public health problem in India

Mahajan, R C

Paragonimiasis, which affects at least 22 million people throughout the world is potentially, is a serious disease in many countries, caused by the lung fluke belonging to Genus Paragonimus and the Family Troglotrematidae1. Paragonimus infection in man is caused by eating undercooked/raw infected crabs and crayfishes harbouring infective metacercariae of the flukes or by ingestion of undercooked meat of paratenic hosts such as pigs, wild boars or rats carrying juvenile flukes1. In India, a focus of human paragonimiasis caused by Paragonimus westermani was first described in Manipur in 1982. At that time, it was widely believed that human paragonimiasis was restricted to the Manipur state only. Recently, human focus of paragonimiasis has been described from Arunachal Pradesh2. Current evidence suggests that paragonimiasis is endemic in practically all the States of North East region of India (Regional Medical Research Centre, Dibrugarh, Assam; unpublished data).

Narain et al2, reported that freshwater crab was a popular food among many tribes of northeastern region. Although infection rates in fresh water crabs is not homogenous, yet up to 59.4 per cent Barytelphusa lugubris crabs were found infected with metacercariae of Paragonimus species at some places in Arunachal Pradesh. Besides Potamiscus manipurensis acts as an intermediate host of lung flukes in Manipur3. The intensity of infection in Barytelphusa lugubris crabs ranged from 15-1000 metacercariae (mean = 165 metacercariae per infected crab)2.

Public health significance of paragonimiasis is being increasingly recognized because this disease is frequently misdiagnosed as pulmonary tuberculosis’. In fact, pulmonary paragonimiasis and pulmonary tuberculosis (PTB) are overlapping public health problems in many countries where both the diseases co-occur. Due to similarity in their clinical, radiological manifestations the chances of diagnostic confusion could increase as has been reported recently from Arunachal Pradesh4. Cases of pulmonary paragonimiasis were often diagnosed as smear negative tuberculosis and were treated with anti-tuberculosis drugs. The implications of this finding are considerable, because the patient gets anti-tuberculosis treatment for a non-tubercular condition. Normally communities in remote areas perceive treatment success or failure with the disappearance of symptoms (haemoptysis and chronic cough in this situation). Hence, this may cast a negative impact on tuberculosis control programme by influencing treatment-seeking behaviour of genuine PTB patients with similar symptoms. The present observations, therefore, emphasize the need to generate awareness among the clinicians and public regarding paragonimiasis, and this disease should be considered in the differential diagnosis of PTB in places where both co-exist. It appears that X-ray along with clinical history will not be sufficient for correct diagnosis of smear-negative tuberculosis in such areas. It will be necessary to take a history of crab/crayfish eating habit of the patients in addition to the examination of sputum for Paragonimus eggs. Where resources permit, ELISA or skin test can also be used for diagnosis of paragonimiasis.

Evidently, accurate and sensitive diagnosis of paragonimiasis is of great importance, both at individual and community level. A diagnostic procedure can be used for a number of applications, ranging from clinical diagnosis of an individual case to the evaluation of control measures. The most reliable means of diagnosis of pulmonary paragonimiasis is finding of parasite eggs in sputum, faeces, pleural effusion and bronchoscopic washing or biopsy specimens etc1. However, sputum examination for detection of eggs is less sensitive method for diagnosis of paragonimiasis and up to seven sputum examinations are recommended in suspected patients1. Further, the parasite eggs are also not detected during pre-patent period of infection or in extra-pulmonary paragonimiasis.

In this issue Narain et al5 have described an indigenously developed ELISA for detection of antibodies against somatic(s) or excretory-secretory (ES) antigens of Paragonimus species. The usefulness of this diagnostic method will be of immense importance for studying epidemiology of Indian paragonimiasis and will be an important step in controlling this disease.

Perusal of literature revealed that efforts have been made to develop immuno-diagnostic methods for detection of paragonimiasis. One of the earliest tests used for diagnosis is intradermal test (ID test)6. However, its major disadvantage is the cross-reactions with other trematodes6 and allergic reactions caused in some patients after their skin test7. Subsequently, enzyme linked immunosorbent assay (ELISA) for detection of antibodies against lung flukes became popular because of high sensitivity and suitability for mass screening8,9. Many workers have used ELISA for detection of antibodies in host sera. However, most of these workers used crude somatic antigens, with the result cross-reactivity with sera of persons suffering from schistosomiasis, clonorchiasis and other trematodes were reported. Another important limitation of using somatic antigen is cross-reaction with sera of persons having Schistosome cercarial dermatitis5. Attempts have been made to reduce cross-reactions by either using partially purified antigens or subjecting test sera to adsorption with heterologous antigens prior to ELISA10. Superiority of excretory/secretory antigens over somatic antigens for increasing the specificity of the ELISA has been demonstrated by several workers9.

Perusal of literature shows that no research has been published on the application of hybridoma technology regarding Indian lung flukes. As such monoclonal antibodies developed against Indian lung flukes should be used. Such study will be an important step to find out the epitope repertoire of parasite antigens of Indian species of lung flukes. Such studies will eventually help to develop highly specific and sensitive diagnostic kits for detection of paragonimiasis.

Of the 50 or more species of Paragonimus reported from different countries11, only 9 species are known to infect man and are responsible for human suffering1. However, the taxonomic status of many species is under question pending further molecular characterizations of these flukes11. The genus Paragonimus shows greatest diversity in terms of geographical distribution, hosts parasitized, pathogenicity, other biological characteristics and species recognized. In India, from several parts different species of Paragonimus have been described from animals in the past and only a few studies from Northeast have reported human infections. Molecular techniques have been used to study inter- and intra-specific variations of lung flukes in order to confirm validity of species identified by traditional methods using only morphological characters12,13. However, the species of Paragonimus present in NE region have yet to be characterized at molecular level. Even the Paragonimus westermani the most common lung fluke of man, is known to be a complex of species and shows variation in pathogenicity and other biological variations in different geographic areas14. Therefore, in order to optimize control of trematode diseases, there exists a need for studying population genetic structure including accurate identification of Indian lung flukes using state of the art molecular techniques for more complete characterization. Further, extensive field studies are desirable to estimate the burden of human paragonimiasis in India. This aspect needs to be tackled on a high priority since the data show that paragonimiasis is an overlapping issue with tuberculosis4.

References

1. Toscane C, Hai YS, Mott KE. Paragonimiasis and tuberculosis, diagnostic confusion: A review of literature. Trop Dis Bull 1995; 92 : RI-R27.

2. Narain K, Devi KR, Mahanta J. Paragonimus and paragonimiasis: a new focus in Arunachal Pradesh, India. Curr Sci 2003; 84 : 985-7.

3. Singh TS, Singh YI. Three types of Paragonimus metacercariae isolated from Potamiscus manipurensis, in Manipur. Indian J Med Microbiol 1997; 15 : 159-62.

4. Narain K, Devi KR, Mahanta J. Pulmonary paragonimiasis and sputum negative pulmonary tuberculosis: a diagnostic dilemma. Int J Tuberc Lung Dis 2004; 8 : 621-2.

5. Narain K, Devi KR, Mahanta J. Development of enzymelinked immunosorbent assay for serodiagnosis of human paragonimiasis. Indian J Med Res 2005; 121 : 739-46.

6. Blair D, Xu ZB, Agatsuma T. Paragonimiasis and the genus Paragonimus. Adv Parasitol 1999; 42 : 113-222.

7. Chen SZ. Abnormal allergy in Paragonimus antigen serumtest and its clinical significance. Chin Med J 1985; 98 : 511-4.

8. Pariyanonda S, Maleewong W, Pipitgool V, Wongkham C, Morakote N, Intapan P, et al. Serodiagnosis of human paragonimiasis caused by Paragonimus heterotremus. Southeast Asian J Trop Med Public Health 1990; 21 : 103-7.

9. Maleewong W, Pariyanonda S, Wongkham C, Intapan P, Daenseegaew W, Morakote N. Comparison of adult somatic and excretory-secretory antigens in enzyme-linked immunosorbent assay for serodiagnosis of human infection with Paragonimus hetertremus. Trans R Soc Trop Med Hyg 1990; 84 : 840-1.

10. Choi WY, Imai JI, Horii Y, Nawa Y. Application of IgG-ELISA for mass screening of Paragonimus and Gnathostoma infections in the central part of Miyazaki Prefecture, Japan. Jpn J Parasitol 1992; 41 : 334-7.

11. Yang JS, Chen MG, Feng Z. Paragonimus and Paragonimiasis in China: a review of the literature. Chin J Parasitai Parasitic Dis 2000; Special issue, 9: 1-78.

12. Blair D, Agatsuma T, Watanobe T. Molecular evidence for the synonymy of three species of Paragonimus, P. ohirai miyazaki, 1939, P. iloktsuenensis chen, 1940 and P. sadoensis miyazaki et al, 1968. J Helminthol 1997; 71 : 305-10.

13. van Herwerden L, Blair D, Agatsuma T. Intra- and interindi vidual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: implications for phylogenetic studies. MoI Phylogenet Evol 1999; 12 : 67-73.

14. Iwagami M, Ho LY, Su K, Lai PF, Fukushima M, Nakano M, et al. Molecular phylogeographic studies on Paragonimus westermani in Asia. J Helminthol 2000; 74 : 315-22.

R.C. Mahajan

Postgraduate Institute of Medical Education & Research

Chandigarh 160012, India

e-mail: indurc@sify.com

Copyright Indian Council of Medical Research Jun 2005

Provided by ProQuest Information and Learning Company. All rights Reserved