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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 7  |  Issue : 2  |  Page : 103-106  

Seroprevalence of human cystic echinococcosis from North India (2004–2015)


Department of Medical Parasitology, Postgraduate Institute of Medical Education and Research, Chandigarh, India

Date of Acceptance01-Aug-2017
Date of Web Publication25-Sep-2017

Correspondence Address:
Rakesh Sehgal
Department of Medical Parasitology, Postgraduate Institute of Medical Education and Research, Chandigarh - 160 012
India
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DOI: 10.4103/tp.TP_15_17

PMID: 29114488

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   Abstract 

Context: Cystic echinococcosis (CE) caused by Echinococcus granulosus is a disease of a significant burden in India. The World Health Organization recommends the use of hospital data for population surveillance to measure the prevalence of CE.
Aim: The aim of this study was to estimate the seroprevalence of CE and to compare with previous prevalence rates to estimate the changing pattern in seroprevalence of CE.
Materials and Methods: A retrospective analysis of laboratory data of 3929 clinically and/or radiologically suspected cases of CE was carried out for 12 years from 2004 to 2015 and compared to the previous data from 1984 to 2003. The seroprevalence of anti-hydatid immunoglobulin G (IgG) was assessed by enzyme-linked immune sorbent assay. Casoni's intradermal skin test and microscopy on aspirated hydatid cyst fluid were also done. The statistical significance was assessed using Chi-square test and Fisher's t-test.
Results: Of the 3929 samples, 1124 (28.6%) were positive for specific anti-hydatid IgG antibody response, while of the 121 tested by Casoni's test, 56 (46.3%) were positive. The seropositivity of CE over the period of 12 years is rising. As compared to our previous data from 1984 to 2003, an overall significant increase in seropositivity was observed during 2004–2015 (28.6% vs. 15.0% in 1984–2003, P < 0.0001).
Conclusions: This study emphasizes the necessity of continuous surveillance and integrated control measures to prevent CE in humans and livestock across the country.

Keywords: Casoni's test, echinococcosis, epidemiology, India, seroprevalence, zoonosis


How to cite this article:
Zaman K, Mewara A, Kumar S, Goyal K, Khurana S, Tripathi P, Sehgal R. Seroprevalence of human cystic echinococcosis from North India (2004–2015). Trop Parasitol 2017;7:103-6

How to cite this URL:
Zaman K, Mewara A, Kumar S, Goyal K, Khurana S, Tripathi P, Sehgal R. Seroprevalence of human cystic echinococcosis from North India (2004–2015). Trop Parasitol [serial online] 2017 [cited 2019 Nov 11];7:103-6. Available from: http://www.tropicalparasitology.org/text.asp?2017/7/2/103/215503




   Introduction Top


Cystic echinococcosis (CE) is a disease of humans and livestock caused by Echinococcus granulosus. The accidental consumption of eggs shed in the feces of infected canines results in the development of one or several hydatid cysts, especially in the liver (70%) and lungs (20%), while rest 10% can occur almost anywhere in the body, namely, brain, musculature, heart walls, kidneys, orbit of the eye, and bone marrow.[1] CE is an endemic zoonosis in many countries of the world except Iceland and Greenland and is of important public health and socioeconomic concern in India. Several studies have shown CE to be an emerging or reemerging disease and it has a much wider geographic distribution than was previously believed.[1] The prevalence of CE in endemic areas is 1%–10%; however, the incidence rate in hospitals is about 1000 times less than the prevalence as only a small proportion of patients who develop severe symptoms seek medical care.[2] In India, CE is present in most parts of the country. A previous study from our center in North India has shown an overall seroprevalence of 15.1% over a period of 20 years in clinically suspected cases of CE.[3] CE may be responsible for a loss up to 3.6 million disability-adjusted life year worldwide.[4]

The diagnosis of CE is challenging because of the late manifestation of symptoms, chronic course of the disease, lack of diagnostic modalities, and nonavailability of these modalities in an endemic area.[5] Several radiological methods such as ultrasonography and computed tomography scan or magnetic resonance imaging may confirm the diagnosis in most of the cases. However, these techniques have limited use for multicavity cysts and solid mass or liver CE. In such cases, serological tests have proven to be helpful for a long time.[6] As per the recommendation by the World Health Organization, hospital data can be used to measure the prevalence of CE in a population.[4] In this study, we retrospectively analyzed the clinical and laboratory data of patients suspected of CE at our tertiary care hospital in North India over a period of 12 years from 2004 to 2015 and compared to the previous data from our center from 1984 to 2003.[3]


   Materials and Methods Top


The clinical and laboratory data of patients attending the outpatient departments or admitted to the wards of our tertiary care center, with a presumptive clinical and/or radiological diagnosis of CE, from January 2004 to December 2015 were analyzed and compared to the previous seroprevalence data from 1984 to 2003. The sera from 3929 patients were subjected to anti-hydatid immunoglobulin G (IgG) detection by enzyme-linked immune sorbent assay (ELISA) as described previously.[3] Casoni's intradermal skin test and microscopy of aspirated cyst fluid were performed in 121 and 521 patients, respectively, as described previously.[3] The Casoni's test was performed till 2009; after which the test was discontinued. The clinical details of 1023 admitted patients who were radiologically and/or surgically confirmed as cases of CE were obtained.

Statistical analysis

The sensitivity of diagnostic methods was calculated taking radiologically and/or surgically confirmed cases as reference standard using the standard formula. The significance of differences in seropositivity in 2004–2015 as compared to our previous data was assessed using Chi-square test, and significance of difference for Casoni's test's positivity was assessed using Fisher's t-test. The data were analyzed using the software SPSS version 20.0 (IBM, Hampshire, UK).


   Results Top


Of the 3929 clinically suspected patients, anti-hydatid IgG antibody response was positive in 1124 (28.6%) patients, of which 49.5% (557) were male and 50.5% (567) were female, thus showing similar rates of seropositivity in males and females. Of the 1124 patients, there were a higher percentage of adults (87.3%; 981) as compared to children (13.7%; 143). Casoni's test was performed on 121 of the 1953 patients till the year 2009, of which 56 (46.3%) were found positive. Microscopy of the aspirated cyst fluid was done on 521 of the 3929 patients, of which 153 (29.3%) were found positive.

The clinical data were available for 1023 surgically and/or radiologically confirmed patients, who were further analyzed for the study [Table 1]. All the 1023 patients were positive for anti-hydatid antibodies by ELISA. Casoni's test was performed on 41 of the 1023 seropositive patients, of whom 32 (78%) were found positive. The microscopy of aspirated fluid was done on samples from 390 cases, of which 110 (28.2%) revealed the presence of scolices and hooklets. Among these 1023 patients, the liver was the most commonly affected site (88.4%, 904) followed by lung (8.7%), spleen (1.2%), kidney (0.4%), and both liver and lung (1%).
Table 1: Seropositivity, Casoni's test, and microscopy results of 1023 surgically/radiologically confirmed cases

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It was observed that the seropositivity of CE over the period of 12 years is rising. As compared to our previous data from 1984 to 2003, an overall significant increase in seropositivity was observed in 2004–2015 (28.6% vs. 15.0% in 1984–2003, P < 0.0001). A similar increase was observed in the positivity of Casoni's test (46.3% in 2004–2009 vs. 24.8% in 1984–2003, P < 0.0001).[3]


   Discussion Top


Seroprevalence may not be an accurate estimate of disease burden; however, the WHO recommends that hospital cases represent a very useful and practical indicator of the incidence and success of control measures even though they underestimate the actual prevalence of the disease.[4] In this study, we retrospectively analyzed the seropositivity data of patients suspected of hydatid disease over a 12-year period (2004–2015) and compared it with our previous data of 20 years (1984–2003). All the confirmed CE patients in our study were found positive for anti-hydatid IgG antibodies. Serological tests have a very practical role in diagnosing CE. ELISA format is more suitable and acceptable for initial screening owing to its higher sensitivity and simplicity of use.[7],[8] We also performed Casoni's test which is still commonly used at many centers in endemic countries of the developing world for diagnosis of CE because of its simplicity and quick interpretation within 30 min although it has a low specificity due to cross-reactivity to other helminths. The sensitivity of Casoni's test has been found to be 63.6% alone and 90.9% when combined with indirect hemagglutination assay for the diagnosis of CE.[9] Another study has shown 59% sensitivity of Casoni's test when compared to ELISA which had 90% sensitivity.[10] Due to the risk of hypersensitivity reactions during Casoni's test, the test was later discontinued. Microscopic examination of hydatid cyst fluid aspirates is also diagnostic, the positivity of microscopy in our study was found to be 29.3%. However, aspiration of hydatid fluid is associated with risk of anaphylaxis and secondary CE in adjacent organs and hence is not a preferred test.

As compared to our previous data from 1984 to 2003, a significant increase in seropositivity rate of 13.6% (P < 0.0001) was observed. The seropositivity study conducted during 1984–2003 was analyzed in two periods, i.e., from 1984 to 1998 and 1999–2003 and it was observed that within the two time zones, the seropositivity had shown a significant increase from 10.9% to 23.1% (P < 0.001).[3] This rise in seropositivity was observed to be persistent in the present study period of 2004–2015. The reason for this increase in seropositivity in the later time periods, i.e., post-1999, as compared to the pre-1999 time periods is not very clear though it could be attributed to an increased awareness of the primary health-care physicians and better referrals to the tertiary care centers, encouraging more patients suffering from clinical symptoms to seek medical help.[7],[10] However, the exact reasons for increasing seroprevalence can only be explored in large well-planned studies. The data from other parts of the country have shown a higher prevalence of CE in rural areas where a large number of people are involved in livelihood activities associated with the disease such as farming and animal breeding.[11],[12]


   Conclusion Top


The rising seropositivity for CE over years as observed in our analysis emphasizes the necessity of robust implementation of control measures to prevent disease-associated morbidity and mortality. The disease can be controlled by preventing transmission of the parasite by improving animal husbandry practices such as restricting home slaughter of sheep and other livestock, control stray dog population, limiting the areas where dogs are allowed, and preventing them from consuming meat infected with cysts. Educating the public about simple personal hygiene measures such as washing hands with soap and warm water after handling dogs, before handling food, and preventing direct consumption of food or water that may have been contaminated by fecal matter from dogs may prove extremely effective in breaking the chain of transmission of this important medical entity.[13] At the same time, mounting active surveillance to assess the disease prevalence in humans as well as livestock across the country will be instrumental in understanding the epidemiology of the disease and aid its control.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Grosso G, Gruttadauria S, Biondi A, Marventano S, Mistretta A. Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World J Gastroenterol 2012;18:1425-37.  Back to cited text no. 1
    
2.
Budke CM, Carabin H, Ndimubanzi PC, Nguyen H, Rainwater E, Dickey M, et al. A systematic review of the literature on cystic echinococcosis frequency worldwide and its associated clinical manifestations. Am J Trop Med Hyg 2013;88:1011-27.  Back to cited text no. 2
    
3.
Khurana S, Das A, Malla N. Increasing trends in seroprevalence of human hydatidosis in North India: A hospital-based study. Trop Doct 2007;37:100-2.  Back to cited text no. 3
    
4.
Eckert J, Gemmell MA, Soulsby EJ. FAO/UNEP/WHO Guidelines for Surveillance, Prevention and Control of Echinococcosis/Cystic Echinococcosis. Geneva: World Health Organization; 1981. Available from: http://www.trove.nla.gov.au/version/22198582. [Last accessed on 2015 May 15].  Back to cited text no. 4
    
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Giri S, Parija SC. A review on diagnostic and preventive aspects of cystic echinococcosis and human cysticercosis. Trop Parasitol 2012;2:99-108.  Back to cited text no. 5
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6.
Sbihi Y, Rmiqui A, Rodriguez-Cabezas MN, Orduña A, Rodriguez-Torres A, Osuna A. Comparative sensitivity of six serological tests and diagnostic value of ELISA using purified antigen in hydatidosis. J Clin Lab Anal 2001;15:14-8.  Back to cited text no. 6
    
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Craig PS, Budke CM, Schantz PM, Li T, Qiu J, Yang Y, et al. Human echinococoosis: A neglected disease? Trop Med Health 2007;35:283-92.  Back to cited text no. 7
    
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Mandal S, Mandal MD. Human cystic echinococcosis: Epidemiologic, zoonotic, clinical, diagnostic and therapeutic aspects. Asian Pac J Trop Med 2012;5:253-60.  Back to cited text no. 8
    
9.
Ray R, De PK, Karak K. Combined role of Casoni test and indirect haemagglutination test in the diagnosis of hydatid disease. Indian J Med Microbiol 2002;20:79-82.  Back to cited text no. 9
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Tenguria RK, Naik MI, Bhat JA, Fomda BA. Comparison of Casoni's intradermal test with enzyme-linked immunosorbent assay in the diagnosis of human hydatid disease. Int J Curr Sci 2013;7:104-9.  Back to cited text no. 10
    
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Rao SS, Mehra B, Narang R. The spectrum of hydatid disease in rural central India: A 11-year experience. Ann Trop Med Public Health 2012;5:225-30.  Back to cited text no. 11
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Akther J, Khanam N, Rao S. Clinico epidemiological profile of hydatid diseases in central India, a retrospective and prospective study. Int J Biol Med Res 2011;2:603-6.  Back to cited text no. 12
    
13.
Centers for Disease Control and Prevention. Echinococcosis-Prevention and Control [CDC website]. Available from: http://www.cdc.gov/parasites/echinococcosis/prevent.html. [Last accessed on 2015 May 15].  Back to cited text no. 13
    



 
 
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