|Year : 2012 | Volume
| Issue : 3 | Page : 225-230
|The spectrum of hydatid disease in rural central India: An 11-year experience
Siddharth S Rao, Bhupendra Mehra, Ravindra Narang
Department of Surgery, Mahatma Gandhi Institute of Medical Sciences (MGIMS), Sewagram, Wardha, Maharashtra - 442 102, India
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|Date of Web Publication||17-Jul-2012|
| Abstract|| |
Background: Hydatid disease or Echinococcosis is a zoonotic disease caused by the larva of Echinococcus species and is one of the oldest known diseases to man. The disease has a worldwide distribution and is also well recognized and documented in India. Aims: This study was carried out with the aim of describing the epidemiology (demography, clinical presentation, imaging characteristics, and in-hospital course) of Cystic Echinococcosis (CE) in central India. Materials and Methods: The clinical study of hydatid disease was conducted as a single case series including both historical and current cases at the Mahatma Gandhi Institute of Medical Sciences, Central India. The study investigator screened all the histopathology records from 1997 to 2004 for historical case group. The current case group extended from 2005 to 2007. The historical case group included 91 patients and the current case group had 26 surgically treated patients. Results: Females were the dominant sex affected by the disease. Hydatid of the liver was more common, especially in the right lobe. Pain in the abdomen was the most common presenting complaint. Lump in the abdomen was the most common clinical finding. Patients with pulmonary hydatid presented to the hospital earlier than the patients with abdominal hydatid (P=0.03). Partial pericystectomy and external drainage was the most commonly performed surgery. The most common postoperative complication was wound infection. Conclusions: This study highlights the epidemiology of CE in the rural region of Indian subcontinent. The population in rural areas are more exposed to zoonotic diseases. Proper education, creating awareness, and implementing strict rules regarding the disposal of remains of slaughtered animals can help eradicate this disease.
Keywords: Cystic echinococcosis, hydatid cyst, hydatid disease, partial pericystectomy, zoonotic disease
|How to cite this article:|
Rao SS, Mehra B, Narang R. The spectrum of hydatid disease in rural central India: An 11-year experience. Ann Trop Med Public Health 2012;5:225-30
|How to cite this URL:|
Rao SS, Mehra B, Narang R. The spectrum of hydatid disease in rural central India: An 11-year experience. Ann Trop Med Public Health [serial online] 2012 [cited 2020 Jul 10];5:225-30. Available from: http://www.atmph.org/text.asp?2012/5/3/225/98624
| Introduction|| |
Hydatid disease or Echinococcosis is a zoonotic disease caused by the larvae (metacestode) of the cestode species of the genus Echinococcus like E. granulosus, E. multilocularis, E. vogeli or E. oligarthus. Classical Cystic Echinococcosis (CE) is caused by E. granulosus complex, while E. multilocularis and E. vogeli are responsible for alveolar echinococcosis and polycystic echinococcosis, respectively.  The study of E. granulosus species has revealed identification of substantial phenotypic and genetic variability and several strains.  All identified strains utilize dogs and other canids as definitive hosts, but differ in the choice of intermediate host, geographic distribution, adult and metacestode morphology, maturation time in definitive hosts, organ localization of metacestode, and protoscolex production.  At least, seven of nine E. granulosus genotypes are infective to humans. Globally, most human cases of CE are caused by the sheep strain (G1) of E. Granulosus. In India G1 and G5 (cattle strain) strain of E. granulosus have been frequently associated with CE.  G2 genotype (Tasmanian sheep strain) in buffalo has been reported from India.  Humans acquire primary CE by ingestion of E. granulosus eggs excreted by infected carnivores. The infection may be acquired by contact with infected definitive hosts, egg-containing feces, or egg-contaminated plants or soil followed by direct hand-to-mouth transfer.  Dog ownership has not been found to be a risk factor in seropositive individuals, indicating an indirect contact with dog feces in the environment.  Eggs can also be ingested with vegetables, salads, uncooked fruits, drinking water,  and other plants that become contaminated.
Cystic echinococcosis has a multitude of clinical presentations ranging from asymptomatic disease to acute emergencies. Hydatid cysts have been reported from every part of the human body like liver, lungs, peritoneum, bones, ovaries, breast, brain, etc. Intact and small-sized cysts have no specific characteristic symptoms. Their clinical manifestations depend on the organ involved; site and size of the cyst; interaction between the expanding cysts and the adjacent organ structures and complications related to cyst rupture; spread of protoscoleces; and bacterial infection.The presentation may also be severe in cases of infection or rupture of the cyst. ,,,,,,,
According to study in 2009, it is estimated that the worldwide incidence of cystic echinococcosis is about 100,000-300,000 cases annually  and is known to occur in all continents and in at least 100 countries.  Increased prevalence of the parasite are found in parts of Europe, around Mediterranean region (variable between 1 and 8 per 100,000), the Russian Federation, China, Africa (prevalence >3%), Australia, and South America (9.2 per 100,000 population).  In East Africa, Kazakhstan, Kyrgyzstan, Northwest-China, and Tibet, it has been observed that the rural populations are particularly at risk.  Iceland and Greenland are free of echinococcosis, while only sporadic cases in domestic animals have been documented in New Zealand, Tasmania, southern Cyprus, Pacific region, and Caribbean.  There has been an increase in seropositive cases of echinococcosis from 10.97% in 1984-1998 to 23.12% in 1999-2003; Casoni's test revealed a similar increase in cases, from 21.38% to 33.83% during the same period in northern India.  The highest prevalence of human hydatid disease in India has been reported from Andhra Pradesh, Saurashtra, and Tamil Nadu.  The prevalence of the disease is reported to be high in food animals in India. 
CE has been studied extensively throughout the world, especially regarding the strain involved, various organs affected, and various surgical options for treatment. However, data from Indian subcontinent is lacking. In the past, there have been few Indian studies describing the prevalence of disease, organs involved, and presenting symptoms. ,,,,,,,,, But there is a paucity of data in terms of clinical presentation, risk factors, investigations, and hospital course. Also, these studies were done about two decades ago and are not truly reflective of current situation. Hence, we wanted to elucidate the basic epidemiology of the disease in our region with reference to the current context. This study was carried out with the aim of describing the epidemiology (demography, clinical presentation, imaging characteristics, and in-hospital course) of CE in central India.
| Materials and Methods|| |
The clinical study of CE was conducted in MGIMS, Wardha, Central India. MGIMS is a 750-bedded tertiary care hospital attached to a medical college situated in the rural area, which has a high zoonotic exposure. The study was conducted from 1997 to 2007. All patients admitted to our hospital have a unique Medical Record Department (MRD) number, which is same for their hospital records as well for all investigations including histopathology. Upon discharge each in-hospital record gets listed in the international classification of diseases (ICD) 10 coding as per their discharge diagnosis. All records are electronically maintained. All patients with abdominal or lung mass are admitted to the hospital and after being examined by consultants, their management is planned.
This was a single case series including both historical and current cases over a period of 11 years from 1997 to 2007. For the historical cases, all the histopathology records from 1997 to 2004 were screened by the study investigator. We included all patients with confirmed histopathology diagnosis of CE (91 cases). We excluded patients whose hospital records were not available (5 cases).
The current cases group extended from 2005 to 2007. All consecutive surgical admissions were screened by the study investigator before discharge from the hospital. The study investigator was informed about all cases with a preoperative diagnosis of CE and those who were taken up for surgical intervention by the respective consultants. Of these, all patients with histopathologicaly confirmed CE were included in the study (26 cases). All patients of suspected CE who did not undergo surgical intervention or whose histopathology did not confirm the diagnosis of CE were excluded from the study.
For the historical case group, the hospital records of all patients included in the study were reviewed by the study investigator and the information was abstracted. For the group of current cases, all patients included in the study were interviewed by the study investigator and information was recorded. For both groups, information was documented under the following headings: (a) Demographic data (age, gender, residence address, occupation); (b) Clinical features (duration of lump in the abdomen in months, site of lump in the abdomen, duration of pain in the abdomen in months, cough and its duration in days, chest pain, jaundice, vomiting, fever); (c) Clinical examination findings (pallor, liver span, presence of hydatid thrill); (d) Investigations (complete hemogram with total leucocyte count, absolute eosinophil count); (e) Ultrasound study (site of CE, size of the cyst in centimeter, complications due to CE); (f) Type of surgical intervention; and (g) Post-operative complication.
For both groups, only histopathologicaly confirmed cases were included in the study. All tissues after surgery are sent to the histopathology section of department of pathology, where after grossing they are submitted for routine histopathology processing. Criteria for diagnosis of cystic hydatid disease are visualisation of a lamellated structure of a cyst wall, germinal layer, scolices and protoscolices on Hematoxylin and Eosin (H&E)-stained paraffin-embedded sections.
All patients in the current case group were included only after written informed consent. A waiver of consent for the historical cases group was taken by institutional ethics committee. The study was approved by institutional ethics committee.
We entered the data electronically by Microsoft Excel and analyzed it by STATA software (Version 10, Stata Corporation, Texas, USA), and performed a descriptive analysis of all collected variables. Mean [Standard Deviation (SD)] as a measure of central tendency for continuous variables and number (proportions) for discrete variables were used. We analyzed normally distributed continuous variables by Student's t test, proportions by Chi-square test.
The size of the cyst on ultrasound imaging was reclassified as < 5 cm, 5-10 cm, and >10 cm by the maximum diameter, for the purpose of analysis.
All patients with CE anywhere in the abdomen (liver, spleen, kidney, peritoneum, omentum) were reclassified as abdominal hydatid for the sake of analysis and others with CE in lungs as pulmonary hydatid.
| Results|| |
A total of 117 patients were included in the study period (1997-2007). A total of 91 cases were from the historical cases group and 26 cases from the current cases group. Five cases from the historical cases group were excluded due to non-availability of hospital records. The basic demographic details of all patients, clinical presentation, and complications are described in [Table 1].
There were two peaks of disease occurrence in the study population. One peak was seen at the age of about 20 years and the other at about 40 years [Figure 1]. Mean age of patients with abdominal hydatid was 37.2 years [Confidence Interval (CI, 33.79 - 40.61)]. Mean age of patients with pulmonary hydatid was 31.4 years (95% CI, 22.75 - 40.08) [Figure 2]. Abdominal hydatid was seen more often in females than males and pulmonary hydatid was more common in males, the difference was statistically significant (P=0.004).
|Figure 2: Comparison of age distribution of patients with pulmonary and abdominal hydatid. The boxes represent the population with the centre line representing the means. The horizontal lines above and below represent the 95% confidence intervals|
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The main presenting symptom of the study population was pain in abdomen (89.47%) followed by lump in abdomen (85.26%). Pulmonary hydatid in the study population presented earlier than abdominal hydatid, with mean duration of symptoms 0.35 month for pulmonary hydatid and 8.15 month for abdominal hydatid (P=0.03).
Eosinophilia was observed in 74.36% patients with a mean Absolute Eosinophil Count (AEC) of 390.52 (±357.85). Absolute eosinophil count of above 1000 cells/cm 3 was seen in five patients (5.75%). AEC of 501-1000 cells/cm 3 was seen in 35 patients (40.23%). Serum bilirubin above 2 mg/dl was seen in 8 patients (6.84%). Casoni's test was not done in any of the patients.
Of the total study population of 117 patients, 106 (90.59%) had single organ involvement and 11 (9.40%) had more than one organ involved. Liver was involved in 88 patients (75.21%) either solitarily or in association with other organs. Lung involvement was seen in 17 patients (14.53%) either solitarily or in association with other organs.
A total of 31 patients (26.49%) presented with complications of the hydatid cyst [Table 2]. None of the patients died due to complications of the disease. The most common post-operative complication that we encountered was wound infection, which was seen in 22 patients (18.80%). Residual cavity was seen in four patients (3.42%). These patients had to be discharged on drainage. The fistula in both the cases healed gradually without any further intervention. There was a single patient with burst abdomen, who was managed by tension suturing. Three patients who were operated for lung hydatid had prolonged Intracranial (IC) drainage due to fistula, which healed eventually in all cases.
| Discussion|| |
CE has a wide geographical distribution and is a cause of serious concern in the endemic region due to severe disease, increase in morbidity and considerable economic loss. , Our study provides an insight into the epidemiology of CE in central India and exemplifies the problems that echinococcosis presents especially in rural community.
Our study revealed that of all patients of CE presenting to our hospital, this disease commonly affects patients in their second and fourth decade, is seen frequently in farmers and has a female preponderance. In our study, patients with CE presented commonly with pain in abdomen followed by lump in abdomen. Patients with pulmonary hydatid presented to the hospital earlier as compared to abdominal hydatid. Liver was the most commonly affected organ followed by lung. Infection was the most common postoperative complication of CE.
In our study population, CE was commonly seen at about 20 and 40 years. Papadimitriou et al. reported 25.55% patients in the age group of 21-30 years and 24.67% patients in the age group of 31-40 years. Mehta et al. reported 27.08% in the second and third decade and 18.75% in the fourth decade. Irshadullah et al. also reported similar distribution with the highest percentage of patients in the age group of 21-30 years (25.83%) and 20% in the fourth decade. It has been consistently seen in various studies through the years and confirmed by our study that this disease in seen in young population who are in their active years.
The risk factors indentified in our study were farming and female sex, which was identical to findings of previous studies. A study done in Xinjiang province of People's Republic of China, during 1951-1990, found that maximum number of cases was detected in farm laborers.  Farming in rural areas of India involves physical labor and working with hands in the soil and contact with livestock. Numerous stray dogs are found here, and hence contamination of soil with dog feces is a common occurrence. This may probably be the reason for transmission of disease by contact with egg-contaminated plants or soil followed by direct hand-to-mouth transfer. This finding supports the hypothesis of significant environmental contamination in open areas wherein parasite eggs survive and remain infective for months under favourable conditions such as high humidity and low temperature. 
Our study showed a predominance of female suffering with CE, of all patients with the disease presenting to the hospital. It can be postulated that since in the rural community, females are more involved in activities related to farming and herding livestock, they are also more likely to be affected by the disease due to environmental contamination. An epidemiological study of echinococcosis in China also found a predominance of disease in females due to farming and herding of livestock. 
Our study established that pain and lump in the abdomen were the common presenting features of CE. According to Balik et al. and Jacob et al.,  pain in abdomen has been the most common presenting symptom (74.01% and 85%, respectively). This was followed by the presentation of lump in abdomen, which was seen in 54.93% cases by Balik et al. and 57.5% cases by Jacob et al.  Contrary to this, Mehta et al. concluded that lump in abdomen was the most common presentation in hydatid disease (54.16%). Balik et al. also found that about one-fifth (22.69%) of their patients had fever and 5.92% patients had jaundice. Jacob et al. also had eight patients (20%) with jaundice and nine patients (22.5%) had fever.
The majority of the hydatid cysts in man are seen in the liver (approximately 75%) because it is the first filtering system for all the ingested ova, which enter the portal system.  A few of these ova that have an average size of 35 μm escape the sinusoidal system of the liver to enter the systemic circulation and pass through the lungs, which acts as a second filter for the ova, making it the second most common site for the disease (approximately 15%).  Hydatid disease of the lung occurs from the larvae, which get trapped in the arterial capillaries of the lung. Occasionally, lung may be the site of secondary metastatic hydatidosis by rupture of a liver cyst. 
Even in the liver, it has been suggested that 85% of the cysts occurred in the right lobe and 15% in the left lobe.  Most of the authors ,, have reported maximal involvement of the liver, with the lung being the second most common site, a trend that has been duly reflected in our study. Interestingly, however, in a study carried out in the Vidharbha region of Maharashtra in India reported more number of lungs than liver being affected with hydatid disease.  A study carried out in Mediterranean region including 459 patients found liver involvement in 316 patients (68.8%), followed by involvement of lung in 79 patients (17.2%).  Another study done in 15,289 Chinese surgical cases observed liver involvement in 11,499 patients (75.2%) followed by lung involvement in 3432 patients (22.4%). 
Although other modalities of treatment of hydatid disease like Percutaneous Aspiration, Injection and Reaspiration (PAIR), [2,9] Percutaneous Evacuation (PEVAC),  Video-Assisted Thoracic Surgery (VATS),  and laparoscopy  have been in vogue and have produced good results in the circumstances where they are indicated, we have treated all our patients by conventional surgery. In a study, both PAIR and surgery were equally effective in reducing the cyst size at 18-month follow-up.  The most commonly performed surgery in our series was partial pericystectomy with external drainage. There are certain distinct advantages with this technique, which have also been highlighted by Al-Hureibi,  who has pointed out that the external drainage would not only manage any remnants that may have been inadvertently left behind during surgery, but the drain can also be used for flushing the cavity in cases of infection and may be used for contrast study to follow the course of obliteration of the cavity. No mortality was seen in our series. Consequently, the most common complication seen was wound infection. Pre- and postoperative chemotherapy with Albendazole was given to all our patients because of its proven effects in sterilizing the cyst, decreasing the chance of anaphylaxis, decreasing the tension in the cyst wall (thus reducing the risk of spillage during surgery), and in reducing the recurrence rate postoperatively. ,
This study highlights the epidemiology of CE in the rural region of Indian subcontinent. The population in rural areas are more exposed to the zoonotic diseases due to their occupation, which is mostly farming. As with other zoonotic diseases, prevention plays an important in the overall management of this disease. Environmental contamination of the soil by dog feces seems an important way of transmission of disease in rural community. Careful washing of hands and food can help tremendously in decreasing this transmission. Proper education, creating awareness, and implementing strict rules regarding disposal of remains of slaughtered animals can also help eradicate this disease. 
| References|| |
|1.||Richter J, Orhun A, Grüner B, Müller-Stöver I, Reuter S, Romig T, et al. Autochthonous cystic echinococcosis in patients who grew up in Germany. Eurosurveillance 2009;14:1-7. |
|2.||Eckert J, Deplazes P . Biological, epidemiological, and clinical aspects of echinococcosis: A zoonosis of Increasing Concern. Clin Microbiol Rev 2004;17:107-35. |
|3.||Bhattacharya D, Bera AK, Bera BC, Maity A, Das SK. Genotypic characterisation of Indian cattle, buffalo and sheep isolates of Echinococcus granulosus. Vet Parasitol 2007;143:371-4. |
|4.||Larrieu EJ, Costa MT, del Carpio M, Moguillansky S, Bianchi G, Yadon ZE. A case-control study of the risk factors for cystic echinococcosis among the children of Rio Negro province, Argentina. Ann Trop Med Parasitol 2002;96:43-52. |
|5.||Himsworth CG, Jenkins E, Hill JE, Nsungu M, Ndao M, Andrew Thompson RC, et al. Emergence of sylvatic echinococcus granulosus as a parasitic zoonosis of public health concern in an indigenous community in Canada. Am J Trop Med Hyg 2010;82:643-5. |
|6.||Yalçinkaya I, Er M, Ozbay B, Uðraþ S. Surgical treatment of hydatid cyst of lung: review of 30 cases. Eur Respir J 1999;13:441-4. |
|7.||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. |
|8.||Tiwary AK, Tiwary RN. Hydatid disease in Chotanagpur region of South Bihar. Indian J Surg 1988;50:14-8. |
|9.||Nepalia S, Joshi A, Shende A, Sharma SS. Management of echinococcosis. J Assoc Physicians India 2006;54:458-62. |
|10.||Sibal RN, Singh P. Hydatid disease in Himachal Pradesh. J Indian Med Assoc 1974;63:211-3. |
|11.||Upadhyaya H, Rai P, Shah PK. Clinical study of hydatid disease in Jamnagar. J Indian Med Assoc 1974;63:213-6. |
|12.||Riberio W. Hydatid disease in Jammu province. Indian J Surg 1975;37:244-8. |
|13.||Reddy DB, Suvarnakumari G, Raju GC. Hydatid disease in Kurnool. J Indian Med Assoc 1979;63:5-8. |
|14.||Mehta RB, Ananthkrishnan N, Gupta BK, Srivastava KK, Mehdiratta KS, Satya P. Hydatid disease in Pondicherry. Indian J Surg 1982;44:88-94. |
|15.||Parija SC, Rao RS, Badrinath S, Sengupta DN. Hydatid disease in Pondicherry. J Trop Med Hyg 1983;86:113-5. |
|16.||Bhobhate SK, Kedar GP, Kher AV. Incidence of hydatid disease in Vidharbha division. Indian J Surg 1984;46:162-4. |
|17.||Sivalingam P, Gnanapa Y, Duraipandy P, Raman C. Hydatid disease in a teaching hospital. Indian J Surg 1985;47:387-91. |
|18.||Irshadullah M, Nizami WA, Macpherson CN. Prevalence of human hydatidosis in Uttar Pradesh. J Commun Dis 1989;21:114-22. |
|19.||Vamsy M, Parija SC, Sibal RN. Abdominal hydatidosis in Pondicherry, India. Southeast Asian J Trop Med Public Health 1991;22S:365-70. |
|20.||Craig PS, Rogan MT, Campos-Ponce M. Echinococcosis: Disease, detection and transmission. Parasitology 2003;127S:5-20. |
|21.||McManus DP, Zhang W, Li J, Bartley PB. Echinococcosis. Lancet 2003;362:1295-304. |
|22.|| Papadimitriou J. The surgical treatment of hydatid disease of the liver. Br J Surg 1970;57:431-3. |
|23.||World Health Organization Office International des Epizooties. WHO/OIE manual on echinococcosis in humans and animals: A public health problem of global concern. World Organization for Animal Health, Paris, France: 2001. |
|24.||Veit P, Bilger B, Schad V, Schäfer J, Frank W, Lucius R. Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 1995;110:79-86. |
|25.||Balik AA, Baþoðlu M, Celebi F, Oren D, Polat KY, Atamanalp SS, et al. Surgical treatment of hydatid disease of the liver: Review of 304 cases. Arch Surg 1999;134:166-9. |
|26.||Langer JC, Rose DB, Keystone JS, Taylor BR, Langer B. Diagnosis and management of hydatid disease of the liver: A 15 year North American experience. Ann Surg 1984;119:412-7. |
|27.||Saidi F. Surgery of Hydatid Disease. 1 st ed. Philadelphia: W B Saunders Company Ltd; 1976. |
|28.||Morar R, Feldman C. Pulmonary echinococcosis. Eur Respir J 2003;21:1069-77. |
|29.||Al-Hureibi AA, Amert A, Al-Hureibi MA, Sharawee Z. Hepatic hydatid cysts: Presentation and surgical management in Yemen. J R Coll Surg Edinb 1992;37:229-31. |
|30.||Schipper HG, Lameris JS, van Delden OM, Rauws EA, Kager PA. Percutaneous evacuation (PEVAC) of multivesicular echinococcal cyst with or without cystobiliary fistulas which contain non drainable material: First results of a modified PAIR method. Gut 2002;50:718-23. |
|31.||Uchikov AP, Shipkov CD, Prisadov G. Treatment of lung hydatosis by VATS: A preliminary report. Can J Surg 2004;47:380-1. |
|32.||Georgescu OS, Dubei L, Tarcoveanu E, Bradea C, Lazescu D, Crumpei F, et al. Minimally invasive treatment of hepatic hydatid cysts. Rom J Gastroenterol 2005;14:249-52. |
|33.||Khuroo MS, Wani NA, Javid G, Khan BA, Yattoo GN, Shah AH, et al. Percutaneous drainage compared with surgery for hepatic hydatid cysts. N Engl J Med 1997;337:881-7. |
|34.||Goel MC, Agarwal MR, Misra A. Percutaneous drainage of renal hydatid cyst: Early results and follow-up. Br J Urol 1995;75:724-8. |
|35.||Kune GA, Morris DI. Hydatid disease In: Schwasyz, Ellis, editors. Maingot's Abdominal Operations. 9 th ed. Appleton and Lange; 1989. p. 1225-40. |
|36.||Beard TC. The elimination of Echinococcus from Iceland. Bull World Health Organ 1973;48:653-60. |
Siddharth S Rao
Department of Surgery, MGIMS, Sewagram, Wardha, Maharashtra - 442 102
Source of Support: None, Conflict of Interest: None
[Figure 1], [Figure 2]
[Table 1], [Table 2]
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