Edited by: Alfonso J. Rodriguez-Morales, Technological University of Pereira, Colombia
Reviewed by: Ana Afonso, University of São Paulo, Brazil; Mario Santoro, Stazione Zoologica Anton Dohrn, Italy
This article was submitted to Infectious Diseases – Surveillance, Prevention and Treatment, a section of the journal Frontiers in Public Health
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Echinococcosis is one of the 20 neglected zoonotic diseases (NZD) prioritized by the World Health Organization (WHO) (
Conditions such as poor hygiene and failure to wash contaminated food facilitate the spread of CE infection in the human population (
A study was conducted in Islamabad and Rawalpindi districts of Pakistan.
Islamabad, the capital city of Pakistan, is located in Pothohar Plateau (33.43°N 73.04°E) at 540 m (1,770 ft.) above the sea level. 505 km2 of this area is urban whereas 401 km2 of is rural (
The data was collected from January to July, 2017(for 6 months). Butcher shops in different areas of Rawalpindi and Islamabad were visited twice per month to collect the data on prevalence and presence of stray dogs in the slaughterhouses.
A cross-sectional survey was designed to get the recent data hydatid cyst incidence. The data was collected from butcher shops of the twin cities. Questionnaire was designed for butcher shops/slaughterhouses among urban and rural areas which was descriptive in nature. The information about stray dogs present along the territory of slaughterhouses/butcher shops were recorded.
The data on presence of stray dogs, CE prevalence in animals, as well as on socio-demographic characteristics was collected using questionnaires. Moreover, data was analyzed to determine the factors associated with the risk of CE. As there is no local specific name of this disease, pictures of cysts in animal organs and of infected humans were shown to the participants to identify the disease better. The knowledge of the participants was measured as binary outcomes (
In order to examine hydatid cysts properly, following parameters were carried out: Types of cysts (sterile, fertile, calcified, or under-developed), organ specificity (lungs and liver), and prevalence of hydatidosis. Presence of cysts in different organs was analyzed by routine post-mortem of the carcass. The cysts were dissected and collected into sterile containers separately on organ basis for further description.
Sterile scalpel blades were used for cyst incision. The fluid present inside these cysts was used to check the existence of protoscoleces either in the form of brood capsule (closes to the germinal layer) or in the cyst fluid considering as a fertility indicative. Viability test was performed on fertile cysts. In viability test a drop of fluid from cyst containing the protoscoleces was observed under microscope to check amoeboid like peristaltic movements. For clear microscopic observations equal volume of 0.1% aqueous eosin solution was also mixed with equal volume of fluid containing the protoscoleces. Sterile hydatid cysts were characterized on the basis of inner lining, generally smooth with a slight turbid enclosed fluid otherwise rough calcified cyst with no or less fluid (
Polyvinyl-lactophenol was used for mounting protoscoleces cysts. Hooks damage was prevented by applying gentle pressure on cover slip. A calibrated eye-piece micrometer was used for all measurements under oil immersion. Morphometric analysis was done as described by Hobbs et al. (
Data was analyzed as described previously (
Data was collected for CE from 123 butcher's shops in Rawalpindi and Islamabad, Pakistan. The slaughtering rate in the butcher's shops was 2–10 animals/day including cattle, goat, sheep, and buffaloes. Overall prevalence of CE in the slaughterhouses/butcher shops was 2.77% (300/10,800) according to this survey. Prevalence was higher in buffaloes followed by cattle, sheep, and goat, respectively. The site of infection, number of cysts and kind of cysts are shown in
Overall prevalence (%) of hydatidosis in various organs of slaughtered Cattle, Buffalo, Goat, and Sheep.
Cattle | 3,845 | 132 | 3.43 | ✓ | ✓ | ✓ | 103 (78) | 29(22) | 73 (55.3) | 31 (23.48) | 19 (14.39) | 9 (6.81) |
Buffalo | 1,103 | 58 | 5.25 | ✓ | ✓ | ✓ | 47 (81) | 11(19) | 48(82) | 5(8.62) | 4(6.89) | 1(1.72) |
Goat | 4,307 | 76 | 1.76 | ✓ | ✓ | 68 (89) | 08 (11) | 37 (48.68) | 21 (27.63) | 15 (19.73) | 3 (3.94) | |
Sheep | 1,545 | 34 | 2.20 | ✓ | ✓ | 34 (100) | – | 19 (55.88) | 3(8.82) | 7(20.58) | 5(14.7) | |
Total | 10,800 | 300 | 2.77 | 252 (84) | 48 (16) | 177 (59) | 60 (20) | 45(15) | 18(6) |
The parameters which were observed to check protoscolex rostellar hook morphology in infected animals were total hooks number, their total length (μm) of hooks and blade length (μm) as shown in
Rostellar hooks morphology of protoscoleces in infected animals.
Total No. of Hooks (NH) | 29.21 ± 1.13 | 26.03 ± 1.17 | 21.00 ± 1.06 | 27.80 ± 1.11 |
Large Hook Length (LTL) (μm) | 24.02 ± 1.03 | 18.37 ± 0.96 | 27.12 ± 0.91 | 19.78 ± 1.02 |
Large Hook blade Length (LBL) (μm) | 15.21 ± 0.44 | 16.02 ± 0.54 | 9.77 ± 0.57 | 10.06 ± 0.38 |
Small Hook Length (STL) (μm) | 19.54 ± 1.03 | 17.97 ± 1.00 | 11.22 ± 0.77 | 13.15 ± 0.72 |
Small Hook Blade Length (SBL) (μm) | 8.9 ± 0.56 | 6.9 ± 0.30 | 9.30 ± 0.38 | 7.2 ± 0.37 |
Protoscoleces hooks number was observed and it was found that total number was 29.21 ± 1.13 in cattle origin, 26.03 ± 1.17 in buffalo origin, 21.0 ± 1.06 in goat origin, and 27.80 ± 1.11 in sheep origin as shown in
Protoscoleces large hooks was observed for total length (micrometers, μm) and it was found that it was 24.02 ± 1.03 in cattle origin, 18.37 ± 0.96 in buffalo origin, 27.12 ± 0.91 in goat origin, and 19.78 ± 1.02 in sheep origin. In goat origin large hook length was maximum (27.12 ± 0.91) and in case of buffalo origin it was minimum (18.37 ± 0.96).
Protoscoleces blade length of large hooks on was observed as 15.21 ± 0.44 in cattle originated infections, 16.02 ± 0.54 in buffalo originated infections, 9.77 ± 0.57 in goat origin, and 10.06 ± 0.38 in sheep origin as shown in
Protoscoleces of small hooks total length was observed as 19.54 ± 1.03 in cattle, 17.97 ± 1.00 in buffalo, 11.22 ± 0.77 in goat, and 13.15 ± 0.72 in sheep origin as shown in
Protoscoleces small hooks blade length on was recorded as 8.9 ± 0.56 in cattle origin, 6.9 ± 0.30 in buffalo origin, 9.30 ± 0.38 in goat origin, and 7.2 ± 0.37 in sheep origin. In goat origin SBL was maximum (9.30 ± 0.38), while in case of buffalo origin it was minimum (6.9 ± 0.30).
In the present study the number of stray dogs were recorded in all 123 slaughterhouse/butcher shops. It ranged from 1 to 5 dogs/site. The main contributing factor to the spread of CE was the large number of stray dogs (
Potential risk factors analysis of CE.
1 | Ever heard about Zoonoses | 04 | 119 |
2 | Presence of stray dogs inside the slaughter house/butcher shop | 107 | 16 |
3 | Proper facilities to dispose animals offals in slaughter house/butcher shop | 04 | 119 |
4 | Discard of infected organs (Lungs/Liver) at the site of slaughtering | 121 | 02 |
5 | Access of stray dogs to the infected organs | 121 | 02 |
6 | Stray dogs were fed with useless meat (Infected) | 112 | 11 |
7 | Stray dogs are ever vaccinated | 02 | 122 |
8 | Cystic Echinococcosis is spreaded from dogs? | 01 | 23 |
9 | Veterinary supervision of slaughtered animals | 04 | 119 |
10 | Health education to butchers | 0 | 123 |
11 | Anthelminthic treatment of stray dogs | 0 | 123 |
In addition, there were few municipal slaughterhouses, limited veterinary supervision and inspection of slaughterhouses, few facilities for the disposal of infected offal, and there was home or illegal livestock slaughtering, and lack of health education. It was observed that stray dogs have a close association with the slaughtering sites and increase the chances to get infected with CE. The finding of this study has showed that stray dogs (range 1–5) were present in the territories of all the butcher shops/slaughter houses that has an open access to infected offal of the slaughtered livestock. These stray dogs are not treated with any antiparasitic drug.
Cystic echinococcosis (CE) is a chronic larval cestode infection caused by
The findings showed that overall prevalence of CE was 2.77%. The prevalence was higher in buffaloes followed by cattle, sheep, and goat, respectively. In Pakistan the first incidence of CE in intermediate hosts was explored in 1968. The prevalence of
In current study, lung and liver was most affected organ as compared to others. The lung wise prevalence was 30.9, 22.8, and 58.8%, in cattle, buffaloes, and camels, respectively while in liver it was 21.42, 17.47, and 26.4% in cattle, buffaloes, and camels, respectively (
A report from Lahore showed that hydatidosis is prevalent in sheep (8.85%) and in goats (6.21%). This survey was conducted to determine the organ specificity of hydatidosis, organ wise distribution of hydatidosis showed that in goats 40.56% in liver, followed by 34.38% in lungs, 16.95% in lungs and liver together, and 0.49% in spleen. In sheep, highly infected organ was lungs whereas liver was most infected organ in goats (
Similarly, frequency of fertile cysts was higher as compared to sterile, calcified, and underdeveloped cysts, respectively. Hydatid cysts can be categorized as non-viable, viable, and fertile (
Zoonotic helminthes (
The dog population depends on the accessibility of resources (for example, shelter, food, and water) (
Stray dogs are one of the important reservoirs for the transmission of zoonotic helminthes that are of public health concern especially
To attain effective control of CE, it is essential to raise knowledge and awareness regarding hazardous practices and defensive measures against the disease within the community. Pakistan, being a developing country, is densely populated and socioeconomically poor. Overall poor sanitary system in Pakistan is very poor and majority of the inhabitants lives in crowded area. Rural inhabitants mainly survive on small-scale agriculture and farming. Laborers working in the fields often interact with animals and, due to illiteracy, have limited knowledge of health and hygiene and therefore are often infected by
In the early years of the twenty-first century, CE contributed a major global disease burden; it is one of the 12 commonest NZDs (
In countries with a high number of stray dogs, such as Pakistan, and where the public education level is low, the first task for CE control should be to raise public awareness and try to prevent infected offal from being fed to dogs. Field studies should be conducted on this subject, training seminars should be given, information should be given to children in primary schools, butchers should be trained, the community should be informed by imams in mosques, and informative TV and radio programs should be broadcast.
The data used and/or analyzed during the current study are available from the corresponding author on reasonable request.
The animal study was reviewed and approved by the Departmental Ethics Review Board (ERB) at the COMSATS University Islamabad (CUI), Pakistan, under ERB/18/72. This study was carried out in strict accordance with the recommendations of the guide for the care and use of laboratory animals.
AK and MA collected the data and wrote the paper following discussions with HA and SS. SS and JC also revised the paper and improved the technical quality of the manuscript. AK and JC contributed reagents and materials. All authors approved the final version of the paper.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors are thankful to AM and SI for their input which aided the completion of this study.
World Health Organization
Neglected Zoonotic Diseases
Cystic Echinococcosis
Disability Adjusted Life Years