Review Article

Cystic Echinococcosis: An Impact Assessment of Prevention Programs in Endemic Developing Countries in Africa, Central Asia, and South America

Table 9

Appraisal summary of Article Meeting Inclusion Criteria [34].

Population:Alay Valley, Kyrgyzstan:
(i) 10 communities: Kyzyl-Eshme, Kabyk, Achyk-Suu, Jaylima, Kashka Suu, Kara Kavak, Sary Mogul, Taldu Suu, Archa Bulak, and Sary Tash
(ii) Small villages of 400 households
(iii) Approximate population: 3,000 people
Dog population:
(i) Average dog density: 1.56 dogs/100m2
(ii) April 2013
Sex: 157 (82.2%) males; 28 (14.7%) females
Age: <5 years old =131 (69.3%); 10-year-old not recorded; 6 (3.1%) dogs no age or sex recorded
(iii) April 2014
Sex: 156 (81.3%) males; 35 (18.2%) females
Age: <5 years old =156 (81.3%); 5 dogs no age or sex recorded

Sample size:Random selection of dogs and households
(i) 7, 610 dogs registered under control program
(a) Pre-program: 318 dogs sampled (May 2012)
(b) Post-program: 191 sampled (April 2013); 192 (April 2014)
(c) Total (2012-2014) = 701 dogs
(ii) 25% of village households registered (149 dog owners)
Lot Quality Assurance Sampling (LQAS):
(i) Assess Praziquantel (PZQ) dosing and CoproELISA prevalence
(ii) Random selection of 18-21 dogs sampled (target 19) from each community.

Program outputs:Echinococcosis Control Program 2012 (Kyrgyzstan, Ministry of Agriculture; financial support from the World Bank):
(i) Animal disease surveillance system
(ii) National public information campaign
(iii) Nationwide vaccination and testing program for eight diseases of livestock and/or dogs (foot and mouth disease, anthrax, rabies, brucellosis, sheep pox, peste des petits ruminants, echinococcosis, and tuberculosis)
Program Output Tested:
Praziquantel (PZQ) dog de-worming:
(i) 109 dogs administered PZQ four months prior to prevalence sampling (2013)
(ii) PZQ tablets provided to local community veterinarians at regional centers
(iii) Veterinarians visited households once every season to either dose dogs or leave tablets with owners to administer. Veterinarians provided dog passports for owners to monitor monthly PZQ administration
(iv) 2015-2016 PZQ de-worming ongoing: estimated 6,000 (2015) to 4,000 (2016) dogs treated
2015 Stray Dog Culling Campaign:
(i) Dog owners advised to tie up dogs and any dogs left roaming, euthanised
(ii) Conducted randomly each year

Study design:Quasi-experimental, randomized before/after study

Program outcomes and/or impact:Cystic Echinococcosis (CE) prevalence in dogs:
Pre-program CoproELISA testing (May 2012):
(i) Fecel samples collected from 4 communities: Kara Kavak = 35, Kashka Suu =42, Sary Mogul =155, Taldu Suu =86
(ii) Only occupants home sampled. Otherwise, six nearest households sampled and questioned about dog ownership of unavailable households. Process continued until a sample of 50 dogs obtained
(iii) CoproELISA test method: Decontaminated (80°C for ≥4 days) and fecel samples extracted by homogenizing, shaking, and centrifuging. Known positive and negative supernatant samples used as controls
(iv) Cutoff values for ROC curve panels determined from previous data of arecoline purge samples in Alay Valley, and necropsy samples from Hobukesar County, Xinjiang China
Post-program CoproELISA sampling (April 2013 and April 2014):
(i) Lot Quality Assurance Sampling (LQAS): fecel samples collected from around dog owner’s home, stored in 0.3% PBS Tween, with 10% formalin. Shipped at room temperature to the University of Salford, UK
Questionnaires:
(i) In 2014, dog owners () asked about dogs’ age, sex, and PZQ administration
(ii) Open-ended questions delivered verbally in Kyrgyz, by native speaker (Bermet Mytynova)
(iii) Answers to “CE causes” classified as “correct,” “incorrect,” or “partially correct.” Correct answers based upon identifying the definitive host (e.g., dogs, foxes, or wolves) or direct cause (e.g., infective eggs in dog feces)

Main findings:Pre-program prevalence: CoproELISA (May 2012): 20.1% ():
Post-program: CoproELISA (2013; 2014):
(i) Prevalence decreased from 5 (2013) to 3 (2014) communities that did not meet the LQAS decision number or program target
PZQ administration (dog owners self-reported):
(i) In 2013, 141 (73.8%) reported dosing in last 7 months before sampling; 1 (0.5%) reported last 11 months; 39 (20.42%) reported never dosing their dogs; and 10 (5.2%) could not recall
(ii) In 2014, 152 (79.2%) reported dosing in the last seven months; 4 (2.1%) dosed between 7 and 8 months; 23 (12.0%) never administered PZQ, and 13 (6.8%) could not recall
(iii) Improvement in PZQ administration in 2014 across communities: 128 (66.7%) coverage. Only two communities (Kashka Suu and Kyzyl-Eshme) failed to meet the LQAS decision number (meaning they had below average PZQ administration rates)
(iv) In 2013, only 4/10 communities reached the 75% PZQ dosing target compared to 8/10 in 2014 (21 months post- program)
Questionnaires:
(i) 149 dog owners participated (some declined to answer and some owned multiple dogs)
(ii) 126 respondents (84.6%) had heard of echinococcosis
(iii) 93 (78.3%) correctly identified causes of echinococcosis
(iv) 13 (10.3%) partially correct responses
(v) From those who had heard of echinococcosis, 20 could not identify a cause
(vi) 23 (15.6%) had never heard of echinococcosis nor identified a cause
(vii) Total: 43 (28.9%) could not identify the cause of echinococcosis, but the majority (78.3%) could
Barriers:
(i) Remoteness (communities and households scattered)
(ii) Community semi-nomadic customs and lack of resources
(iii) Lack of funding for diagnostic tests
(iv) Free roaming dogs; and changing population numbers
(v) Financial costs and human resources present challenges to sustainability of PZQ treatments every 6 weeks. It requires consistent PZQ administration to reduce environmental eggs burdens and break transmission cycles. Thus, longer-term studies were advocated

Limitations:(i) Recall bias: owners could not recall PZQ administration
(ii) Sample size calculation unclear. Reported as an “estimated” value from unpublished data from the Kyrgyz Ministry of Agriculture, Land Reclamation, and the Kyrgyz State Inspectorate for Veterinary and Phytosanitary Safety
(iii) Missing signalment details for dogs (age and sex)
(iv) Results on local knowledge not comparable, as no pre-program measures
(v) No detail about dog culling or if humanely euthanised
(vi) Minimal analysis or further testing of questionnaire results
Confounding variables:
(i) 4/10 communities sampled before program (2012) versus 6 post-program. Communities may have different dogs, sheep, and human population demographics
(ii) Multiple sub-programs comprised the broader national program, and public health notices appeared on Kyrgyz television during the program. These program outputs were not controlled or tested
(iii) No sample size calculation for stray dog population
(iv) Due to logistics (time) all dogs not sampled in one community (Kashka Suu)
(v) Fecel samples collected around dog owners’ homes may have belonged to stray dogs or wildlife vs. the residing dog
(vi) Non-standardized PZQ administration method
(a) Veterinarians or dog owners administered PZQ
(b) In Sary Mogul, 0/19 dogs administered PZQ four months before sampling (2013), compared to 16/19 dogs in Jaylima