Cystic Echinococcosis: An Impact Assessment of Prevention Programs in Endemic Developing Countries in Africa, Central Asia, and South America
Table 8
Appraisal summary of Article Meeting Inclusion Criteria [45].
Population:
Northwest China: Six communities in Hobukesar County, Xinjiang Uyghur Autonomous Region: (i) Narenhebuke (ii) Budengjian (iii) Changan Kul (iv) Chahete (v) Bayenoma (vi) Tiebukenwusan Ethnic groups: (i) Uyghur (ii) Han Kazakh (iii) Hui (iv) Mongol Lifestyle: (i) Pastoral and semi nomadic agricultural communities (livestock farming) Owned dogs: (i) Majority adult males (78.6%) (72.2% ≤4 years old) Stray dogs: (i) 21 male (ii) 17 female (≥1 years old)
Sample size:
(i) Stray dogs (): convenience sampling (non-randomized) (ii) Owned dogs (): randomized sampling of ≥19 dogs per community (iii) 117 dog owners: randomized sampling
Program outputs:
Chinese National Echinococcosis Control Programme implemented in Xinjiang (2010): (i) Praziquantel (PZQ) (0.2g/tablet): 1–2 tablets for dogs >15 kg, once a month. Supervised dosing to confirm dogs swallowed tablets and dosing date recorded (ii) Environmental prevention: dog feces collected, buried, or burned every 5 days after de-worming (iii) Dog population control: culling (iv) Humans: ultrasound (US) screening and medical treatment
Study design:
Quasi-experimental non-randomized before and after study
Program outcomes and/or impact:
Pre-program Cystic Echinococcosis (CE) prevalence: (i) 50/139 dogs (36% sampled in Hobukesar County, Narenhebuke) Post-program (April 2013) six communities: (i) Dog necropsy: 38 dogs caught by local dog catcher. Euthanised by qualified animal technician using intravenous ketamine (ii) Experienced researchers used a magnifying glass to inspect small intestine for CE worm burden. Worms washed in water and stored in 70% ethanol for PCR analysis Lot Quality Assurance Sampling (LQAS) evaluation: (i) CoproELISA: Dog fecel samples collected from grounds surrounding each household. Stored in 0.3% PBS Tween, with 10% formalin. Transported to Salford University, UK, at room temperature. If was not met, translators consulted other community areas where dogs could be sampled (ii) Analysis: genus-specific sandwich ELISA. Fecel samples extracted by homogenizing, shaking, and centrifuging. Supernatant collected. Conjugate antibody: hyperimmune rabbit IgG from adult Echinococcus granulosus worms. Capture antibody: Anti-E. granulosus whole worm somatic (iii) Positive controls: fecel supernatants of known positives (arecoline purge from Kyrgyzstan) and a sample spiked with E. granulosus whole worm extract (1 : 100 concentration) (iv) Negative controls from a low endemic area (Falkland Islands) PCR stray dog necropsy samples: (i) DNA extracted from Taenia spp. and Echinococcus spp. worms using a Qiagen® DNEasy Blood & Tissue kit (ii) DNA extracted from fecel samples (1 g) using a QIAamp® DNA Stool kit (iii) Positive controls: sequenced DNA from adult E. multilocularis/E. granulosus/Taenia hydatigena (iv) Negative controls: PCR grade water Questionnaire (): (i) Four communities sampled: Bayenoma, Budengjian, Changan Kul, and Tiebukenwusan (ii) Delivered in Mandarin Chinese, Mongolian, or Kazakh (iii) Age, sex, and last PZQ dosing recorded (iv) Dog owners asked to describe echinococcosis
Main findings:
Prevalence stray dogs: (i) Dog necropsy (n =38) 20 dogs (52.6%) Taenia spp.; 16 (42.1%) Echinococcus spp.; 13 (34.2%) infected with both parasites; 14 dogs (36.8%) neither (ii) PCR: 15/15 (E. granulosus G1) tested tapeworm positive samples (≥99% match) Prevalence owned dogs: (i) Range: 15% in Chahete to 70% in Budengjian; overall () (ii) CoproELISA positive ground fecel samples () (iii) CoproELISA positive cases (>35%) in 5/6 communities (iv) Only Chahete had CoproELISA prevalence <35% threshold. However, no dog owners reported dosing their dogs with PZQ over the past 2 years prior to sampling, and Chahete was a newly established farm. Thus, it could not be concluded if Chahete’s prevalence reduction was attributed to program outputs (v) PCR: 26 samples (50%) tested positive for E. granulosus. All negative for E. multilocularis DNA Dog owners self-reported Praziquantel dosing: (i) 43 (36.8%) reported never dosing; 16 (13.7%) could not recall the last dosing; 26 (22.2%) administered PZQ within 6 weeks prior to sampling; 23 (27.4%) between 6 weeks to 2 years. Great variation among six communities with dosing ranging from 5-93.3% (ii) 15/26 (57.7%) dog owners who reported dosing their dogs no earlier than 6 weeks prior were CoproELISA positive (iii) LQAS decision rule for PZQ dosing only met in Changan Kul (23 dogs dosed in year before sampling). This meant low PZQ administration (<90%) in 5/6 communities (Bayenoma, Budengjian, Chahete, Narenhebuke, and Tiebukenwusan) Questionnaire: (i) Could accurately describe CE: Bayenoma 5/13 (38.5%); Budengjian 14/19 (73.7%); 18 (94.7%) in Changan Kul; and 4 people (26.7%) in Tiebukenwusan (ii) Decision rule for knowledge of echinococcosis reached in 2/6 communities (Budengjian and Changan Kul). Meaning, knowledge did not fall below average (65% threshold) in these 2 communities. Notably, Changan Kul had PZQ dosing rates >90% target threshold in the previous year Barriers: (i) Unsustainable PZQ dosing in remote and semi-nomadic communities, due to logistics (funding, time, access, climate, skilled program workers, and dogs dislike tablet taste)
Limitations:
(i) Ethical issue: no sample size justification for stray dog euthanasia numbers (ii) Convenience sampling of stray dog population may not be representative of local population, e.g., if dogs caught from one specific area (iii) No consent obtained for 9 owned dog fecel samples collected (iv) Missing questionnaire data (v) Not guaranteed feces collected from the ground belonged to associated household owned dog (vi) Inability to accurately measure dog weights (vii) PCR test: ground collection of dog feces conducted in dry and warm environments that may have denatured or degraded DNA (viii) Pre-program CoproELISA prevalence data from secondary study. Thus, post-program sample groups not the same as pre-program. Variations in collection or analysis methods between studies can reduce reliability and internal validity (ix) Not clear why only 4/6 communities administered questionnaires (p.2), but in results, it states that 117 dog owners were sampled across 6 communities (p.4) (x) Lack of detail about questionnaire delivery, consent, participant information and question types (xi) Tapeworm samples lost in transport (xii) No detail of necropsy method used to “estimate” Echinococcus spp. worm burden (xiii) Recall bias: some dog owners did not regularly record PZQ administration (xiv) LQAS is limited to group vs. individual village-based analysis (confidence intervals are wider for individual villages, which reduced precision) (xv) No significance tests for CoproELISA prevalence reductions in 2/6 communities (Budengjian and Changan Kul), in relation to PZQ dosing (xvi) Study stated that PZQ dosing is only beneficial to owned dogs. Although less sustainable for stray dog populations, treatment may be beneficial in reducing environmental egg burdens. Stray dogs are likely to access intermediate hosts (e.g., livestock or wildlife carcasses) due to roaming behavior
