Review Article

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

Table 12

Appraisal summary of Article Meeting Inclusion Criteria [46].

Population:(i) Middle Atlas, Morocco, North Africa (locality of Had Oued Ifrane)
(ii) Total area: 27, 550 km2; 15% of Morocco’s mountain area
(iii) Climate: mountainous continental; Mediterranean: cold, rainy, and snowy in winter; hot and dry in summer
(iv) Agropastoral zone: livestock (sheep breeding: Timahdit breed or cattle of similar herd size)
Sample population:
(i) Owned dogs (2-3 dogs per household) or stray (>1 years old) from three douars (villages), 20-30 km from each other
(ii) Located near a weekly market (souk) and slaughterhouse

Sample size:(i) 225 owned and stray dogs

Program outputs:Dog Praziquantel (5 mg/kg) de-worming (December 2016 to August 2017):
3 groups:
(i) Group A Douar Assaka: 2-month treatment interval and sampling three times (Dec, Feb, April)
(ii) Group B Douar Sanoual: 3-month treatment interval and sampling (Dec, March, June)
(iii) Group C Douar Sidi Bel Khir: 4-month treatment interval and sampling (Dec, April, August)
(iv) All groups composed of owned (60–75%) and stray dogs (25–40%)
(v) Stray dogs identified from images and owned dogs by owners
(vi) Dogs who missed any sample sessions were excluded

Study design:Non-randomized controlled trial

Program outcomes and/or impact:Prevalence of Cystic Echinococcosis (CE) (December 2016-August 2017):
Owned Dogs:
(i) Arecoline hydrobromide (4 mg/kg body weight or 2 mg/kg for a second dose) fed in meat balls to induce defecation and egg expulsion
Stray dogs:
(i) Levomepromazine (25 mg orally) for sedation before arecoline administration
Fecel sample tests:
(ii) Fecel flotation
(iii) Microscopic examination of worms and eggs
  (a) Positive samples confirmed with CoproPCR
  (b) After sample collection, feces disinfected with alcohol for at least 5 minutes and burned

Main findings:Pre-program prevalence:
(i) Owned Dogs: range 23.5% to 38.8%
(ii) Stray Dogs: range 51.3% to 68.5%
Post-program (December 2016 to August 2017): prevalence decreased in stray and owned dogs across all groups, but more significantly in owned dogs:
(i) Group A: owned dogs (0.24-0); stray dogs (0.5-0.05)
(ii) Group B: owned dogs (0.4-0); stray dogs (0.63-0.18)
(iii) Group C: owned dogs (0.35-0.05); stray dogs (0.76-0.5)
(iv) Stray dogs were 14 times as likely to be CE infected compared to owned dogs (odds ratio = 14; 95% CI: 6-30; ). Higher prevalence in stray dogs attributed to free access to condemned organs from slaughterhouses and weekly markets
(v) Monthly risk was lowest in group A (2 monthly intervals) compared to B (3 monthly) and C (4 monthly intervals). Infection risk highest in group C
(vi) 2 monthly PZQ intervals for owned and stray dogs can effectively control shedding of infective eggs
(vii) Season significantly () associated with prevalence;
  (a) Reduced risk of infection during second sampling period, as dry and warm summer conditions decrease environmental survival of CE eggs
  (b) During colder, winter months, higher risk of infection, due to extended lifecycle of eggs. Increase also attributed to increased livestock slaughter during winter
  (c) Interactions between time and dog type (stray or owned), and time and site not significant (, )
Barriers:
(i) Primary transmission cycle: stray dogs in urban areas; roaming or shepherding dogs in rural areas
(ii) Dogs are kept as house and livestock guards, often in close contact with owners; especially women and children (high risk demographic)
(iii) Home slaughtered livestock primary source of infection for owned dogs
(iv) Condemned offal from slaughterhouses or weekly markets (souk) source of transmission for stray or roaming dogs

Limitations:(i) No sample size calculation
(ii) Study design and methods unclear: a self-identified longitudinal study, which used odds ratio to identify risk factors, such as being a stray vs. owned dog. However, unlike case control studies that focus on pre-existing disease cases, odds ratio seemed to be applied like a relative risk ratio within a prospective cohort study, to calculate disease incidence. This made reported measurements of incidence vs. prevalence confusing
(iii) Ethical issue: arecoline can cause adverse reactions in young or old dogs and is generally prohibited in pregnant dogs. No signalment details for dog ages or sex
(iv) Difficult to identify exact prevalence values
(v) Pre-program prevalence ranges: unclear if this was an average across all three sites
(vi) Could not source cited articles for fecel floatation or microscopic tests. However, use of fecel flotation to detect E. granulosus is not highly sensitive, as Taenia and Echinococcus eggs are morphologically indistinguishable using fecel float ([47], p.123)
(vii) PCR methodology described in reference to several secondary studies. Difficult to identify which parts of each methodology were utilized, especially in reference to PBS and DNA extraction methods from Mathis et al. [48] and Abbassi et al. [49]
Confounding variables:
(i) Different exposure times for groups A, B, and C, due to different administration interval periods (e.g., variable time spans from 4-8 months at three sites). Instead, having three different interval groups per site, sampled at the same time, would have controlled for seasonal variation
(ii) Research bias: researchers or statisticians not blinded to de-worming intervals for each group
(iii) Not clear if dog owners or skilled worker administered PZQ
(iv) No specification about whether skilled or unskilled personnel collected fecel samples, analyzed them for CoproPCR, fecel flotation, or microscopy
(v) Does not distinguish between stray versus owned dogs