ABSTRACT
Ivermectin remains the only safe drug for the control and
treatment of onchocercisis in endemic areas. Despite some reports on its
sub-optimal response in some parts of Ghana, long term treatment has shown that
it can eliminate the infection and interrupt transmission in Africa. Taking
into account the feasibility of elimination of onchocerciasis infection and
transmission interruption with ivermectin mass treatment alone, Joint Action
Forum (JAF), and the governing body of African Programme for Onchocerciasis
Control in 2011, has reaffirmed its endorsement for the Programme to pursue the
elimination of onchocerciasis in Africa. Aowin district of the Western Region
of Ghana is meso-endemic for onchocerciasis infection and had received
ivermectin mass drug treatment for 10 years. This study was undertaken to
assess the impact of 10 years of mass drug administration with ivermectin on
the level of endemicity and intensity of O. volvulus infection in Aowin
district following the claim made by the District Health Directorate that
onchocerciasis transmission and infection had been eliminated in the district.
A cross sectional survey was conducted in 20 endemic communities situated along
rivers in the district. In all, 1,698 volunteers took part in the study. They were
examined by palpation for onchocercal nodules or onchodermatitis. Of the 1,698
volunteers examined, 300 who were positive for palpable nodules or
onchodermatitis were skin-snipped for microfilarial load assessment. Community
microfilarial load (CMFL) for each of the studied community was also
determined. Onchocercal nodules and microfilarial prevalence were used to
measure the level of endemicity. The intensity of infection was measured using
CMFL, a reference index used by the Onchocerciasis Control Programme. The
results indicated that, 298 (17.6%) out of the 1,698 examined had palpable
nodules. A significant difference was observed (p=0.0001) in the nodule
prevalence between males and females. Out of the 300 skin snipped, 173 (57.7%)
were microfilarial-positive. The microfilarial prevalence and community
microfilarial load in the study communities ranged from 8.3-88.9% and
1.0-5.2mf/mg respectively. The overall nodule and microfilarial prevalence
recorded suggest strong evidence of on-going transmission of onchocerciasis
despite 10 years of annual mass treatment. Halting ivermectin treatment in the
district is not recommended as it might risk recrudescence of transmission.
CHAPTER ONE
INTRODUCTION
1.1: Background
Human onchocerciasis is a
debilitating disease affecting about 37 million people in the world (Basáñez et
al., 2006). About 500,000 people suffer from visual impairment and 270,000 have
gone blind (WHO, 1995). It is also an important cause of severe dermatitis and
musculoskeletal pains (WHO, 1995).
Onchocerca volvulus is the
causative agent responsible for onchocerciasis (river blindness) and the
various dermatological manifestations (Hoerauf et al., 2011). The infections
are primarily restricted to Africa with about 96% cases mostly in the Western
sub-Saharan region (Basáñez et al., 2006; WHO, 2011). O. volvulus is
transmitted by Simulium damnosum, particularly S. damnosum sensu lato (s.l.) is
the major species in Africa (Crosskey, 1990; Crosskey and Howard, 2004). Humans
are the only known natural reservoirs (Udall, 2007). The third stage filarial
larvae, L3, which is the infective larval stage are introduced by the black fly
into the human host when it feeds on a blood meal, and the life cycle is
completed when adult worms, residing in the nodules produce microfilariae (mf)
that move throughout the dermis of the host are taken up by the black fly
(Taylor et al., 2010). Simulium flies reproduce in rapidly flowing streams and
rivers and the prevalence of infection and disease in a community depends upon
how the community is close to the riverine breeding site of the black flies
with communities adjacent to rivers serving as the highest burden of infection
and disease (Taylor et al., 2010).
Onchocerciasis prevalence is
highest among the age population between 20-30 years (Hailu et al., 2002;
Little et al., 2004a). Men compared to female generally have higher disease prevalence
possibly because of their high exposure to the bites of the black flies during farming and fishing activities.
Prevalence is lowest in children under 10 years as children have less exposure
to the bite of the Simulium flies whose biting activities are greatest in the
morning (Hailu et al., 2002; Little et al., 2004a).
Adult filarial worms present in the
nodules beneath the skin of the infected host can survive up to 14 years
(Plaisier et al., 1990; Winnen et al., 2002). During this period, millions of
microfilariae are produced and released into the skin of the infected
individuals. The presence of these microfilariae in the skin of the infected
individuals is responsible for the main clinical complications due to
inflammatory reactions to the macrofilariae in the dermis and in the eyes (WHO,
1995).
The disease is a chronic,
multisystemic one that leads to severe itching, blindness, skin lesions,
epilepsy as a result of heavy infection, and reduced life expectancy among
sighted individuals with high microfilarial (WHO, 1995). Some other
consequences of infection with O. volvulus includes disability leading to
significant morbidity, social ostracism, reduced work and abandonment of
fertile river valleys causing reduction in agricultural output among the
disease affected populations (Prost, 1986; Vlassoff et al., 2000; Boussinesq et
al., 2002; Pion et al., 2002; Little et al., 2004b;). Annually, Onchocerciasis
causes approximately 1.5 million healthy life-years lost as a result of impairment
and mortality (Evans, 1995; Oladepo et al., 1997; Remme, 2004; Remme et al.,
2006). Over half of this result from dermal diseases that have negative impact
on income generating capacity, health and socio-economics of those that are
affected and their dependents. (Evans, 1995; Oladepo et al., 1997; Remme, 2004;
Remme et al., 2006).
Onchocerciasis is a serious public
health issue because of the detrimental and devastating effects of the disease
to both human and economic development (WHO, 1997). Over the past decades,
governments, policy and decision makers in the world community have continuously made efforts to
control and eliminate this infectious disease. In the year 1975, the World
Health Organization (WHO) launched the Onchocerciasis Control Programme (OCP)
of West Africa. The aim of the programme was to eradicate onchocerciasis as a
disease of public-health importance from the savana areas of 11 West African
countries including Ghana (WHO, 1997). The core activities of the programme
included aerial larvicide spraying of rapidly flowing streams and rivers to
control the multiplication of the Simulium flies and treating infected
individuals with Diethylcarbamazine (DEC) that can kill microfilariae (WHO,
1997). However, DEC treatment of the infected individuals led to severe adverse
effects and therefore was not considered safe for mass drug administration
(Hawking, 1979).
Onchocerciasis control under the
umbrella of Onchocerciasis Control Programme in West Africa (OCP) in the 11
West African countries achieved some significant successes. By the end of the
programme in 2002, it covered 1,200,000 square kilometres, protected 30 million
people that were at risk of the infection and prevented 600,000 people from
blindness making 25 million hectares of land safe for relocation (Hopkins,
2005). It has reduced the problem of millions of the world’s poorest people
(Harlem, 2002; Hopkins, 2005).
The efforts of various governments
and policy makers to control and eliminate onchocerciasis as a public health
burden currently rely on mass drug administration of ivermectin under the
following programme; African Programme for Onchocerciasis Control (APOC), the
former Onchocerciasis Control Programme (OCP) and Onchocerciasis Elimination
Program for the Americas (OEPA) (Sturchio, 2001). The drug ivermectin or
Mectizan® was donated by Merck & Co, in 1987.
Ivermectin was registered in 1987
for human use to treat onchocerciasis and later lymphatic filariasis (Thylefors
and Lawrence, 2008; Ottesen et al., 2008). To date (2016), it continues to be the only safe drug for mass
treatment of onchocercisis (Cupp et al., 2011). National control programmes in
the former OCP and the WHO African Programme for Onchocerciasis Control (APOC)
provide ivermectin treatment periodically using community-based volunteers
(Amazigo et al., 2002) to reduce and possibly eliminate the infection where
feasible. The recommended dose is 150 μg/kg body weight per annum or three
times in a year and has effect on the microfilariae in the skin and the eyes
(Enk, 2006; Canga et al., 2008). The drug is able to reduce levels of
microfilariae in the skin and the eye and maintain it for about 9-12 months. (Greene
et al., 1985; Lariviere et al., 1985; Awadzi et al., 1985; Diallo et al., 1986;
White et al., 1987). Reduction of microfilarial density in the skin can
significantly reduce parasite transmission but transmission cannot be
interrupted after the initial few years of administration of ivermectin (Remme,
2004; Ndyomugyenyi et al., 2004). The drug also has advantageous effect on symptoms
and clinical presentations of the disease. The drug relieves the intense
itching from the infection and progression towards blindness except in very
advanced cases. However, ivermectin does not kill adult worms directly, but
hinders the release of microfilariae from the adult female worm just after the
initial dose (Cupp et al., 2004; Duke, 2005). This effect can last up to a
period of one year after treatment leading to degeneration of intra-uterine
microfilariae and multiple treatments with the drug may increase mortality of
adult worms (Cupp et al., 2004; Duke, 2005). Multiple doses of the drug have
been shown to also have effect on the development of the embryo of the worms
and also cause progressive restitution of the cellular anti-filarial immune
response (Schulz-Key et al., 1992).
Due to the safety profile of the
drug, it has been extensively used in mass drug administration since the
mid-1990 and it is the WHO recommended approach for the control of
onchocerciasis (WHO, 2006). As the drug has limited effect on the adult
onchocercal worms, it means that persistent treatment is required in order to
repress the manifestations of the infection over time (WHO, 2006).
While early computer models estimated 25 years treatment to interrupt
transmission, recent evidence has proposed that 5 to 15 years of ivermectin
mass treatment might interrupt transmission depending on the treatment method
and the pre-control endemicity level (Winnen et al., 2002; Cupp and Cupp,
2007).
Within the past 29 years of Mass
Drug Administration (MDA) using ivermectin, a billion treatments have so far
been administered and currently, Mectizan Donation Program (MDP) approves an
average of 140 million treatments for onchocerciasis and lymphatic filariasis
per year (MDP, 2016). Treatment of onchocerciasis using ivermectin mass drug
administration has brought significant reduction in the transmission of the
disease in the endemic areas (WHO, 2012). By mid-2012, bi-annual mass
treatments with ivermectin had eliminated or interrupted transmission of the
disease in 10 onchocerciasis foci in the Americas (WHO, 2012).
Many communities in Africa and
Latin America have also benefitted from the infrastructure and distribution
systems that were developed for the onchocerciasis control and elimination
programmes. The successful nature of these ivermectin-based programmes
worldwide created a model for health care. Its successful policies and plans
have proven the possibility of putting forth activities and efforts to target
other diseases that are chronic in poor and remote localities of the world to
effect improvements in productivity, morbidity and long-term mortality (Hotez et
al., 2007).
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