Important entomological events in the history of onchocerciasis (‘river blindness’)

Abstract

This article reviews the major events that entomology has played, and still plays, in the history of onchocerciasis (‘river blindness’) from life-cycle discovery to the current global goal of elimination of parasite transmission in all endemic areas. The identified events include the various attempts to implement successful vector control, the important introduction of the microfilaricide ivermectin and the new improvements in laboratory-based techniques to identify infected blackflies and refine onchocerciasis epidemiology and programme monitoring. These scientific events are paralleled with the development of a series of increasingly ambitious public health targets, first to reduce blindness due to this infection, then to reduce the prevalence of all the clinical symptoms (ocular and dermatological disease) and, finally, in more recent times, to interrupt actual transmission of the parasite. Five major areas of onchocerciasis-related entomology (i.e. the effects of fly biting; vector competence and migration; epidemiology; vector control; and management of elimination programmes) illustrate the importance of entomology to achieving success in eliminating the transmission of Onchocerca volvulus; success that has already been achieved in four countries in Latin America and now in one country in Africa (Niger, 2024), the continent where the vast majority of remaining endemicity is found.

Introduction

Blackflies (Simuliids) are globally distributed members of the family Simuliidae of insects (Figure 1). A few species of blackflies are the vectors of the filarial nematode Onchocerca volvulus in parts of the tropics, where the infection can cause severe dermal and ocular pathology in humans.¹ The breeding of these flies in flowing waters has been given the vernacular name ‘river blindness’ because of the resulting human disease¹ (Figures 2–4), although in terms of prevalence, the dermal disease, with the accompanying intolerable itching and marked physical changes, is by far the more prevalent of clinical manifestations seen in this condition. Blackflies can, on occasion, also acquire other species of onchocercal parasites by biting non-human animals, such as cattle infected with Onchocerca ochengi.² The similarity of these two filarial parasites often leads to diagnostic confusion when assessing for the presence of O. volvulus in caught blackflies. Importantly, molecular tests are now identifying new, more specific markers that can more easily distinguish between these two filarial parasites.³

Figure 1.

The head of the blackfly vector of onchocerciasis, Simulium damnosum s.l., from the Abu Hamed focus in northern Sudan (photograph credit: CD Mackenzie).

Figure 2.

Simulium larvae on vegetation taken from fast-flowing water (photograph credit: CD Mackenzie).

Figure 4.

A Simulium fly emerges from its cocoon that is attached to vegetation taken from the River Nile in the Abu Hamed onchocerciasis focus, northern Sudan. (Note that, in the natural situation, a newborn fly emerges into an air bubble on the vegetation, which then floats to the surface and releases the insect.) (Photograph credit: CD Mackenzie).

As outlined in this review, and in the publications in the associated Supplement, many of the programmatic actions, the knowledge of affected human populations regarding the disease and the early historical events in human onchocerciasis have been, and remain, directly related to the blackfly vector in one way or another. A clear field example of the strong link between the perceptions of human populations regarding the vector and the disease itself occurred in the now onchocerciasis-free Abu Hamed focus in northern Sudan.⁴ Here, the disease, the fly and, ironically, the local governmental health worker responsible for treatment, were all known by the same local name: ‘conteb’.

The objective of this brief review is to highlight, from a historical perspective, the important roles that entomology has played, and still plays, in the management of this disease and application of the field programmes aimed at the elimination of transmission of this devastating parasite. This discussion provides a background for the specific discussions that follow in this present Entomology Supplement, a collection of articles covering information gained from major initiatives such as the West African Onchocerciasis Control Programme (OCP), and other important studies and events over the past 50 y.

History

The British naval surgeon O’Neil was the first to identify the parasitic origin of dermal onchocerciasis (Figure 5); in 1874, he identified parasites in the skin condition known as ‘craw craw’ whilst attending to individuals rescued from the ongoing slave trade on the west coast of Africa. In 1890, the German parasitologist Leuckart identified the worms found in ‘craw craw’ samples as filarial parasites. Blacklock first defined the role of blackflies as the vector of this infection in 1926, working in Sierra Leone, demonstrating that Simulium damnosum sensu lato was the intermediate host of O. volvulus.⁵ However, the Guatemalan physician, Robles, had already suggested, 11 y earlier, that simuliids might be the vectors, as he associated the presence of onchocercal eye disease with living near simuliid breeding sites in fast-flowing rivers.⁶ In 1928, colonial medical staff in Wau, Sudan (now South Sudan), also attributed blindness to working near the local Jur River and coined the term ‘Jur River Blindness’, a name that is still recognised today in South Sudan. The Belgian ophthalmologist, Hissette, working in the Belgian Congo in the early 1930s, also proposed that ocular blindness could be due to onchocerciasis.^6,7,8

Figure 5.

Important events in the medical and political history of onchocerciasis, highlighting events related to entomology and the definition of the blackfly vector. OCP: Onchocerciasis Control Programme.

Mexican health authorities, in the 1930s (1932–1940), carried out the first concerted approach to reduce and prevent the development of the disease ‘river blindness’ by controlling the vector blackflies in their riverine breeding sites. These initial efforts involved vegetation clearance and the use of ‘Paris Green’ as an insecticide (larvicide), but neither approach was successful.⁹ The disinfectant, creoline, was partially effective, but was abandoned due to environmental damage. Further attempts at environmental destruction of larval habitats in Congo (1942–1944) were also only partly effective, and the first unqualified successes in eliminating this vector were achieved in Kenya using both vegetation clearance and dichloro-diphenyl-trichloroethane (DDT) larvicide, resulting in the disappearance of the Simulium neavei vector (1943–1954). This success stimulated further vector control programmes in the 1950s, in Congo, Nigeria, Uganda, Guatemala, Ghana, Mexico and Sierra Leone. These continued into the 1960s in Benin, Guinea-Bissau, Burkina Faso, Mali, Cameroon and Côte d’Ivoire.¹⁰ These efforts led to a significant boost in scientific interest in Simulium and its relationship to onchocerciasis, and in West Africa led to the initiation of an extensive vector control programme in the early 1970s, known as the West African Onchocerciasis Control Programme (OCP).¹¹ This programme eventually included 11 countries, starting with Benin, Burkina Faso, Côte d’Ivoire, Ghana, Mali, Niger and Togo in 1974, then later adding Guinea, Guinea-Bissau, Senegal and Sierra Leone. The plan for the OCP was to target Simulium breeding sites in the river systems using aerial spraying, with the hope that this would interrupt the parasite’s transmission long enough to control the disease as a public health problem, and specifically reduce the number of cases of blindness. A vector control programme was preferred over a chemotherapy approach as the antifilarial drugs at that time caused unacceptable side reactions.¹¹ The World Bank took the lead on this critical public health effort, recognising the suffering and the enormous economic impact the disease was causing in these fertile areas. Many of the most farmed riverine lands were being abandoned by local farmers due to the consequences of blackfly bites. The World Bank was supported by other major international agencies, including the WHO, the Food and Agriculture Organization (FAO) and the United Nations Development Programme (UNDP). In the 1970s, French, German and British entomologists worked with African experts, all of whom became involved in the management and scientific evaluation of the OCP and its activities. The OCP was successful in bringing down the number of cases of blindness with a reduction in the prevalence of infected blackflies.¹² However, in 1987, it was the addition of the donation by Merck & Co. of the microfilaricidal agent ivermectin, a drug well known to the veterinary community, that finally enabled the major moves to have an impact on this infection, first with its control, then the actual elimination of the transmission of O. volvulus.¹³

Subsequently, various studies in research centres across Africa have addressed different aspects of the interaction between humans and Simulium. Thompson, in 1977, working in Cameroon, focused on the role of human factors, such as sweat, in attracting appetitive (blood-hungry) blackflies.¹⁴ In more recent times, there have been essential studies on the interaction between this vector and endemic communities, including details of their attraction to humans and the knowledge and opinions of those living in blackfly-infested areas.^15,16 This work laid the groundwork for the development of non-human blackfly-catching systems needed to acquire insects for programme evaluation.¹⁷ Cytotaxonomy has also been a valuable tool in distinguishing between different species of blackflies and improving the understanding of the distribution of the transmitting species of flies.¹⁸ Other angles taken by researchers have focused on improving the ability to detect the parasite within the insect with new nucleic acid amplification tests (e.g. PCR—(E47))³ and gene-based mapping of fly movements.¹⁹ Field activities have been enhanced by a refocus on breeding site-driven epidemiology and a clearer definition of the transmission status of geographic zones. ‘Bio-epidemiological factors entirely define Transmission Zones’ (TZs).²⁰ Still, as these can be very large, they are usually broken down into implementation units called operational TZs (OTZs) based on a combination of bio-epidemiology and operational convenience, hence the acronym ‘OTZ’ to distinguish them from ‘transmission zones’.²⁰

Simulium biting can have a direct effect on the individuals being bitten and fed upon, both through direct (focal damage to the skin) and indirect (damage from excessive scratching of these pruritic bite sites); these effects make locations with high biting rates unpopular places to live. The bites of Simulium sp. cause damage when they puncture the epidermis and upper dermis with the sawing cutting action of their jagged mandibles, creating pools of blood that coincidently include dermal parasites that they will transmit. As this damage involves the pigmented cell layer at the base of the epidermis, it directly contributes to the pigment changes typically seen in onchocerciasis. In addition, individuals, especially those who are being repeatedly bitten, can develop an allergic response to the blackfly saliva. The itching and accompanying scratching with the individual’s fingernails can severely damage the skin and, along with the coexisting dermal damage caused by the presence and death of Onchocerca microfilariae, significantly contribute to the overall clinical changes seen in onchodermatitis.¹

In the early 1970s, the annoyance of blackfly biting was so severe to residents in Uganda, including inmates of a field farm prison, that it motivated the authorities to implement a DDT-based larvicidal programme purely to reduce the number of irritating flies.²¹ This was done purely to address vector issues and was not related to onchocerciasis-control needs. However, the experiences learnt with vector reduction in Uganda provided essential evidence that was used to support the planning for the major west African vector control initiative, the OCP.

All these advances in our knowledge of blackflies in onchocerciasis, together with better understanding of the parasite’s biology, and the use of ivermectin, have moved us closer to the global goal: reducing disease levels; and now, to the more exacting goal of eliminating transmission. Indeed, four Latin American countries (Colombia,²² Ecuador,²³ Guatemala²⁴ and Mexico²⁵) have already achieved the elimination goal and, recently, one African country (Niger) joined this successful group.^26,27 Correspondingly, the specific country and global targets for onchocerciasis have also changed since the start of the OCP. In 1995, the African Programme for Onchocerciasis Control (APOC) expanded control programme efforts from West Africa to the entire continent. In 2002, experts believed that elimination similar to that achieved in the Americas was not feasible without major technological change.²⁸ However, the achievement of elimination of transmission in a number of intra-country endemic foci in Africa, such as Sudan,²⁹ Uganda,³⁰ Senegal³¹ and Mali,³¹ encouraged the WHO to accept that elimination was indeed feasible in Africa, or at least could be approached using the current tools and programmatic strategies.^32,33 Worthy of mention in this context is the entomological achievement of the elimination of the vector on the onchocerciasis-endemic island, Bioko, in Equatorial Guinea.³⁴ These encouraging successes convinced the WHO in 2013 to recommend to the World Health Assembly that the target for onchocerciasis programme success should be changed from control (i.e. elimination of a public health problem) to elimination of parasite transmission (WHA66.12).³⁵ This more exacting requirement for defining elimination again emphasises the importance of entomology in onchocerciasis programmes because the essential definition of elimination constitutes a lack of parasites in the heads of the transmitting flies.

The major areas of entomology in onchocerciasis

The initiation of the OCP in West Africa in the mid-1970s acted as a major impetus for gaining a better understanding of the blackfly vectors of onchocerciasis. Over the following three decades, much fundamental information about the role of Simulium in onchocerciasis, and its control, emerged from important research activities that included fly biology, habits and migration, as well as the genetic variations in the Simulium flies acting as vectors. Currently, the roles entomology plays in the control and elimination of onchocerciasis transmission can be divided into five major areas: the effects of fly biting; vector competence and migration; epidemiology; vector control; and management of elimination programmes.

The effect of the vector on its hosts

As mentioned above, people living in areas where anthropophilic (human-biting) Simulium flies are plentiful are usually very aware of their presence, as the blood-seeking female flies cause irritation and annoyance. This recognition by local inhabitants is helpful when onchocerciasis teams mapping breeding sites are looking for active sites. Careful questioning of residents about the presence of blackflies helps programme teams to identify nearby breeding sites, and when there are peak seasonal biting periods; this provides essential information for planning programmatic activities such as monitoring and evaluation.^36,37 When interviewing local residents it is important to be sure that the information gained is related to blackflies: the use of photographs of flies at different magnifications is most useful, as well as visiting any potential breeding sites mentioned with the residents themselves.

Vector competence and migration

Vector competence, the ability to transmit the parasite to another host, is one area of Simulium biology that is not often mentioned in programmatic terms, but is an essential factor in the history of onchocerciasis. The establishment of new endemic areas depends on the coexistence of the parasite and a competent vector capable of sustaining its life cycle. The distribution of the infection outside Africa provides clear examples of vector competence, such as in Ecuador.³³ In the mid-1840s, a slave ship was wrecked on the Esmeraldas coast in northern Ecuador, and the Africans on board, who were likely to have come from onchocerciasis-endemic areas in Africa, were stranded in this forest riverine area where the highly competent vector Simulium exiguum was present. More than 100 y later, of the seven river valleys in this area—other than the initially inhabited Cayapas River system—only two were found to be endemic for onchocerciasis; these were the only two where S. exiguum was present. The blackfly breeding in the other five river valley systems was the much less competent blackfly, Simulium quadrivittatum. Similarly, onchocerciasis distribution in Yemen was also likely to have arrived with migrants from endemic Africa via the Red Sea slave trade that had existed since the first century CE. Here, the infection is also found only in valleys (‘wadis’) where the competent vector, Simulium rasyani, is present, and not in other valleys where only non-competent flies are present.³⁸

Important understanding of the factors involved in the migration of the Simulium involved in onchocerciasis was gained from studies in the OCP countries^39–41 and in Sudan (now South Sudan).⁴² These findings included that blackflies, in some circumstances, can be found at least 550 km from their original breeding sites.⁴³ A critical new approach to enhancing maps of blackfly movement and understanding their migration is genetic tracing.¹⁹

Epidemiology

An essential difference of the onchocerciasis programme from other neglected tropical disease (NTD) mass treatment systems is that the programmatic mapping is now based on biologically defined zones rather than the more standard administrative zones (e.g. districts), as seen with the lymphatic filariasis’s ‘implementation units’ (i.e. official, governmentally defined, districts).²⁰ Thus, maps of Simulium breeding sites are developed within operationally feasible areas with a biological TZ. These operational areas are known as operational transmission zones and are now key to the activities of an elimination programme (e.g. mass drug administration [MDA], and Monitoring and Evaluation [M&E]). In the past, programmes have used human indicators, such as nodule presence and dermal microfilarial loads, to define zones of endemicity,^44–46 but with the new target of transmission interruption, and the optimal indicator to show this being the presence of parasites in the head of the vector, entomology has become a vital indicator.

Knowing where active blackfly breeding sites are located is a key step in identifying areas where onchocerciasis transmission is occurring. This enables the development of a map of OTZs, that is, areas central to many steps in the elimination programme management. For example, indicating where mass drug treatment is needed, and where the optimal sites for monitoring and evaluation activities are located. Much of the methodology for establishing the location and boundaries of OTZs is based on reliable knowledge of breeding sites, the presence of the vector blackfly, peak breeding seasons, migration and other characteristics of the vector blackfly’s habitat and behaviour. Knowledge of breeding sites is central to defining the outer limits of onchocerciasis-endemic areas, now encapsulated in a protocol named Onchocerciasis Elimination Mapping (OEM).^36,37,47

The significant global decision that enhanced the importance of entomology in elimination programmes was the change in the global onchocerciasis intervention goal from disease control (which only required treatment of mesoendemic and hyperendemic areas and was mainly based on evidence of infection in the host humans) to the more rigorous goal of elimination of parasite transmission (which requires knowledge of the parasitological status of the blackfly in all endemic zones).^33,48 This change resulted in the need to carry out MDA in any newly defined hypoendemic areas. OEM was developed to identify previously untreated endemic areas. The OEM protocol requires identification of the vector relative to non-vector blackflies, knowledge of breeding sites and identification of the biological and environmental characteristics of potentially endemic areas in relation to the vector.⁴⁷

One of the most significant advances in understanding the vector stimulated by the OCP initiative was the defining of the different forms of Simulium and their roles in onchocerciasis transmission.^49,50 Improved techniques for identifying different cytoforms of this insect were an important step in understanding the distribution of the parasites in different locations across endemic areas. Similarly, these studies improved the understanding that differences in vectorial capacity can occur with different cytoforms, an important fact that must be considered in identifying the specific role of local blackflies in a specific endemic area.

The well-established approach of blackfly cytotaxonomy has been extremely useful and, hopefully, will be used more often as more young scientists become interested in supporting their national programme efforts. However, genomic tracing will probably give more specific information about fly population migration.¹⁹ Genetic sequence information can be used to assess ‘the per-generation rate of movement of blackflies from one onchocerciasis endemic area to another’,¹⁹ data that will be especially important in situations where eliminating transmission is challenging (e.g. during infection resurgence, and the establishment of new foci of infection) and will hopefully provide much-needed answers.

The use of specialised techniques such as cytotaxonomy, and gene sequencing to define the subtypes of Simulium present in a country, requires training and technical facilities that were available in the OCP but are generally not currently available in many, if not most, onchocerciasis-endemic countries. However, it is important to increase training in these techniques for the new generation of entomologists, and to locate the facilities to carry out these types of investigation in endemic countries.

Vector reduction

The OCP extensively used the Simulium-active larvicides, ‘Abate’ (temephos), an organophosphate that kills larvae by inhibiting an essential nervous system enzyme of the larvae. However, concern about the development of resistance to this agent^51,52 catalysed investigations into the use of other insecticides, with the identification of agents such as the bacterium Bacillus thuringiensis (commonly known as ‘Bt’),⁵³ which produces toxins that kill larvae; Bt is suitable for use in smaller rivers as a biological control of Simulium breeding, as an approach to vector control.

Since the closure of the OCP, and perhaps due to the successes being seen with ivermectin in MDA programmes, vector control has not been a high priority for most national elimination programmes in recent years. However, individual efforts to control vector breeding have been applied in a few areas. The elimination of transmission of onchocerciasis in the contained areas of Bioko Island in Equatorial Guinea was achieved by combining vector control with high coverage with ivermectin⁵⁴; this success on Bioko demonstrates the potential usefulness of vector control. Situations where vector control might be seriously considered include places where challenges arise in consistently implementing MDA (i.e. an inability to achieve adequately high drug coverage for long enough periods: 10–15 y), or when biting rates are so high that ivermectin MDA is ineffective. There may also be specific clinical situations related to onchocerciasis and the vector blackflies that can be addressed by vector control, such as ‘nodding syndrome’, purportedly closely linked to onchocerciasis.⁵⁵

An old environmental approach to vector control once used in Mexico and Kenya in the 1930s and 1940s that has recently been re-evaluated in appropriate Simulium breeding sites, is the active removal of the submerged vegetation where the larvae are deposited (Figure 4). This technique, termed ‘slash and clear’, is helpful only in areas where large volumes of accessible vegetation are serving as the substrate for the fly’s development.^56,57 However, many breeding sites either have limited amounts of vegetation that is able to be cleared, or have non-vegetation substrates that are difficult to remove (e.g. stones and rocks). There is also evidence that the deployment of vector-attracting traps (e.g. an Esperanza trap) can sometimes reduce vector biting rates in nearby areas.⁵⁸

Another example of vector reduction through changing the environment was attempted with the O. volvulus vector S. neavei, a vector of onchocerciasis in areas in East Africa (e.g. Kenya and Uganda); S. neavei larvae and pupae attach themselves to freshwater crabs in the local rivers. Initially, the control approach was to treat or remove the crabs themselves, but this soon changed to the more effective larviciding of the host rivers with DDT (Abate); the latter approach brought about a dramatic reduction in Simulium biting rates.⁵⁹

Elimination programme management

The establishment, maintenance and assessment of national onchocerciasis elimination programmes requires entomologically based knowledge of mapping, breeding-site information and infection prevalence levels (i.e. data on parasite load in the vector’s head: infectivity). Serological assessment in specific age groups of the resident human population for the presence of O. volvulus antibodies provides important additional data, but the major programmatic decisions and the final definition of successful interruption of the transmission of the parasite are based on entomological data. Thus, insect-based data are central to a national programme’s continuing management, and notably for the advice provided by national onchocerciasis expert advisory committees that oversee the programmes for their respective Ministries of Health.^60,61

A significant contribution to the planning and implementation of onchocerciasis-elimination activities that came from the vector research in the OCP period and later, was the defining of different forms of Simulium and their roles in onchocerciasis transmission.^50,62 Improved techniques for defining different cytoforms of this insect vector were a key step in understanding the distribution of O. volvulus in different locations across the endemic areas. The finding that different cytoforms show differences in vectorial capacity was key to identifying the specific roles of local blackflies in an endemic area, as well as understanding issues such as the persistence of parasites in specific areas and parasite resurgence.

The use of techniques such as cytotaxonomy to define the subtypes of Simulium present requires training and technical facilities that were available in the OCP but are generally not currently available in many, if not most, of the current onchocerciasis-endemic countries. It is important to increase training in these techniques for the new generation of entomologists, and to locate the facilities to carry out these types of investigation in endemic countries. Hopefully, blackfly cytotaxonomy will be used more often as more young scientists become interested in supporting the efforts of their national programmes. This is also the case with the newer genomic tracing, which will probably give more specific information about fly population migration and involvement.^19,63,64 Genetic sequence information can be used to assess ‘the per-generation rate of movement of blackflies from one onchocerciasis endemic area to another’¹⁹; this will be especially important in situations where eliminating transmission is challenging (e.g. during infection resurgence and the establishment of any new foci of infection).

The capability to define the specific Simulium species present in endemic areas remains of high importance, especially as known O. volvulus vectors (e.g. S. damnosum s.l. and S. neavei) can occur sympatrically; management of vector control programmes is likely to be improved by such information. Ongoing research seeks to improve the current techniques and protocols essential for detecting and quantifying the parasite in both the vector and the host; currently these tests are primarily molecular (PCR, etc.) or immunological (antigen and antibody detection), respectively, and are sometimes technically complex.^3,65 Most are still currently carried out in major local or regional reference laboratories, and thus current research is aiming towards tests designed for on-site (point-of-use) or at least local laboratory use.

It is essential to point out that there is a critical need for basic entomological expertise to ensure that the insects collected for analysis and testing (PCR, etc.) for the presence of O. volvulus are actually those of the vector Simulium sp. This skill requires, at least until automatic artificial intelligence-based sorting systems are developed, entomological expertise for separating simuliids from other irrelevant insects. Mistakes in the identification of the field-collected insects included in PCR testing can have significant adverse effects on programmatic decisions; for example, these can lead to erroneously low estimations of transmission (by including non-vector insects obviously free of infection); this has already been anecdotally reported by country programmes. There is also a need to improve field methods for catching appetitive (blood-seeking) vectors; challenges in obtaining sufficient flies for adequate parasitological assessment in the laboratory are being observed in some endemic areas, and this is probably being exacerbated by current global climate changes.⁶⁶

An important advance in the management of onchocerciasis control, and now elimination, took place with the development of two computer models that simulated the impact of the major active interventions (vector control, ivermectin distribution) and external influences estimating the time taken to achieving the breaking of O. volvulus transmission. The stochastic simulation model ONCHOSIM evaluated treatment strategies in both Africa and Latin America^67,68; this model considers blackfly biting rates in assessing the impacts of ivermectin MDA and vector control. A more conservative second model, an individual-based simulation model (EPIONCHO-IBM), which focuses on ivermectin distribution rather than vector control, was developed more recently⁶⁹; this latter model predicts a longer time line to elimination of transmission than ONCHOSIM does.

Similar to the issue of genetic resistance that became important with extensive larviciding with temephos issues, resistance also became of concern with the use of ivermectin as a microfilaricide in humans. This issue was highlighted by a report in Ghana in 2011 where the local team reported a suboptimal response to ivermectin’s effect on microfilariae.⁷⁰ Administration of doxycycline, which kills O. volvulus by attacking the essential endosymbiont Wolbachia present in this filaria, was proposed as the solution to removing the potentially ivermectin-resistant parasites in Ghana.⁷¹ Other explanations for suboptimal responses have been proposed, such as reduced specific immune responses to O. volvulus⁷²; it is known that the microfilaricidal effect of ivermectin is likely enhanced by the host’s strong immune response against the parasite.⁷³

Although there have been impressive reductions in the prevalence of O. volvulus across almost all endemic countries following their implementation of ivermectin MDA, as these elimination programmes move closer to national success in breaking transmission, issues related to persistently low levels of parasite presence become more relevant. Consequently, discussions regarding combining ivermectin distribution with vector control,⁷⁴ and perhaps the use of the newer anthelminthic drug moxidectin,⁷⁵ have become more relevant and the inclusion of some form of vector control will likely be an important aspect in national programmes.

Final comments

A primary element in controlling most infectious diseases is understanding and managing the spread between those affected (i.e. the mode of transmission). In the case of human onchocerciasis, knowledge of the blackfly vectors, Simulium spp., and their distribution, behaviour, breeding habits and infection status, has been central to many activities related to this disease over the past 50 y. Indeed, the ultimate indicator for having broken transmission of this infection—that is, the current global goal—is the absence of the parasite in the heads of blackflies: ostensibly an ‘entomological parameter’.³¹ Thus, onchocerciasis is a clear example where knowledge of the blackfly vector is central to programmatic activities and achieving the ultimate goal. Understanding the habits, locations, migration patterns and infection rates is clearly the domain of entomologists, making these specialists central players in the global effort to eliminate onchocerciasis transmission.

Improving parasite-detection tests, both in the vector and in the host (which has also been a major challenge to date), is an issue that needs more intensive investigation. Improving the methods available for capturing blackflies, and safely preventing the development of their larvae in breeding sites, are two valuable goals that would substantially enhance progress towards preventing the transmission of O. volvulus. However, such research requires funding, which is undoubtedly a challenge in an era when securing finance for such infections is, unfortunately, currently ranked as low among the priorities of many organisations and governments for research support.

As shown in this review, entomology and entomologists are major players in virtually all aspects of the onchocerciasis infection complex. However, there are currently relatively few such specialised entomologists, largely due to a lack of career opportunities in the past 10–20 y. Even if there are significant advances in detecting O. volvulus in blackflies in the near future, more individuals with entomological skills in onchocerciasis will be needed if the global goal of eliminating transmission of this infection is to be achieved in the foreseeable future. In recent years, efforts have been made to train more African entomologists on this disease, which will hopefully help to fill this current gap. A major component of entomology in onchocerciasis is having a strong understanding and appreciation of the field aspects (Figure 3); it is therefore essential that training in blackfly field methodology is included in the education curriculum. Similarly, the relatively recent production of the WHO’s manual of entomology is an essential means of disseminating what was often seen as specialised knowledge requiring many years of training.⁷⁶ Hopefully, young scientists, who are already trained in the basics of entomology and working on other insect groups, will enter the blackfly world.

Figure 3.

A Yemeni technician examining blackfly larvae present on vegetation growing in flowing river water present in the onchocerciasis-endemic wadis (valleys) in southwestern Yemen (photograph credit: CD Mackenzie).

Author contributions

Charles D. Mackenzie (Conceptualization [lead], Writing—original draft [lead], Writing—review & editing [lead]), Rory J. Post (Writing—original draft [supporting], Writing—review & editing [supporting]), and Daniel A. Boakye (Writing—original draft [supporting], Writing—review & editing [supporting])

Funding

This supplement was supported by the Reaching the Last Mile Fund (RLMF), a consortium led by His Highness Sheikh Mohamed bin Zayed Al Nahyan, President of the UAE and Ruler of Abu Dhabi, with additional support from the Bill & Melinda Gates Foundation [Grant Number OPP1193778] as a member of the donor consortium of the RLMF at the END Fund.

Competing interests

There are no competing interests.

Ethical approval

Not applicable.

Data availability

Data referenced to is available in the reference provided. The authors are available for further information needed.