Impact of seasonal changes on human onchocerciasis transmission and disease elimination

Abstract

The current guidelines for stopping treatment and verifying elimination of onchocerciasis recommend entomological and epidemiological surveys to be performed during the peak transmission season, which is generally assumed to occur during the rainy season, although this may not necessarily hold true in all transmission zones (TZs). This review has synthesized data, from a literature search, on the effects of seasonality on transmission in West and Central Africa. Seasonality affects vector population dynamics by altering terrestrial and aquatic ecology. In TZs with perennial rivers, peak transmission and peak vector density may either coincide or occur at different periods. These peaks could occur in either the rainy or the dry season in both forest and savanna zones, and the periods may change between years. Therefore, countries should establish updated local biting patterns at a TZ prior to vector collection. Also, while using peak biting density as a convenient indicator for when to commence vector collection (because of the need for a sufficient sample size), the survey period should include months in both seasons to increase the chances of collecting during peak transmission. Seasonality significantly impacts onchocerciasis transmission elimination; and it also offers critical avenues for effective intervention and transmission evaluation.

Background

Human onchocerciasis is still a public health problem in many countries in Africa despite several decades of control.¹ The causative agent, Onchocerca volvulus, is transmitted by blackflies of the genus Simulium. The main vectors in Africa belong to the Simulium damnosum complex, which juvenile stages develop, attached to submerged substrates, in fast-flowing sections of rivers.

Interventions against onchocerciasis in Africa have moved from large scale vector control by the Onchocerciasis Control Programme (OCP) in West Africa (1974–2002), to mass drug administration (MDA) of ivermectin by the African Programme for Onchocerciasis Control (APOC, 1995–2015). Ivermectin MDA is presently the mainstay, and supplementary vector control where feasible, with the current goal being transmission elimination.¹ Transmission elimination of the Onchocerca volvulus parasite involves four phases: disease mapping, intervention, post-treatment and postelimination surveillance, all of which require entomological surveys.

Some aspects of the current WHO guidelines for stopping treatment and verifying elimination of onchocerciasis² are poorly applicable in Africa, despite the continent's long experience of onchocerciasis control. The guidelines, for instance, recommend the collection of at least 6000 blackflies from a transmission zone (TZ) to quantify the level of infectivity of the blackfly population (entomological evaluation), but fail to provide objective criteria for delineating a TZ. This has left countries with various challenges³ and freedom to delineate TZs based on convenience and operational feasibility. In some countries, for example, districts or administrative regions or states are considered as TZs. Also, the stipulated minimum 6000 blackflies may be statistically insufficient in most of the very large TZs in Africa.

In addition, the WHO guidelines recommend both entomological and serological surveys to be performed during the peak transmission season. It has been generally assumed that peak transmission occurs in the rainy season when the blackfly density is assumed to be greatest. Nevertheless, this may not hold true for every site within and across TZs. Therefore, collecting large numbers of blackflies requires understanding of the vector population dynamics for optimal timing of the collection period and appropriate selection of collection points. The timing also requires consideration of when transmission is at its peak to increase the chances of detecting any residual infections. However, there is a paucity of knowledge regarding which period of the year peak transmission occurs.

Knowledge accumulated during the many years of vector control by the OCP in West Africa and other published works has shown that seasonal changes have a bearing upon the vector dynamics and disease transmission. Knowledge of this seasonal fluctuation in S. damnosum s.l. breeding sites and spatiotemporal distribution and age-structure of the cytoforms (cytospecies and cytotypes) in a TZ is important for guiding the design and execution of surveys, especially as the cytospecies differ in their efficiency to transmit O. volvulus.^4,5 Also, knowledge of vector population dynamics is crucial in predicting the impact of interventions on onchocerciasis transmission.⁶ This review aims to leverage the extensive knowledge from the OCP, APOC and other scientific resources to address the critical question regarding the optimal timing of entomological surveys and other related programmatic activities.

Methods

Data sources and search strategy

This review was focused on information related to blackfly vectors in West and Central Africa. A search was made in PubMed, RePORTER, Scopus and the WHO Institutional Repository for Information Sharing (WHO IRIS) with the following Medical Subject Headings (MeSH) and keywords (((Season OR Seasonality OR Climate change OR Environmental factors) AND (Onchocerciasis OR Onchocerca volvulus) AND (Transmission) AND (Vector OR Blackfly OR Black fly OR Simulium))). The search on WHO IRIS was further refined by selecting three main author categories: African Programme for Onchocerciasis Control, Onchocerciasis Control Programme in the Volta River Basin Area and Onchocerciasis Control Programme in West Africa. French literature was obtained by searching the Horizon Pleins Textes (IRD) database using different combinations of the keywords: onchocerciasis (‘onchocercose’), season (‘saison’), vector (‘vecteur’), Simulium, transmission. Additional papers and reports were obtained by reading through the reference lists of included papers, and via a direct search on Google using the appropriate keywords. English and French papers (peer review articles and reports) were included up to November 2024.

Inclusion/exclusion criteria

Searched records (papers) were systematically included or excluded (Figure 1) from the study beginning from reading the title to abstract to the methodology and then the entire paper. WHO IRIS papers were initially scanned in whole for any relevant topic because most of them were not scientifically structured papers. Papers included for comparing entomological indicators were those whose results for the indicator(s) were presented separately for the two seasons (rainy season and dry season). Papers relating to ecological/environmental factors influencing development and movement of the vectors were selected based on the study area (West and Central Africa) and their relevance to seasonality. To compare the relevant entomological indicators with respect to season and bioecology, mostly papers that stated the vegetation type or the bioecology of the study sites were exploited. However, in a few instances, the vegetation type or the bioecology of the study sites were searched on the internet and obtained from other peer-reviewed publications published around the same period from the same area.

Figure 1.

Inclusion and exclusion criteria flow diagram of identified records. WHO IRIS: WHO Institutional Repository for Information Sharing.

Data extraction

Data related to the effect of seasonality on the distribution, development and movement of S. damnosum s.l., and on human exposure and transmission indices (biting, parity, infectivity), were exported into Microsoft (Microsoft Corporation, Washington, USA) Excel spreadsheet. Also, information on the ecology and environmental factors of the study area and their influence on the vector were retrieved. This was done by the lead author (FA).

Results

Included papers

A total of 1268 papers were screened from PubMed (147), WHO IRIS (935), Scopus (129), Horizon Pleins Textes (IRD) (11), RePORTER (12), direct Google search (21) and Search from references (13). Seventy-three papers were exploited for this review, addressing onchocerciasis in 12 countries in West and Central Africa (Table 1). Most studies contained data from Cameroon (n=18), Nigeria (n=11) and Ghana (n=8). Simulium damnosum s.s. (32 papers), S. sirbanum (26) and S. squamosum (21) were the most frequently analyzed vectors (Table 1).

Table 1.

Some effects of seasonality on entomological indicators and risk factors in the three ecological zones, and the countries and cytospecies of Simulium damnosum s.l. in the included papers

Ecological zone	Effect of seasonality	Country	Vector species (number of papers)	Method of species identification	Number of papers on entomological indicators (breeding sites productivity, parity rate and infection/transmission)	Number of papers on ecology/environmental factors on vectors/vector movements/species distribution only*	Publication years
Forest	• Not very drastic seasonal changes in climatic/environmental factors; linear and radial dispersal occur in both seasons	Liberia	S. soubrense (1), S. yahense (4), S. sanctipauli (1)	Morphology, Cytotaxonomy	70, 71	9, 13, 29	2015, 1976, 1960, 1984, 1987
		Nigeria	S. soubrense (1)	ND	51, 52, 53, 54, 56, 69	10, 11, 15	2021, 2015, 2008, 2010, 2005, 2008, 2023, 1999, 2022
	• Several perennial vector breeding and productive sites; peak biting season depends on nature of river	Ivory Coast	ND	ND	ND	12, 28	1966, 2012, 1964
		Cameroon	S. mengense (1), S. soubrense (1), S. squamosum (1), S. yahense (1), S. damnosum s.s. (1)	Cytotaxonomy	17	13, 24, 29	1976, 2022, 1976, 1960
	• Year-round parasite transmission in most perennial sites; peak transmission may occur in either the rainy or dry season	Togo	S. yahense (2), S. squamosum (3), S. sanctipauli (1), S. damnosum s.s. (2), Djodji form of S. sanctipauli (1)	Morphology, cytotaxonomy	66, 63	19, 20	2023, 1983, 1988, 1992
	• Higher exposure in open farmland in rainy season and working in plantation (cocoa, rubber)	Sierra Leone	S. sanctipauli/soubrense (1), S. yahense (1), S. squamosum (1)	Isoenzyme electrophoresis, morphology	55	67	1990, 1990
	• Changes in species composition due to immigration of savanna vectors during the dry season	Ghana	S. yahense (1)	Morphology	68		1992
Savanna	• Drastic seasonal changes in climatic/environmental factors; mainly linear dispersal occurring underneath riverbank tree galleries	Ghana	S. damnosum s.s. (3), S. sirbanum (2)	ND	ND	9, 14, 57	2015, 2012, 1971
		Burkina Faso	S. damnosum s.s. (1), S. sirbanum (1)	Morphology	43	12, 28	1966, 1964, 2019
		Mali	S. sirbanum (4), S. damnosum s.s. (2)	ND	37, 38, 44	14, 39	2012, 2012, 2009, 1966, 1983
		Niger	S. sirbanum (1)	ND		14	2012
	• Strictly rainy season breeding in many temporary streams/rivers	Ivory Coast	S. damnosum s.s. (2), S. sirbanum (1), S. sanctipauli/S. soubrense (1)	Morphology	ND	14, 16	1983, 2012
	• Year-round or seasonal breeding in the few perennial rivers; peak biting and transmission mostly in the dry season	Togo	S. damnosum s.s. (2), S. sirbanum (1), S. sanctipauli (1), S. soubrense (2), S. squamosum (2), S. yahense (1)	Morphology, cytotaxonomy	ND	16, 19, 20, 25	1983, 2023, 1983, 2023
	• Absolute seasonal (rainy season) transmission in very dry savanna areas	Benin	S. damnosum s.s. (1), S. sirbanum (1), S. soubrense (1), S. squamosum (1)	Morphology, cytotaxonomy	ND	16, 19, 20	1983, 2023, 1983
	• Changes in species composition due to vector emigration in the dry season and immigration in the rainy season	Cameroon	S. damnosum s.s. (7), S. sirbanum (6), S. squamosum (4), S. yahense (1)	Morphology, cytotaxonomy	41, 50, 58, 60	17, 18, 61, 72, 74	2022, 2024, 2016, 1987, 1987, 1990, 1975, 2001, 1987
	• Higher exposure in the dry season around perennial rivers serving as a center for household and economic activities (e.g. irrigation farming)	Senegal	S. sirbanum (2), S. damnosum s.s. (2)	ND	37, 38	ND	2009, 2012
		OCP$	S. damnosum s.s. (1), S. sirbanum (1), S. squamosum (1)	Morphology, cytotaxonomy, isoenzyme electrophoresis	42	21, 22, 26, 34	1979, 1995, 1990, 1979
Forest-savanna transition/Guinea savanna	• Considerable seasonal changes in climatic/environmental factors; mainly linear dispersal underneath riverbank tree galleries, with little radial dispersal in the rainy season	Ghana	S. damnosum s.s. (3), S. sirbanum (3), S. sanctipauli (1)	Cytotaxonomy, morphology, molecular	45, 48, 62	33	1966, 2020, 2024, 2014
		Nigeria	ND	ND	36	11, 23, 31	2015, 1983, 2008, 1955
		Burkina Faso	ND	ND	ND	12,13	1966, 1976
		Cameroon	S. mengense (4), S. squamosum (6), S. damnosum s.s. (2)	Morphology, cytotaxonomy	46, 47, 49, 65	17, 18, 30, 73, 76	2022, 1998, 2000, 1998, 2021, 2022, 2022, 2024, 1987
	• Year-round parasite transmission in most perennial sites; peak biting or transmission may occur in either the rainy or dry season	Benin	S. damnosum s.s. (1), S. sirbanum (1), S. soubrense (1), S. squamosum (1)	Cytotaxonomy	ND	16, 19	1983, 2023
	• Higher exposure in the dry season around perennial rivers serving as centers for the seasonal camping of farmers and nomadic herdsmen	Togo	S. damnosum s.s. (1), S. sirbanum (1), S. sanctipauli (1), S. soubrense (1), S. squamosum (1), S. yahense (1)	Cytotaxonomy	ND	16, 19	1983, 2023
		Sierra Leone	S. sirbanum (1)	Morphology	ND	35	1995

ND: Data/information not available; OCP: Onchocerciasis Control Programme.

^*These papers do not contain data for entomological indicators such as breeding sites productivity, parity rate and infection/transmission.

^$Studies involving several countries of the OCP area.

Ecology and rainfall of study areas (West and Central Africa)

The ecology in African settings is generally separated into savanna and forest zones, with several forest-savanna transition areas resulting from persistent deforestation. The area experiences two distinct seasons: rainy (wet) and dry seasons. Rainfall is influenced by shifts of the Inter-Tropical Convergence Zone and the accompanying West African Monsoon.⁷ Rainfall in areas below 10°N is bimodal while above 10°N a single peak occurs in mid-summer (around August).⁷ The rainy season is generally longer in forest (March to October) than in savanna zones (June/July to October). The effect of global warming is projected to affect the area by intensifying the water cycle, its variability and monsoon precipitation.⁸

Effect of seasonality on the vectors and transmission elimination

Seasonality and species distribution

Geographical and multiple ecological factors govern the colonization and proliferation of blackfly taxa at the breeding sites.⁶ These ecological requirements differ among Simulium taxa, even among taxa of a species complex.^6,9 Hence, water physico-chemical features (e.g. temperature, pH, discharge rates, conductivity and river size) are important in selection of breeding rivers by cytoforms of the S. damnosum complex.^6,10–15 Therefore, changes in water temperature may affect the distribution of these cytoforms.^9,14 Because these hydrological features are liable to change between seasons (e.g. increase in water temperature in the dry season), this may in turn lead to changes in the species composition. Consequently, seasonal changes in species composition have been observed at breeding sites in Togo¹⁶ and northern Cameroon,^17,18 involving both savanna and forest cytoforms. Seasonality also causes changes in species distribution due to seasonal migration associated with particular cytoforms.^16,18–22

Seasonality and vector movements

The dispersal distance of a blood-seeking female fly depends on shade temperature,²³ the biting density, the availability of vertebrate host and the probability of obtaining a full blood meal.²⁴ Hence a larger proportion of dispersive blackflies consists of nulliparous flies.^25,26 Blackflies either disperse radially in all directions from the breeding site, or linearly along the watercourse.^26,27 Radial dispersal is favored by high humidity, cloudy or foggy weather and the presence of shades provided by tree canopy.^23,26,28,29 Tree cover (e.g. in cocoa, banana, rubber plantation, gallery forest) prevents direct sunlight and also provides still air space underneath, which is necessary for smooth and rapid flight by the blackfly.^28–30

Forest areas do not experience drastic variation in humidity, cloudiness and tree covers between seasons.²⁸ Hence, dispersal in forest areas is both linear and radial in both seasons, although involving longer distances during the more humid rainy season.^26,28,29 Radial dispersal in savanna areas is low, except during the rainy season, and mostly occurs in Guinea savanna areas.²⁷ Hence female blackflies are mostly concentrated around the breeding sites in savanna areas.^28,29 Linear dispersal is most common in savanna areas, covering considerable distances following the shade provided by uninterrupted tree galleries around the riverbanks.^27,28

Generally, daily radial dispersal of S. damnosum s.l. in search of bloodmeal covers on average 15–20 km^22,31,32 around their breeding site. Also, they may disperse linearly up to 96 km in search of suitable breeding sites.^24,33 Seasonal effects such as the drying up of breeding sites in the dry season, together with the northeasterly Harmattan winds at the beginning of the dry season, and the southwesterly monsoon winds during the early rainy season, result in long-distance bidirectional migration of mostly savanna flies (S. sirbanum and S. damnosum s.s.: >400 km).^21,22  Simulium squamosum, a forest-dwelling blackfly, also migrates northward during the heavy rainy season,^18,20 covering >150 km.²⁰ Hence, reinvasion by migratory blackflies was a major challenge during vector control activities of the OCP.^22,34,35 In fact, seasonal expansion of geographical ranges and relative abundance of cytoforms¹⁹ is common in West and Central Africa. Therefore, the blackfly collection period for entomological assessments should be planned to incorporate these movements to maximize the diversity of species collected. This will ensure the collection of migrating blackflies, which are usually parous and infective.^21,34

Seasonality in breeding sites and adult flies’ productivity

It takes about 10–20 d for S. damnosum s.l. eggs to develop to adults. The biting density of adult blackflies is directly related to the density of preimaginal stages.²⁷ The establishment of S. damnosum s.l. breeding sites requires the presence of submerged suitable substrates near the surface of the river, adequate water current and the presence of larval food.¹² In addition, other extrinsic factors such as the physicochemical properties of water (temperature, pH, discharge rates, conductivity and river size) are important in the colonization of potential breeding sites.^6,10–14 Therefore, breeding and productivity of a potential breeding site occur when the appropriate favorable factors are united.

There exist variations in seasonal breeding of blackflies in savanna, forest-savanna and forest ecological zones.¹⁷ In savanna areas in the OCP and other parts of West and Central Africa, the distribution of breeding sites and their productivity of adult flies peaked during the rainy season.^17,26,36 In very dry savanna zones (Sahel zones), blackflies breeding is limited to the few months (3–6) of the rainy season during which the rivers are flowing.^37–39 In the dry season, breeding sites prevalence and productivity reach a minimum given that most of the seasonal streams dry up. In some of these areas, however, the perennial rivers become productive mainly during the dry season. This is because these perennial rivers flood in the rainy season, resulting either in insufficient water current to form rapids,²⁶ or in increased water current that sweeps off or deeply submerges larval supports and increases water turbidity.^17,36 In such areas, breeding resumes or increases in the dry season when the water is at intermediate to low levels and the rocks and supports have been exposed while the water has become less turbid.^17,26,36,40 Therefore, the highest biting rates in savanna areas occur in the rainy season, in areas around the seasonal streams/rivers, or in the dry season in areas around the perennial rivers.^17,41

The rainy season peaks of adult blackfly biting density usually occur during the early and late rainy seasons⁴² while the dry season peak is usually in the mid to late dry season.^41,43 This is because, at the beginning of the rainy season when the seasonal rivers start flowing, flies return to the breeding sites to occupy the newly formed rapids, while the next peak at the end of the rainy season is a result of the stability of the water level and the resurfacing of the larval supports that had been deeply submerged during the months of maximum precipitation.^36,40 Meanwhile, fluctuation in water volume disfavors the breeding of S. damnosum s.l., hence, the sudden increase in water volume in the rainy season^28,44 or an abrupt decrease at the beginning of the dry season²⁸ results in decreased S. damnosum s.l. breeding.

Blackflies breeding and biting usually occur throughout the year in most medium to large rivers in Guinea savanna and forest-savanna transition. However, some seasonal patterns occur in these rivers with some sites having maximum fly density during the dry season^45,46 while other sites show peaks in the rainy season.^23,47,48 This contrasting seasonal pattern occurs even between sites along the same perennial river in the same area.⁴⁹ In such a scenario, the most plausible explanation may not be the stability of the water level or exposure of submerged supports,^49,50 but rather seasonal differences in dispersal of the vectors between the sites. In fact, in the study where the discrepancy was observed in sites along the same river,⁴⁹ the site with higher fly density in the dry season showed higher dispersal rates in the rainy season (as sites further away from it had peak biting in the rainy season).⁴⁹

In forest areas, breeding sites are common in both rainy and dry seasons and the peak breeding period may occur in either of the two seasons because most rivers are perennial (except the small streamlets). Studies have found breeding sites and productivity of adult blackflies to be higher in either the dry^17,51 or the rainy^10,52–56 season. The dry season peak is, as above, due to exposure of submerged vegetation and rocks leading to increased rapids and larval supports. On the other hand, the rainy season peaks occur because, while the increased water volume leads to disappearance of the rapids formed by interlocking rocky beds, new and often larger breeding sites are formed from increased water current.^12,28

Depending on the year,⁵⁷ environmental factors such as the early or late arrival of rains and climatic changes may affect the period of availability and productivity of breeding sites. For instance, Cheke and Garms²⁰ observed that many rivers that were productive in the same period in the preceding years remained dry during the same period in 1981. Also, Ayisi and colleagues^17,41 observed seasonal breeding (only during the dry season) in the Vina du Nord River in northern Cameroon, although previous studies had observed year-round breeding at this site.^58–60

Seasonality, parity rate and infection/transmission by blackflies

Higher parity signifies a higher risk of transmission because parous flies must have fed on blood at least once, while nulliparous flies have never fed on blood. The parous rate is affected by the longevity and the rate of emergence of young blackflies, as well as dispersion and immigration by adult blackflies.⁶¹ Consequently, the parity rates assessment indicates the age structure of the flies and serves as a proxy for the success of larviciding.^34,61 The parity rate is important in deciding when to stop MDA, hence the threshold for stopping MDA (<1 infective larva in 2000 blackflies) assumes a parity of 50%.²

In the absence of migration, the parous rates are expected to be lower during the peak blackfly production season due to the high turnover of teneral adults emerging from breeding sites. This trend has been observed in forest-savanna areas in Cameroon and Ghana^49,62 and in forest areas in Ghana and Nigeria.^52,53,62 However, higher parous rates can also coincide with peak vector density.^{41,46,47,51,63} This mostly occurs in the dry season^41,46,51,63 and can be explained by the presence of immigrant flies from seasonal streams, preferential dispersal of nulliparous flies from the riverbank^25,60 and greater dry season longevity of S. damnosum s.l.¹²

The force of transmission of onchocerciasis is contributed by the vector density, vectorial capacity and the parasite density in the skin of the host. Therefore, transmission is expected to be greatest when these factors are at their peaks. The peak transmission season typically aligns with the highest levels of microfilaridermia and biting density.^46,64 This is likely a natural co-adaptation to enhance propagation of the parasite by the vector.

The peak transmission season of onchocerciasis varies across geographical and ecological zones. In savanna areas, transmission is either restricted to the rainy season (around seasonal streams/rivers) or predominant in the dry season (around perennial rivers).^41,46 A high transmission by the perennial rivers during the dry season likely results from a locally breeding vector population coupled with infected immigrant blackflies coming from the seasonal streams. In the savanna areas covered by the OCP, the precise peak transmission period was habitually at the start and the end of the rainy season.⁴² Slightly similar to that, transmission around perennial rivers in forest-savanna and savanna areas was highest during mid to late dry season, sometimes extending to the early rainy season.^41,47,49,65 This is irrespective of the cytoforms of S. damnosum complex involved.

The risk of transmission in forest areas mostly occurs throughout the year as most rivers maintain sufficient flow to support breeding. The peak transmission season varies from one forest area to another, either occurring in the rainy season,^{53–55,66–68} and sometimes exclusively so (despite the presence of vectors in the dry season),^54,55 or in the dry season,^{49,56,63,69–71} sometimes consisting of >73% of annual transmission.⁷⁰ These contrasting observations may be due to seasonal differences in human and vector movements.

The force of transmission most often reaches a maximum when the blackfly density is greatest.^{41,42,46,49,51,69} However, some studies^47,65,71 have observed transmission peaks occurring outside of the peak biting period. Whether the peak transmission and biting density coincide or not seems not to depend on geography, but probably on undetermined factors related to vector longevity, cytospecies and migration. Hence, studies in different years in the same area showed peaks coinciding in some years⁴⁹ but not in others.^47,65

Seasonality and risk/exposure of population

Activities that bring humans close to breeding sites increase their exposure to blackfly bites and, hence, the risk of O. volvulus infection. Sometimes these activities are seasonal or they peak during certain seasons, thereby conferring seasonal trends in human population/subpopulation exposure. For instance, cocoa farming mostly intensifies during the rainy and early dry seasons; so too does fishing around seasonal streams, although this only occurs in the rainy season. Hence, sand mining, hunting, fishing and farming (cocoa, banana, rubber) near breeding sites,^30,31,47,72 or visiting open farmland in the forest zone during the rainy season,^55,67 exposes individuals to high numbers of bites and thus the risk of infection. In addition, working with or using a ferry to cross large bodies of water may increase the risk of infection and disease.^49,72

Most S. damnosum s.l. species adults have a maximum longevity of about 30 d, with savanna flies living longer than forest flies, and they are mostly concentrated near the breeding sites.^12,28 As seasonal streams and rivers in savanna areas dry up during the early to mid-dry season, the few perennial rivers experience an increase in human activities for household and economic needs, such as fishing, laundry, irrigation farming, sand mining and bathing. This coincides with the time when the breeding of blackflies is usually at its peak,⁴¹ increasing exposure.

Furthermore, the perennial rivers in savanna and forest-savanna areas often serve as points for transhumance by cattle herders.^73,74 The presence of large cattle numbers provides an alternative blood meal source for blackflies and confers zooprophylactic protection for the human population.^58,74 On the other hand, the seasonal camping of nomadic herdsmen with their cattle and, frequently, of farmers by the riverside, exposes them to a higher risk of infection.^72,73

In summary, seasonality affects environmental and human elements that impact the vector dynamics and the risk of onchocerciasis infection (Figure 2).

Figure 2.

Effect of seasonality on risk factors of Onchocerca volvulus transmission. CMFL: Community Microfilarial Load.

Seasonality effects on onchocerciasis elimination programmatic activities

Seasonality has a strong bearing on the programmatic activities in the different phases of transmission elimination of O. volvulus. Ideally, annual MDA should occur just before the peak transmission season/months to optimally suppress transmission during the expected peak period.⁷⁵ Equally, the cost and effectiveness of vector control would be impacted by seasonality effects.^32,76 In addition, seasonal movement of human populations contributes to non-compliance to MDA,^77,78 thereby affecting transmission elimination. Table 2 summarizes the effects of seasonality on some programmatic activities.

Table 2.

Effect of seasonality on major events of onchocerciasis transmission elimination programs

PROGRAM EVENT	EFFECTS OF SEASONALITY
MDA	Drug coverage
	• Difficult distributing in rainy season in remote/enclaved areas90
	• Absenteeism or influx of seasonal migrants (farming or transhumance)73,77,78
MDA	Effectiveness of MDA
	• Timing of IVM distribution just before peak biting season75
Epidemiological survey	Scheduling of survey
	• Timing of survey at peak transmission season2
OEM	Identification of vector breeding sites
	• Essential in defining need for intervention91
	• Requires survey in both seasons17
Breeding site mapping	Identification of vector breeding sites
	• Essential in defining an active program area91
	• Essential for selecting evaluation sites91
	• Requires survey in both seasons17
	• More challenging during rainy season
Monitoring impact	Density of biting flies
	• Ability of collecting adequate flies for valid assessment2
Vector control	Efficacy and cost
	• Affects discharge rates, hence volume of insecticide needed32
	• Ease and efficiency33,76
PES	Presence of larvae and adults
	• Ability of collecting sufficient flies for assessment2

IVM: ivermectin; MDA: mass drug administration; OEM: onchocerciasis elimination mapping (reassessment of onchocerciasis transmission in all areas previously excluded from intervention); PES: postelimination surveillance.

Discussion

The results show that seasonality affects the important entomological indicators and risk factors of O. volvulus parasite transmission and elimination in the study area. This is consistent with studies in endemic countries in Latin America.^79–81

The presence of life stages of Simulium vectors is one key indicator of possible O. volvulus transmission. Because the vectors require specific bioclimatic and environmental conditions to propagate, seasonality significantly impacts parasite transmission. It affects the ability of the vectors to disperse around the breeding site, and to embark on long-distance wind-borne migration. Season-related changes in macro- and micro-ecological conditions of the aquatic (e.g. temperature, pH, conductivity, discharge rate) and terrestrial (e.g. air temperature, wind, cloudiness, availability of shades) environments (Figure 1) induce spatiotemporal redistribution of the vector taxa. There are three major consequences of such regular seasonal redistribution of the blackfly vectors to onchocerciasis elimination programs: (i) it results in fluctuation of vector density at the breeding sites; (ii) dispersing or migrating vectors can carry infections to areas that have been cleared of transmission; and (iii) the introduction of more competent vector taxa to new areas.

Knowledge of the location's specific seasonality effects is critical for planning, budgeting and implementation of vector collection to quantify the transmission potential. Periods of high vector densities are usually specific to the ecological zone (savanna or forest), but also to the nature of the river (perennial or seasonal; rocky or sandy riverbed). As a general rule, in savanna zones, perennial rivers with rocky beds attain peak vector densities during the dry season, while fly densities around seasonal streams and rivers are greatest during the rainy season and are usually zero in the dry season. Some perennial streams in savanna zones do have breeding in both seasons, with a minor peak in the rainy season and a major peak in the dry season. Year-round breeding occurs in most forest areas with breeding usually stable throughout, higher in the dry season,¹⁷ or higher in the rainy season.¹² Given the requirement of collecting large numbers of blackflies, elimination programs should therefore plan blackfly collection to span the period predicted to have high vector densities.

The seasonal patterns of the important indicators and risk factors of onchocerciasis transmission (biting rates, breeding sites availability and productivity, parity, infectivity, vector movement) may vary over time and between years. Although peak biting rates do not always coincide with peak periods of the other important indicators such as parity and infectivity, fly abundance remains the most convenient indicator to determine and use in choosing when to commence blackfly collection. It is therefore recommended to establish more recent blackfly biting dynamics and not to depend on historical data. This is because climate change and human activities can affect river flow and local ecosystem,⁸² thereby affecting blackfly breeding (presence or absence of breeding sites), or breeding period (dry vs rainy season), or breeding duration (seasonal or perennial). For instance, dam construction led to the disappearance of breeding sites in Sudan^83,84 and Ghana,⁸⁵ while it led to perennial breeding at a historical seasonal site in Burkina Faso.⁴³ Also, changing patterns in land use, climate change and water pollution are possible reasons for the disappearances of Simulium vectors from historical breeding sites.^86,87 Recent blackfly biting dynamics should be established by performing initial spot test catches 1 y prior, guided by community knowledge of patterns of blackfly activity from key informants.⁸⁸

The goal of fly collection in programmatic settings is to capture large numbers of flies over a period and duration that optimizes the likelihood of collecting any infected specimens in the population.² Ideally, collections for verification of transmission interruption/elimination should be done throughout several years to maximize the chances of detecting any circulating parasite. However, largely due to budgetary constraints, most countries are often left with one option: fly collection within a few months (<1 y, usually 4–8 mo). Nevertheless, with sufficient advance knowledge of seasonal patterns in a TZ coupled with community knowledge, surveys for impact assessment or verification of transmission interruption can be effectively scheduled to achieve the best possible results within the allocated time.⁸⁹ The fly collection period within the year should be sufficiently long enough to enable collection of large numbers of blackflies (depending on the size of the TZ, at least 6000 flies per TZ) containing a high proportion of parous and potentially infective flies. Hence, fly collection in TZs with perennial breeding should include months in both the rainy and dry seasons, because parity and parasite transmission peaks do not usually coincide with peak fly abundance.

There is heterogeneity in infection of individuals in communities, and this is related to their routine activities that expose them to infection.^59,67 Seasonality further compounds exposure by creating specific environments that favor the aggregation of people in high-risk sites in the community for economic, leisure and household activities.

Knowledge of seasonality patterns is important in effectively implementing other programmatic activities in the four phases of transmission elimination. For instance, when feasible (considering logistics, as well as vector and human inter-migration), to schedule annual MDA in different TZs in a country based on their peak transmission seasons. Also, to strategically implement complementary vector control (larviciding, ‘Slash and Clear’) during the dry season at the perennial rivers in savanna zones, which, during this time, serve as a reservoir for vectors from the seasonal streams/rivers and transmission indicators and would be at their peak. These would contribute to accelerate the interruption/elimination of transmission.

In conclusion, seasonality greatly impacts onchocerciasis transmission and elimination. There are important regional and local seasonal patterns in vector population and transmission dynamics and peaks. The basic pattern is that biting and transmission peaks occur in the rainy season, but there are exceptions when these peaks occur during the dry season or the transition months. The pattern at a TZ is dependent on the ecology (savanna vs forest), the nature of the river (perennial vs seasonal) and also on the riverbed geology (rocky or sandy/muddy). It is, therefore, important to establish local seasonal biting patterns at the TZ before commencing vector collection for entomological evaluations. Because the peak transmission season (or months) may occur before, during or after the peak biting season (or months), blackfly collection should be scheduled to cut across both seasons. Collecting in both seasons will equally enable the inclusion, in the sample, of all possible vector species that occur at some point in the TZ (including immigrant flies).

Authors’ contributions

DAB, DKD and FA conceived and wrote the original draft of the manuscript. All the authors were involved in writing, reviewing and editing the manuscript.

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, and some aspects of the study by the UNICEF/UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (WHO/TDR) and the END Fund (New York, NY, USA).

Competing interests

None declared.

Ethical approval

Not required.

Data availability

The data underlying this article are available in the article.