Population-based prevalence survey of follicular trachoma and trachomatous trichiasis in the Casamance region of Senegal

Trachoma is the leading infectious cause of blindness worldwide [1]. Repeated ocular infections with the bacterium Chlamydia trachomatis can lead to subepithelial follicles (trachomatous inflammation, follicular (TF)) and/or inflammation (trachomatous inflammation, intense (TI)). TF and TI are referred to as active trachoma, which is usually found in children. After years of infection, trachomatous scarring (TS) can occur, resulting in the eyelid contracting and causing the eyelashes to turn inwards and scratch the cornea (trachomatous trichiasis, TT), leading to corneal opacity and blindness [2].

The World Health Assembly has set a target for the Global Elimination of Blinding Trachoma by the year 2020 (GET 2020) [3], to be achieved through implementation of the SAFE strategy for trachoma control: Surgery for TT, Antibiotics to treat active disease, Face washing and Environmental improvement. The latest World Health Organization (WHO) guidelines are that any individual with TT should be offered surgery, but that surgery should be prioritised where the prevalence is >0.1%. Elimination of TT as a public health problem is achieved when there are fewer than 2 cases of TT unknown to the health system per 1000 adults aged 15 years or above at the district level (or <1 case per 1000 total population) [4, 5]. Districts and communities with a TF prevalence of ≥10% in 1–9 year-olds should receive mass antibiotic treatment annually for a minimum of three years, before re-assessing the prevalence to determine whether treatment can be discontinued (when TF prevalence in 1–9 year-olds falls <5%) [4]. There are no recommendations for the use of facial cleanliness and environmental improvement indicators for the assessment of trachoma elimination, but these SAFE strategy components should be implemented at any TF prevalence level [4–6].

The dry, arid, Sahel belt of West Africa reports some of the highest prevalence rates for TF and TT [7]. In The Gambia, trachoma was the second leading cause of blindness in 1986 [8], but following formation of the National Eye Health Programme (NEHP) which implemented trachoma control activities, the prevalence of active trachoma in 0–14 year-olds decreased from 10.4% to 4.9% (a 54% reduction) by 1996 [9]. In 2006, TF prevalence in 1–9 year-olds remained ≥10% in two Gambian regions (12.3% and 10.0%) [10], and mass drug administration (MDA) with azithromycin was initiated in 11 rural districts. In 2011, results from the Partnership for the Rapid Elimination of Trachoma (PRET) showed that the overall TF prevalence in four districts was 2.8% (compared to 6.5% at baseline in 2008) [11]. The Gambia’s NEHP has subsequently reported national prevalences of TF ranging between 0.2 and 3.2%, and TT ranging between 0 and 1.7%, suggesting that The Gambia has reached the elimination target for TF but that further efforts are needed to reduce the burden of TT [12]. Similarly in Mali, the National Blindness Prevention Programme (PNLC)’s trachoma control programme formed in 1998 has helped reduce TF prevalence from a range of 23.1–46.7% in the 1990’s to below 10% in 84% of districts in 2013 [13]. Approximately 27,000 more TT surgeries are required to meet the elimination of trachoma as a public health problem target of fewer than two cases of TT unknown to the health system per 1000 persons aged ≥15 years [4, 5]. Trachoma prevalence data from Guinea Bissau are limited, but a population-based prevalence survey in the Bijagós Archipelago found 22.0% active trachoma in 1–9 year-olds [14], and prevalence of TT is reported to be 3.5% [15].

In Senegal, whose northern regions lie to the west of the Sahel area, the last national trachoma survey was conducted in 2000, and showed that 10.8% of children aged less than 10 years had active trachoma, 2.6% of women aged over 14 years had TT, and 1.4% of women aged more than 14 years had corneal opacity [16]. A study conducted in 2004 in the Nioro department (within Kaolack Region, which had a prevalence of 6.8% in the 2000 survey), had an active trachoma prevalence of 17.4% in children aged 2–5 years [17]. These results demonstrate that trachoma is a public health problem in Senegal, with heterogeneity throughout the country. The Senegalese national programme for trachoma control began in 2004, and mass treatment of districts commenced in 2005.

The Casamance region of Senegal (Fig. 1), which underwent low-level conflict for approximately 20 years since the 1990’s, was not included in the national trachoma survey, and therefore the appropriate SAFE trachoma control efforts could not be targeted or implemented. A prevalence survey in the Casamance region was needed so that the Senegalese National Eye Care Programme (NECP) could plan its trachoma control activities (number of TT operations, requirements for mass antibiotic treatment, and whether hygiene and sanitation interventions were needed). Furthermore, capacity building was required in this region to enable the NECP to conduct its own trachoma prevalence surveys to assess control intervention needs and impact, and provide data to the WHO.

This is the first trachoma survey to be conducted in the Bignona Department of Casamance in the Casamance region of Senegal. The estimated prevalence of TF in 1–9 year olds was 2.5% (95% CI 1.8–3.6) and the prevalence of TT in adults over the age of 14 years was 1.4% (95% CI 1.0–1.9). Both the TF and TT prevalences are lower than those reported in Senegal’s national trachoma survey conducted in 2000 (10.8% active trachoma in children <10 years, and 2.6% TT in women aged >14 years) [16]. The prevalence of TT in women in our study was 1.8% (95%CI 1.3–2.4).

The WHO determines that trachoma elimination has been achieved in a country if the TF prevalence in 1–9 year olds is <5% (precision of 4%, with a confidence interval of 2%) and the prevalence of TT cases unknown to the health system is <0.2% (2 cases per 1000 people aged ≥15 years) [4, 5]. In order to verify elimination, countries are required to meet WHO criteria for elimination and to demonstrate that this is sustainable for at least three years following cessation of programmatic interventions.

The WHO implementation units for trachoma elimination purposes are defined as districts (population between 100,000–250,000 individuals), which are the normal administrative unit for health care management, sub-districts (groupings of at least three villages permitting sub-unit stratification of a district) and villages (population between 8000 and 20,000 individuals) [5]. As the Casamance district population sizes were 66,135 (Sindian), 91,322 (Tenghori), 18,033 (Tendouck) and 56,937 (Diouloulou), we interpreted prevalence data at the Bignona Department of Casamance regional level, as opposed to the district level, because its population size of 232,427 equates to that of a WHO standard district level administrative unit [4, 19]. The TF prevalence at the regional level in 1–9 year olds was lower than the 10% WHO threshold, indicating that community MDA is not required (although facial cleanliness and environmental improvement efforts may continue), and was lower than the 5% threshold, indicating that TF is not a significant public health problem in this region or its districts [4, 6]. This is supported by the low TI prevalence of 0.5% in 1–9 year-olds, especially as TI is less specific as a clinical sign of trachoma than TF is [23].

Despite the encouraging TF results at the regional level, of the 60 communities surveyed in the Bignona Department of Casamance, two had a TF prevalence ≥10%, indicating they may require annual MDA for three years in addition to interventions promoting facial cleanliness and environmental improvement as proposed by the SAFE strategy [6]. Further investigation of these two, and their surrounding, communities is warranted to determine whether or not this higher TF prevalence is limited to these two communities [4]. However, as the TF prevalence was <5% at both regional and district levels, these communities are likely “the tail of the decline” [4]. The 10 communities with 5–10% TF prevalence are recommended to receive facial cleanliness and environmental improvement interventions, and in the remaining 48 communities, TF control is not currently a priority [4]. In this setting, sub-district community level decisions regarding MDA are required to ensure that trachoma elimination goals are achieved [4].

Furthermore, continued monitoring and surveillance are required in this setting, as re-emergence of ocular C. trachomatis infection and active trachoma has been documented in The Gambia following cessation of MDA [24]. Additionally, the Casamance region borders Guinea Bissau to the south, where TF prevalence in 1–9 year olds was estimated to be ≥20% in some districts. Though Guinea Bissau has now completed three rounds of MDA in most regions and is currently conducting impact surveys, this remains a potential concern. As a result of this risk of re-emergence, Neglected Tropical Disease (NTD) Programmes should regularly monitor districts with previous disease to ensure that it does not re-emerge as a significant public health problem [5]. National and regional surveillance systems should be employed to achieve this and should consider both active and passive surveillance for TF and TT case-finding [5, 25].

The low TF prevalence in the Casamance region was unexpected since no specific trachoma control efforts have been implemented there, unlike in other regions of Senegal or the neighbouring countries of The Gambia and Mali [12, 13]. The natural disappearance of trachoma without trachoma-specific intervention has been described elsewhere in Nepal and in one village in The Gambia [26, 27]. These findings are thought to be associated with the alleviation of poverty and improvements in sanitation, water supply, education and health care [27]. Senegal’s Human Development Index (HDI) improved from 0.367 in 1990, to 0.380 in 2000, and to 0.456 in 2010. This pattern is similar to that for The Gambia, whose HDI value increased from 0.330 in 1990, to 0.384 in 2000, to 0.441 in 2010 [28]. Thus, it is possible that a TF prevalence decrease due to secular trend, i.e. in the absence of trachoma control programmes, may have occurred. This explanation is supported by the high TT prevalence, which may represent the clinical sequelae from a previously higher burden of TF.

A component part of the HDI measure is educational attainment, and low household head educational attainment has been associated with TF in some countries such as Tanzania [20], but not in The Gambia [20, 22]. The household head education levels in our study were similar to those recorded in The Gambia [22], with 54.2% having attended school and two-thirds finishing with primary-level education. Thus, improvements in educational attainment are required in this region before achieving the Millennium Development Goal of universal primary education [29].

The risk factor questionnaire enquired about ethnicity, as the Casamance region population is distinct from other Senegalese regions, with the predominant ethnic group being Diola (82.4% in our study). Nationally, 44% of the population is of Wolof ethnicity, compared with 5% of Diola ethnicity. There are no reported ethnic group associations with trachoma in Senegal, and as the prevalences of TF and TT were too low to conduct formal risk factor analyses in our study, it was not possible for us to explore any associations in our population. Further investigations to assess whether ethnicity is related to health outcomes could nonetheless be warranted, as ethnicity has been associated with health outcomes (such as child mortality [30]) in this region.

The environmental risk factor data provide evidence of good water and sanitation levels in the Casamance region, and may also help explain the low prevalence of TF we observed. The proportion of children with unclean faces (dirt on the face (5.4%), ocular discharge (2.4%), nasal discharge (14.7%), flies on the face at the time of examination (0.3%)) was less than that found by Faye et al. in a Trachoma Rapid Assessment conducted in Senegal’s Kaolack region, where 12.5% of children aged 2–5 years had dirty faces and 4.6% had flies on their faces [17]. Latrine access was also higher in our study at 88.4% (compared to 60.9%), and 90.4% of respondents in our study reported that the time to fetch water was <30 min, whereas the water source was <25 m away for only 21.3% of those in Faye et al.’s study [17]. Environmental factors such as latrine and water access and use have been associated with active trachoma [31]. Latrines likely lead to reduced fly-eye contact, ultimately hindering transmission [32] – the high levels of latrine access in our study may explain the low proportion of children with flies observed on their faces. Access to water has been associated with reduced active trachoma, so long as it is used for hygiene purposes [33]. However, as our questionnaire was designed to be simple and quick in order to increase participation and completion, whilst enabling us to assess basic environmental conditions, we did not support the responses with observations of latrine use or measurements of water use practices, meaning we are unable to verify the responses given.

In striking contrast to the low TF prevalence, TT prevalence was high and far exceeded the WHO target for elimination as a public health problem of 0.2% (2 cases per 1000 adults aged ≥15 years) at both the regional and district levels [4, 5]. We found TT to be more prevalent in females than in males (1.8% versus 0.8%), with females having 2.3 times the odds of having TT than males. This association, which has been reported by others and reviewed with a meta-analysis showing a 1.8-fold higher risk of TT in females than males globally [34], is probably because women are the predominant caregivers and are in closer contact with children [35, 36]. However, other explanations such as females suffering higher loads of infection, being more prone to persistent infection, and/or being more biologically susceptible to consequences of C. trachomatis infection, may also play a role [35].

The natural history of trachoma posits that TS leads to TT [2], and there are several non-trachomatous causes of trichiasis, including inflammation, genetic defects and traumas [5, 37]. Although TT was significantly associated with having TS, with only 6/39 (15.4%) of individuals with TT also having TS recorded, our reported TT prevalence could be an over-estimate and could in fact be as low as 0.2% (15.4% of 1.4%). However, there is poor inter- and intra-observer agreement of TS grading, and consequently it is has not been included in the Global Trachoma Mapping Project methodology [38]. As the graders who conducted this survey were trained and assessed with a focus on TF and TT identification, we have decided to attribute the trichiasis cases recorded to a trachomatous aetiology. However, further work in this region to investigate whether the trichiasis is in fact due to trachoma, or other causes, is warranted. Notably, recent trachoma surveillance recommendations are that “the presence of scar, or the inability to evert the lid due to lid tightness, should be taken to indicate that the trichiasis is TT” in order to avoid misdiagnosis of TT [5].

The WHO recommends that all individuals with TT should be offered surgery, and that surgery should be prioritised where the prevalence is ≥0.1%. Based on the regional population size of 232,427, our census data indicating that 55.9% of the population is aged ≥15 years, and a TT prevalence of 1.4%, there are an estimated 1819 TT surgeries to conduct. Guidelines for TT management are provided by the WHO [1, 25]. One strategy is active TT case-hunting and surgery camps, as done in The Gambia, with surgeries recorded in a central, electronic TT registry to enable consistent data collection from across the region and ensuring appropriate follow-up care of all cases identified [12].

Limitations of the study are that there was not sufficient statistical power to conduct a risk factor analysis for TF due to the low prevalence, and that the sample size target of 2732 children aged 1–9 years was not achieved, with only 1432 children examined. Strengths of the study include providing the first data on TF and TT prevalence in this region, obtaining environmental data within which to contextualise the prevalence data, and capacity building within the region by having successfully trained 40 individuals from the region through a mixture of workshops and field exercises.

The prevalence of TF in 1–9 year olds in the region and its districts was below the WHO 5% threshold for elimination, indicating that trachoma control for TF is not a priority in this setting. However, adequate monitoring and surveillance of TF at sub-district level will be required to ensure that elimination targets are sustained and that TF does not re-emerge as a public health problem. TT surgery remains the priority for trachoma elimination efforts in the region. The prevalence of TT far exceeds the 0.2% WHO threshold in adults aged ≥15 years for elimination of trachoma as a public health problem, with surgery needing to be prioritised urgently to meet the WHO elimination targets.