Progress on elimination of lymphatic filariasis in Sierra Leone

Progress on elimination of lymphatic filariasis in Sierra Leone Background: A baseline survey in 2007–2008 found lymphatic filariasis (LF) to be endemic in Sierra Leone in all 14 districts and co-endemic with onchocerciasis in 12 districts. Mass drug administration (MDA) with ivermectin started in 2006 for onchocerciasis and was modified to add albendazole in 2008 to include LF treatment. In 2011, after three effective MDAs, a significant reduction in microfilaraemia (mf) prevalence and density was reported at the midterm assessment. After five MDAs, in 2013, mf prevalence and density were again measured as part of a pre-transmission assessment survey (pre-TAS) conducted per WHO guidelines. Methods: For the pre-TAS survey, districts were paired to represent populations of one million for impact assessment. One sentinel site selected from baseline and one spot check site purposefully selected based upon local knowledge of patients with LF were surveyed per pair (two districts). At each site, 300 people over five years of age provided mid- night blood samples and mf prevalence and density were determined using thick blood film microscopy. Results are compared with baseline and midterm data. Results: At pre-TAS the overall mf prevalence was 0.54% (95% CI: 0.36–0.81%), compared to 0.30% (95% CI: 0.19–0.47) at midterm and 2.6% (95% CI: 2.3–3.0%) at baseline. There was a higher, but non-significant, mf prevalence among males vs females. Eight districts (four pairs) had a prevalence of mf < 1% at all sites. Two pairs (four districts) had a prevalence of mf > 1% at one of the two sites: Koinadugu 0.98% (95% CI: 0.34–2.85%) and Bombali 2.67% (95% CI: 1.41–5. 00%), and Kailahun 1.56% (95% CI: 0.72–3.36%) and Kenema 0% (95% CI: 0.00–1.21%). Conclusions: Compared to baseline, there was a significant reduction of LF mf prevalence and density in the 12 districts co-endemic for LF and onchocerciasis after five annual LF MDAs. No statistically significant difference was seen in either measure compared to midterm. Eight of the 12 districts qualified for TAS. The other four districts that failed to qualify for TAS had historically high LF baseline prevalence and density and had regular cross-border movement of populations. These four districts needed to conduct two additional rounds of LF MDA before repeating the pre-TAS. The results showed that Sierra Leone continued to make progress towards the elimination of LF as a public health problem. Keywords: Lymphatic filariasis, Wuchereria bancrofti, Neglected tropical disease, Mass drug administration, Pre-transmission assessment survey, Sierra leone * Correspondence: yzhang@hki.org Helen Keller International, Regional Office for Africa, Dakar, Senegal Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Koroma et al. Parasites & Vectors (2018) 11:334 Page 2 of 10 Background piloted in the same year by adding albendazole to the Lymphatic filariasis (LF) is a vector-borne disease caused community-directed treatment with ivermectin (CDTI) by one of three filarial parasite species, Wuchereria platform in six districts. This was expanded in 2008 by the bancrofti, Brugia malayi and Brugia timori [1], and it is NTDP to all 12 co-endemic districts reaching all targeted transmitted by mosquitoes, mainly the Anopheles mos- communities [15]. MDA results reported by the NTDP quitoes in West Africa [2, 3]. LF causes physical and between 2008 and 2010 indicated good community emotional suffering from the disabling and disfiguring compliance: epidemiological coverage (i.e. proportion of lesions (such as hydrocoele, lymphoedema, lymphangitis people ingesting the LF medicines during treatment and elephantiasis) and economic loss due to diminished among the total population of the endemic communi- productivity and incapacitation, and affects mainly poor ties and districts) was above 65%, programme coverage countries and marginalised people [4–6]. The World (i.e. proportion of people ingesting the LF medicines Health Organization (WHO) estimates 120 million during treatment among the eligible people in the en- people globally are affected, with an estimated 40 million demic communities and districts) was above 80%, and the having clinically significant manifestations and the dis- geographical coverage (i.e. proportion of communities and ease was identified as the second most common cause of districts that were actually treated among the total num- long-term disability [7, 8]. ber of endemic communities and districts) was maintained In 1993 the International Task Force on Disease at 100% [15]. In 2011, a midterm impact assessment was Eradication identified LF as one of six diseases that conducted after three annual rounds of MDA in these 12 could be eradicated globally based on available diagnos- districts, and the results suggested progress was on track tic tools and strategies. The World Health Assembly to achieve LF elimination objectives in Sierra Leone [15]. passed resolution WHA 50.29 in 1997 calling for LF In 2013, a pre-transmission assessment survey (pre-TAS) elimination as a public health problem globally by the was conducted in the 12 districts that had received at least year 2020. Subsequently, the WHO launched the Global five effective rounds of LF MDA. This paper presents the Programme to Eliminate LF (GPELF) in 2000 to support pre-TAS survey results, in comparison with the baseline endemic countries and a Global Alliance for the Elimin- and midterm data and discusses whether the criteria for ation of LF (GAELF) was established [9]. The two princi- conducting a transmission assessment survey (TAS) for pal objectives are an interruption of LF transmission and stopping LF MDA had been met in districts. alleviation/prevention of LF-related disability and suffer- ing [9, 10]. According to the WHO recommendation, Methods the main strategy is annual mass drug administration Mass drug administration (MDA) of albendazole (400 mg) together with diethyl- Integrated annual onchocerciasis/LF MDA with iver- carbamazine (6 mg/kg) or ivermectin (200 μg/kg) to mectin plus albendazole was implemented from 2008 to those known at-risk populations eligible within endemic 2013 in all 12 co-endemic districts. MDA was areas [8–10]. Annual MDA with a minimum treatment district-wide covering all villages, towns and district coverage of 65% in the total at-risk population for at headquarter towns. Within villages, community drug least five years is required to achieve the objective distributors (CDDs) were literate members selected by (microfilaraemia prevalence to below 1%) [8–10]. In their communities and trained by district health workers 2015, among the 73 known LF endemic countries, 18 no to conduct MDA and report adverse events. The CDDs longer required MDA and were conducting post-MDA administered between 1 and 4 ivermectin tablets de- surveillance [1]. Togo was confirmed as the first African pending on the height of the person using a dose pole country to eliminate LF as a public health problem in while only one tablet of albendazole was administered to 2017 [11]. Globally, the estimate for people requiring LF each eligible person. District health workers supervised MDA has dropped from 1.41 billion in 2011 to 856.4 the CDDs with support from district health management million in 2016 [1]. teams (DHMT) and national NTDP staff. The CDTI In 2005, the Ministry of Health and Sanitation in Sierra plus albendazole strategy, which was based on volunteer Leone conducted nationwide LF mapping with support CDDs, could not work in the urban district headquarter from WHO and found that all 14 districts were endemic towns where people refused to accept medication from for LF while 12 rural districts (except Western Areas), volunteers without formal training. Therefore, students were co-endemic with onchocerciasis [12, 13]. The exist- in health and nursing institutions were trained to con- ing National Onchocerciasis Control Programme (NOCP) duct MDA in headquarter towns [16]. MDA was per- was expanded in 2007 to become the national integrated formed once a year between October and December. Neglected Tropical Disease Programme (NTDP) including Community registers used previously for onchocercia- LF, schistosomiasis and soil-transmitted helminthiasis sis MDA were modified to include albendazole and pro- [12, 14, 15]. An integrated LF/onchocerciasis MDA was vided to all targeted villages. The register captured all Koroma et al. Parasites & Vectors (2018) 11:334 Page 3 of 10 members of each community, including those eligible for through the preparation of thick blood film for micros- MDA and those not eligible. Before each MDA in rural copy was used [12, 15]. A fingertip blood sample (60 μl) communities (villages), CDDs conducted a pre-MDA cen- was collected from each participant between 22:00 h and sus and updated the community register. MDA details 02:00 h, smeared gently and uniformly in a circular were also captured in the registers. Simple tally sheets shape onto a slide and allowed to air dry at room were used in urban areas by health and nursing students temperature for 12–24 h. The next day, the dried smear for recording MDA data. Each level had a summary form was dehaemoglobinized through flooding with distilled for ease of reporting: CDDs and health/nursing students water for 3–5 min, air-dried again, fixed with methanol to the supervising staff of peripheral health unit (PHU), for 30–60 s, stained with GIEMSA for 10 min, and ex- PHUs to the DHMT, and DHMTs to the NTDP. amined for microfilariae (mf) under a light microscope by experienced technicians. Positive findings of mf were Survey site selection recorded, and individual density of infection was calcu- WHO guidelines were followed for each survey [17, 18]. lated and expressed as the number of mf per ml of At baseline (2007–2008), followingnationalmapping of blood. For quality control, all positive slides and 10% of LF using immunochromatographic test (ICT) cards, one the negative slides were preserved and examined later by site with the highest ICT prevalence in each district was an experienced researcher. selected as sentinel site (SS) and the baseline data on microfilariae (mf) were collected [12]. As the population Statistical analysis size in most districts was below 500,000, two districts were Data were recorded in Microsoft Excel and analysed in paired to represent a population close to one million de- SPSS (IBM, Version 23). Prevalence and density of mf pending on geographical proximity and epidemiological were calculated for all 12 districts and compared with the characteristics [12, 17, 18]. At midterm, SS and spot check midterm and baseline data previously published [12, 15]. sites (SCS) were selected and surveyed: one SS and one The 95% confidence intervals (CI) for prevalence were cal- SCS per pair of districts, as described previously [15]. culated using the Wilson score method without continuity During pre-TAS in the 12 rural districts, the same SSs as correction [19]. The arithmetic mean density of infection for midterm assessment were surveyed in Bo, Bonthe, with 95% CI was calculated for the total population exam- Kailahun, Koinadugu, Kono and Port Loko, together with ined and for positives-only. The Chi-square test was used different SCSs purposefully selected in Bombali, Kambia, to compare the differences in prevalence, and the Kenema, Moyamba, Pujehun and Tonkolili in consult- Kruskal-Wallis test was used to compare the differences ation with DHMTs and PHU staff from communities with in density. Differences in prevalence and density were high numbers of patients with hydrocoeles or lymph- considered significant when P <0.05 [12]. edema. The 2 districts in the Western Area did not imple- The total population used in rural areas was the total ment MDA until 2010 so were not eligible for pre-TAS in number of people recorded in community registers dur- 2013. In each of the pairs, an SS was selected in one dis- ing the pre-MDA census, while the total population used trict and an SCS in the other. Since Bombali was the only in urban areas was the figure projected from the 2004 district with greater than 1% mf prevalence at mid-term national census [20], with an annual growth rate of 2.5%. assessment after three effective rounds of MDA [15], two A point prevalence map showing geographical locations SCSs were selected in that district. of the survey sites and results was produced with ArcGIS software (ESRI, version 10.4) [12, 21]. Sampling and diagnosis In all surveys, convenience sampling was used at each site [12, 15]. Two-day training was conducted for all Results technicians before the study started to ensure standard- MDA results 2011–2012 isation of activities and data recording. Upon arrival in MDA results for 2008–2010 were published previously communities the survey teams first met with community [15], and are not shown in this paper, while MDA results leaders to obtain their approval, then meetings were held for 2011–2012 are shown in Table 1. In total, 14,253 vil- with the community to explain the study and its signifi- lages and urban areas were treated in the 12 districts cance. The coordinates of each study site were recorded each year in 2011–2012, which represents 100% geo- using hand-held global positioning system units. graphical coverage for endemic villages and urban areas. A minimum of 300 participants over five years of age Over four million people were targeted annually. Overall were required for pre-TAS [17], so if the sample sizes epidemiological coverage was 75.9% and 79.6% in 2011 could not be reached at the primary villages, the survey and 2012, respectively, and was over 65% in each district teams moved to neighbouring villages until the sample in each round. The overall programme coverage was sizes were met. Night blood survey methodology 94.9% and 93.6% in 2011 and 2012, respectively, and was Koroma et al. Parasites & Vectors (2018) 11:334 Page 4 of 10 Table 1 Lymphatic filariasis MDA results in 12 districts of Sierra Leone in 2011 and 2012. Geographical coverage of villages/urban areas was 100% in all 12 districts in 2011 and 2012 District 2011 2012 Population MDA Coverage (%) Population MDA Coverage (%) Eligable Total Treated Epidemiological Programme Eligable Total Treated Epidemiological Programme Bo 444,317 555,397 427,682 77.0 96.3 483,417 568,727 449,508 79.0 93.0 Bombali 390,424 488,030 366,980 75.2 94.0 424,781 499,743 399,794 80.0 94.1 Bonthe 118,597 148,246 112,424 75.8 94.8 128,703 151,416 120,640 79.7 93.7 Kailahun 343,508 429,386 335,567 78.2 97.7 373,737 439,691 349,889 79.6 93.6 Kambia 258,571 323,214 244,376 75.6 94.5 281,326 330,972 263,822 79.7 93.8 Kenema 488,245 610,307 463,162 75.9 94.9 531,550 625,354 501,280 80.2 94.3 Koinadugu 300,392 375,491 282,735 75.3 94.1 326,826 384,502 307,878 80.1 94.2 Kono 358,286 447,858 342,241 76.4 95.5 389,816 458,608 364,975 79.6 93.6 Moyamba 261,017 326,272 238,818 73.2 91.5 283,987 334,103 264,863 79.3 93.3 Port Loko 399,995 499,994 378,976 75.8 94.7 434,034 510,629 403,508 79.0 93.0 Pujehun 188,875 236,094 176,924 74.9 93.7 205,496 241,760 192,140 79.5 93.5 Tonkolili 341,039 426,299 325,639 76.4 95.5 370,702 436,121 345,643 79.3 93.2 Total 3,893,266 4,866,588 3,695,524 75.9 94.9 4,234,375 4,981,626 3,963,940 79.6 93.6 over 80% in each district in each round. Similar effective mf prevalence in two older age groups at midterm from MDA coverage was reported for 2008–2010 [15]. the baseline. At pre-TAS, while most districts showed continuous decrease from midterm in mf prevalence in Microfilaraemia prevalence all age groups, there was a rebound in mf prevalence in At pre-TAS a total of 4230 night blood samples were certain age groups in a number of districts, most evi- collected: males 2275 (53.8%), females 1955 (46.2%). The dently in the 15–30 years group in Bombali, Kailahun, pre-TAS results for each district are shown in Table 2 Koinadugu and Kono and in the > 30 years group in and compared to baseline and midterm by mf preva- Koinadugu which were all > 1%. lence, arithmetic mean mf density for persons tested positive only (AMD-positives) and arithmetic mean mf Microfilaraemia density density for all persons tested (AMD-all). At pre-TAS the overall AMD-all was 1.04 mf/ml (95% At pre-TAS the mf prevalence was 0.54% (95% CI: CI: 0.30–1.77 mf/ml) and overall AMD-positive was 0.36–0.81%), not significantly different from 0.3% at 137.12 mf/ml (95% CI: 88.80–185.44 mf/ml) as shown in midterm (χ = 3.741, df =1, P >0.05) but signifi- Table 2. For districts, AMD-all was below 1 mf/ml ex- cantly lower than 2.6% at the baseline, a decrease of cept Bombali, Kailahun and Koinadugu districts. There 79.2% (χ = 63.292, df =1, P < 0.0001). The mf prevalence was no statistically significant difference in mf density in in males 0.70% (95% CI: 0.43–1.14%) was almost twice that males vs females (H = 2.308, df =1, P > 0.05). in females 0.36% (95% CI: 0.17–0.74%), though the At pre-TAS, the overall AMD-all was not signifi- difference was not statistically significant (χ = 2.317, cantly higher than midterm (0.05 mf/ml) (H = 3.778, df =1, P > 0.05). Similarly, the mf prevalence by sex df =1, P > 0.05), but significantly lower than the had slightly increased from midterm (males 0.35%, χ =3.408, baseline (1.32 mf/ml), a reduction of 21.2% (H = 62.810, df =1, P > 0.05; females 0.25%, χ = 0.508, df =1, P >0.05) df =1, P < 0.0001). The overall AMD-positive (137.12 mf/ but decreased significantly from the baseline (males ml, 95% CI: 88.80–185.44) was significantly higher than 3.3%, χ = 42.579, df =1, P < 0.0001; females 2.0%, both midterm (17.59 mf/ml) (H = 16.625, df =1, χ = 24.165, df =1, P < 0.0001). P < 0.0001) and the baseline (50.90 mf/ml, 95% CI: 40.25– The trend of age prevalence in each district at base- 61.62) (H = 18.251, df =1, P < 0.0001). line, midterm and pre-TAS is shown in Fig. 1.The people tested at each survey point were divided into Eligibility of districts for conducting TAS three age groups: 5–14 years; 15–30 years; and > 30 Prevalence at both SS and SCS were below 1% in years. There were no baseline data for the 5–14 years Bo-Pujehun (0.3% and 0.3%, respectively), Bonthe-Moyamba age group as only people of 15 years and above were (0% and 0%, respectively), Kambia-Port Loko (0% and 0.3%, tested at baseline. All districts showed major decrease in respectively), and Kono-Tonkolili (0.6% and 0%, respectively) Koroma et al. Parasites & Vectors (2018) 11:334 Page 5 of 10 Table 2 Summary results of LF studies in 12 districts of Sierra Leone at baseline, midterm and pre-TAS Districts by Baseline survey 2007–2008 (95% CI) Midterm 2011 (95% CI) Pre-TAS 2013 (95% CI) Evaluation n mf Prev (%) AMD-all AMD-positive n mf Prev (%) AMD-all AMD-positive n mf Prev (%) AMD-all AMD-positive unit (mf/ml) (mf/ml) (mf/ml) (mf/ml) (mf/ml) (mf/ml) Overall 8233 2.6 (2.3–3.0) 1.32 (1.00–1.65) 50.90 (40.25–61.62) 6023 0.30 (0.19–0.47) 0.05 (0.03–0.08) 17.59 (15.64–19.55) 4230 0.54 (0.36–0.81) 1.04 (0.30–1.77) 137.12 (88.80–185.44) By Sex Male 3863 3.3 (2.8–3.9) 1.83 (1.21–2.44) 55.08 (39.00–71.15) 3170 0.35 (0.19–0.62) 0.06 (0.03–0.10) 18.18 (14.80–21.56) 2275 0.70 (0.43–1.14) 1.36 (0.08–2.64) 115.56 (60.68–170.43) Female 4370 2.0 (1.6–2.4) 0.88 (0.59–1.18) 44.76 (32.89–56.64) 2853 0.25 (0.12–0.51) 0.04 (0.01–0.07) 16.67 (-) 1955 0.36 (0.17–0.74) 0.66 (0.08–1.23) 183.33 (70.06–296.60) By district and sites 1 Bo 1005 2.0 (1.3–3.1) 1.97 (0.84–3.11) 99.17 (58.32–140.01) 500 0 (0–0.76) –– 350 0.29 (0.05–1.60) 0.29 (0.00–0.85) 100 (-) Pujehun 624 0 (0–0.6) –– 500 0 (0–0.76) –– 305 0.33 (0.06–1.83) 0.11 (0.00–0.32) 33.33 (-) 2 Bonthe 504 1.2 (0.6–2.6) 0.83 (0.02–1.63) 69.44 (13.68–125.21) 499 0.20 (0.04–1.13) 0.03 (0–0.10) 16.67 (-) 309 0 (0–1.23) –– Moyamba 500 1 (0.4–2.3) 0.67 (0–1.36) 66.67 (6.33–127.00) 500 0 (0–0.76) –– 330 0 (0.00–1.15) –– 3 Kambia 619 2.1 (1.2–3.6) 0.97 (0.23–1.71) 46.15 (17.04–75.27) 500 0.40 (0.11–1.45) 0.07 (0–0.16) 16.67 (-) 300 0 (0–1.26) –– Port Loko 500 4.4 (2.9–6.6) 3.53 (1.48–5.59) 80.30 (44.49–116.12) 499 0.20 (0.04–1.13) 0.03 (0–0.10) 16.67 (-) 357 0.28 (0.05–1.57) 0.56 (0.00–1.66) 200 (-) 4 Kono 875 2.4 (1.6–3.6) 1.11 (0.37–1.84) 46.03 (20.09–71.97) 499 0 (0–0.76) 0 0 320 0.63 (0.17–2.25) 0.89 (0.00–2.44) 141.67 (0.00–1518.17) Tonkolili 500 2.4 (1.4–4.2) 0.63 (0.24–1.03) 26.39 (17.99–34.79) 523 0.19 (0.03–1.08) 0.03 (0–0.10) 16.67 (-) 316 0 (0–1.20) –– 5 Bombali 2 –– – – –– – – 303 0 (0–1.25) –– Bombali 1 830 6.9 (5.3–8.8) 1.93 (1.28–2.57) 28.07 (21.70–34.44) 506 1.58 (0.80–3.09) 0.26 (0.08–0.45) 16.67 (-) 337 2.67 (1.41–5.00) 8.21 (0.00–16.93) 175.00 (57.95–292.05) Koinadugu 636 5.7 (4.1–7.7) 1.99 (0.95–3.04) 35.19 (19.83–50.54) 498 0.80 (0.31–2.05) 0.17 (0–0.34) 20.83 (7.57– 34.09) 305 0.98 (0.34–2.85) 1.15 (0.00–2.51) 116.67 (7.13–226.21) 6 Kailahun 624 2.6 (1.6–4.1) 2.08 (0.00–4.89) 81.25 (0.00–195.58) 499 0.20 (0.04–1.13) 0.03 (0–0.10) 16.67 (-) 385 1.56 (0.72–3.36) 1.69 (0.00–3.46) 108.33 (2.37–214.29) Kenema 1016 0.6 (0.3–1.3) 0.34 (0.00–0.70) 58.33 (4.42–112.24) 500 0 (0–0.76) –– 313 0 (0–1.21) –– Koroma et al. Parasites & Vectors (2018) 11:334 Page 6 of 10 Fig. 1 Age mf prevalence curve at baseline, midterm and pre-TAS in each district as shown in Fig. 2 and Table 2. These eight districts, control, as reported in some other countries [28, 29]. In therefore, qualified for conducting TAS to confirm Sierra Leone, ivermectin was used pre-conflict in limited whether LF MDA could be stopped. However, in space in the country [30], but large scale use through Bombali-Koinadugu districts, the prevalence at three CDTI did not start until 1995 as the Special Intervention sites was 0%, 2.7% and 1% and in Kailahun-Kenema it Zone of the African Programme of Onchocerciasis Con- was 1.6% and 0% at two sites. These four districts, trol, in meso- and hyper-endemic villages [13]. However, therefore, failed to meet the criteria for conducting due to the civil conflict between 1991–2002, CDTI did TAS and MDA had to continue for at least two add- not achieve satisfactory treatment coverage until 2005 itional rounds. and was expanded to accommodate district-wide LF MDA by adding albendazole in 2007–2008 [13]. There- Discussion fore, the prior ivermectin use in the 12 dsitricts may Our results showed that the criteria for initiating TAS have contributed to the reduction of LF prevalence. were achieved in eight of twelve districts after five effect- It was observed that mf prevalence and overall mf ive rounds of MDA. Mf prevalence declined significantly density had dropped significantly at the midterm survey from 2007–2008 to 2011 and sustained those gains be- compared to baseline [15] and then increased slightly at tween 2011 and 2013. This indicates that the NTDP pre-TAS. This observation could be due to the conveni- continued to make progress towards LF elimination ence sampling strategy that relies on volunteering, and since integrated onchocerciasis/LF MDA using ivermec- so different sets of the population might have been tin/albendazole was piloted in 2007. Many similar stud- tested. In addition, the highest mf prevalence was re- ies have been conducted in Kenya, Egypt and Cameroon corded at the purposefully selected SCSs, and particular that have shown a similar significant reduction in LF care had been taken to identify probable hotspots at prevalence and density after five to eight years of LF pre-TAS [31, 32]. MDA [22–25]. The results in Sierra Leone were also in Although not statistically significant, almost twice as line with the expectations of the GPELF [9, 10]. How- many males were tested mf positive as females. This ever, four districts still had mf prevalence of over 1% and may be explained by transmission dynamics as males failed to qualify for conducting TAS. may be more active and exposed to mosquito bites in Prior to MDA, the endemicity of LF in Sierra Leone the local context, especially since the launch of universal was one of the highest in Africa [26]. In the early 1990s, bednet coverage targetting women and children [33]. It surveys showed 34.8% mf prevalence in three villages of has also been suggested that females may be more resist- Moyamba district [27]. However, in 2007–2008, the ant to LF infection due to hormonal activity [33]. At pre-MDA mf prevalence for the 12 districts ranged from pre-TAS it was observed that prevalence and density 0 to 6.9% [12]. This significant reduction may have been were highest in more active age groups (15–30 years). partly due to the use of ivermectin for onchocerciasis This may have been due to the continued transmission Koroma et al. Parasites & Vectors (2018) 11:334 Page 7 of 10 Fig. 2 Geographical locations and point mf prevalence of each survey site and district categories for TAS qualification. Paired districts sharing sentinel sites and spot check sites are shown in same colours. Numeral figures at survey sites are point percentage MF prevalence for each site in those districts that failed to qualify for TAS and mos- than five annual MDAs while more than six annual quito biting rates are higher in these more active age MDAs may be needed for implementation units with a groups [33]. On the other hand, it had been observed high baseline prevalence [23, 25, 34, 35]. The marked re- that older adolescents and young adults were the most duction in prevalence and density in most of the districts non-compliant to MDA in urban settings in Sierra after five rounds may have been partly due to the rela- Leone. It may be that these groups were most concerned tively low baseline prevalence [12]. Recent scale-up of about their reproductive health (females unsure about insecticidal-treated bed nets (ITNs) and long-lasting in- whether or not they were pregnant at the time of MDA) secticidal nets (LLINs) distribution and use, and indoor and long-term fertility status, and they may be less aware residual spraying (IRS) for malaria in Sierra Leone may of the disease-risks than the older age groups who may have also benefited the LF results shown in this paper. have seen cases of lymphoedema and hydroceles fre- Over six million ITNs were distributed nationwide in quently as they were growing up. The results highlighted the past five years in Sierra Leone [36–38], and the per- the need of improved measures to reach the 15–30 years centage of households owning mosquito nets increased group in the future MDA in those districts that failed to from 40% in 2008 to 65% in 2013 [38]. IRS was also con- qualify for conducting TAS. ducted in selected chiefdoms (sub-district) of four dis- The number of MDA rounds needed to eliminate LF tricts: Bo, Bombali, Kono and Rural Western District depends on baseline infection levels, vectoral capacity, [38]. The benefit of use of ITNs, LLINs and IRS on LF the efficacy of the MDA regimen used (ivermectin plus elimination has been reported in different countries albendazole), and community adherence with MDA [3, 39–41]. On the other hand, the pre-TAS failure in [23, 25, 34, 35]. Elimination of LF is achievable in some Bombali and Koinadugu may be explained by the rela- implementation units with low baseline infection in less tively high baseline prevalence and density in the Koroma et al. Parasites & Vectors (2018) 11:334 Page 8 of 10 districts. It is also suggested that the pre-TAS failures positives-only; APOC: African Programme for Onchocerciasis Control; CDD: Community-directed drug distributor; CDTI: Community-directed may have been partly due to cross-border transmission treatment with ivermectin; CI: Confidence interval; CNTD: Centre for Neglected of LF as all four districts that failed are located along the Tropical Diseases; DHMT: District Health Management Team; GAELF: Global border (Bombali, Koinadugu and Kailahun with Guinea; Alliance for the Elimination of LF; GPELF: Global Programme to Eliminate LF; FTS: Filariasis test strip; ICT: Immunochromatographic test; IRS: Indoor residual and Kailahun and Kenema with Liberia) [42–44]. Both spraying; ITN: Insecticidal treated nets; LF: Lymphatic filariasis; LLIN: Long-lasting Guinea and Liberia had not yet succeeded in reaching insecticidal nets; MDA: Mass drug administration; MF: Microfilaraemia; 100% geographical coverage for LF MDA and high mf: Microfilariae; MOHS: Ministry of Health and Sanitation; NBS: Night blood survey; NOCP: National Onchocerciasis Control Programme; NTDP: Neglected prevalence rates were recorded in neighbouring Liberia Tropical Disease Programme; PHU: Peripheral health unit; Pre-TAS: Pre- prior to the 1980s [45, 46]. A similar problem of transmission assessment survey; SCS: Spot check site; SS: Sentinel site; cross-border transmission of LF through migration be- TAS: Transmission assessment survey; TBF: Thick blood film; USAID: United States Agency for International Development; WHO: World Health Organisation tween Thailand (far advanced with LF elimination) and Myanmar (in its early stages of LF elimination) has been Acknowledgements highlighted in several publications [43, 47, 48]. Kailahun The NTDP has received most of its funding from the USAID through its had a similar baseline mf prevalence to four other dis- former NTD Control Programme managed by RTI International and the current End in Africa Project managed by FHI 360, and technical support tricts that passed the pre-TAS but had remarkably differ- through Helen Keller International. Additional funding has been received ent challenges with cross-border migration with both from WHO and Sightsavers. The authors wish to thank the WHO for providing Guinea and Liberia. technical support to the NTDP and the survey team leaders: A Tia, S Saffa and F Sahr for the quality control. Thanks also go to the district health team and There are several possible limitations of the study. community participants for their collaboration. Districts were paired to meet the WHO recommenda- tion of having one SS and one SCS per one million Funding population: one district had an SS while the other had The baseline mapping surveys were funded by the WHO, and all subsequent an SCS. This led to fewer sites surveyed per implemen- impact assessments were funded by the USAID through its NTD Control Programme managed by RTI International and currently the End in Africa tation unit (district) as recommended. The results ap- Project managed by FHI 360. The contents are the responsibility of the plied to and affected the decision for two districts authors and do not necessarily reflect the views of USAID or the United (implementation units). In the case of Kenema district, States Government. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. although the mf prevalence was below 1% threshold at the site in the district, it could not be considered as hav- Availability of data and materials ing passed the pre-TAS because there was only one site All data generated or analysed during this study are either included in this within Kenema and the mf prevalence was above the 1% published article or are available from the corresponding author and can be made available with permission from the MOHS Sierra Leone. threshold in the other district of the pair. Furthermore, the districts were paired based on proximity and topo- Authors’ contributions graphic features, but may not be as similar in relation to JBK (2005–2009) and SS (2009–2014) are former NOCP/NTDP programme transmission dynamics. This district pairing strategy managers and designed and coordinated the studies and initial reports. AC, should be reconsidered, and each district should be sur- JP, MB and MS led the field work and data collection. JBK drafted the manuscript. JBK and YZ conducted the data analysis. YZ produced the point prevalence map. veyed separately as an implementation unit in the future. MH and YZ revised the manuscript. All authors read and approved the final Another limitation is that it was impossible to compare manuscript. baseline data for the ages 5–14 years because this age group was not studied at baseline per previous WHO Ethics approval and consent to participate guidelines [17, 18]. This pre-TAS was part of the monitoring and evaluation activities of the national LF elimination programme and was conducted by the NTDP of the MOHS Sierra Leone per WHO recommendations. Ethical approval for the Conclusions survey was obtained from the MOHS Research and Ethics Committee. There was a significant reduction of LF mf prevalence Informed oral consent was first obtained from village chiefs and then from each participant before samples were collected and their acceptance was and density after five annual LF MDAs across the 12 recorded on a form by the leader of the survey team, as literacy rates are rural districts in Sierra Leone that are co-endemic with low in the country. For participants under 15 years, consent was obtained onchocerciasis. Eight of 12 districts passed the pre-TAS from their parents. All participants were eligible for inclusion without discrimination on gender, social status, religion or ethnicity. Participants’ identities were with < 1% prevalence and qualified for a TAS. The other protected by collecting, recording and analysing data such that participants four districts that failed to qualify for TAS will need to remained anonymous. conduct two additional rounds of MDA before repeating the pre-TAS. These promising results for LF were pos- Consent for publication Although consent was obtained from participants before the study, data sible because of good community adherence to treat- collection was conducted such that participants remained anonymous during ment during MDA campaigns. data entry and analysis. No individual’s identity can be revealed upon publication. Abbreviations AFRO: WHO Regional Office for Africa; AMD-all: Arithmetic mean MF density Competing interests for entire population studied; AMD-positive: Arithmetic mean MF density for The authors declare that they have no competing interests. Koroma et al. Parasites & Vectors (2018) 11:334 Page 9 of 10 Publisher’sNote 21. Zoure HG, Wanji S, Noma M, Amazigo UV, Diggle PJ, Tekle AH, et al. The Springer Nature remains neutral with regard to jurisdictional claims in published geographic distribution of Loa loa in Africa: results of large-scale maps and institutional affiliations. implementation of the Rapid Assessment Procedure for Loiasis (RAPLOA). PLoS Negl Trop Dis. 2011;5:e1210. Author details 22. Ramzy RM, El Setouhy M, Helmy H, Ahmed ES, Abd Elaziz KM, Farid HA, et Family Health International 360, Ghana Country Office, Accra, Ghana. al. Effect of yearly mass drug administration with diethylcarbamazine and National Neglected Tropical Disease Control Programme, Ministry of Health albendazole on bancroftian filariasis in Egypt: a comprehensive assessment. and Sanitation, Freetown, Sierra Leone. Helen Keller International, Freetown, Lancet. 2006;367:992–9. Sierra Leone. Helen Keller International, Regional Office for Africa, Dakar, 23. 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Progress on elimination of lymphatic filariasis in Sierra Leone

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Biomedicine; Parasitology; Entomology; Tropical Medicine; Infectious Diseases; Veterinary Medicine/Veterinary Science; Virology
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Abstract

Background: A baseline survey in 2007–2008 found lymphatic filariasis (LF) to be endemic in Sierra Leone in all 14 districts and co-endemic with onchocerciasis in 12 districts. Mass drug administration (MDA) with ivermectin started in 2006 for onchocerciasis and was modified to add albendazole in 2008 to include LF treatment. In 2011, after three effective MDAs, a significant reduction in microfilaraemia (mf) prevalence and density was reported at the midterm assessment. After five MDAs, in 2013, mf prevalence and density were again measured as part of a pre-transmission assessment survey (pre-TAS) conducted per WHO guidelines. Methods: For the pre-TAS survey, districts were paired to represent populations of one million for impact assessment. One sentinel site selected from baseline and one spot check site purposefully selected based upon local knowledge of patients with LF were surveyed per pair (two districts). At each site, 300 people over five years of age provided mid- night blood samples and mf prevalence and density were determined using thick blood film microscopy. Results are compared with baseline and midterm data. Results: At pre-TAS the overall mf prevalence was 0.54% (95% CI: 0.36–0.81%), compared to 0.30% (95% CI: 0.19–0.47) at midterm and 2.6% (95% CI: 2.3–3.0%) at baseline. There was a higher, but non-significant, mf prevalence among males vs females. Eight districts (four pairs) had a prevalence of mf < 1% at all sites. Two pairs (four districts) had a prevalence of mf > 1% at one of the two sites: Koinadugu 0.98% (95% CI: 0.34–2.85%) and Bombali 2.67% (95% CI: 1.41–5. 00%), and Kailahun 1.56% (95% CI: 0.72–3.36%) and Kenema 0% (95% CI: 0.00–1.21%). Conclusions: Compared to baseline, there was a significant reduction of LF mf prevalence and density in the 12 districts co-endemic for LF and onchocerciasis after five annual LF MDAs. No statistically significant difference was seen in either measure compared to midterm. Eight of the 12 districts qualified for TAS. The other four districts that failed to qualify for TAS had historically high LF baseline prevalence and density and had regular cross-border movement of populations. These four districts needed to conduct two additional rounds of LF MDA before repeating the pre-TAS. The results showed that Sierra Leone continued to make progress towards the elimination of LF as a public health problem. Keywords: Lymphatic filariasis, Wuchereria bancrofti, Neglected tropical disease, Mass drug administration, Pre-transmission assessment survey, Sierra leone * Correspondence: yzhang@hki.org Helen Keller International, Regional Office for Africa, Dakar, Senegal Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Koroma et al. Parasites & Vectors (2018) 11:334 Page 2 of 10 Background piloted in the same year by adding albendazole to the Lymphatic filariasis (LF) is a vector-borne disease caused community-directed treatment with ivermectin (CDTI) by one of three filarial parasite species, Wuchereria platform in six districts. This was expanded in 2008 by the bancrofti, Brugia malayi and Brugia timori [1], and it is NTDP to all 12 co-endemic districts reaching all targeted transmitted by mosquitoes, mainly the Anopheles mos- communities [15]. MDA results reported by the NTDP quitoes in West Africa [2, 3]. LF causes physical and between 2008 and 2010 indicated good community emotional suffering from the disabling and disfiguring compliance: epidemiological coverage (i.e. proportion of lesions (such as hydrocoele, lymphoedema, lymphangitis people ingesting the LF medicines during treatment and elephantiasis) and economic loss due to diminished among the total population of the endemic communi- productivity and incapacitation, and affects mainly poor ties and districts) was above 65%, programme coverage countries and marginalised people [4–6]. The World (i.e. proportion of people ingesting the LF medicines Health Organization (WHO) estimates 120 million during treatment among the eligible people in the en- people globally are affected, with an estimated 40 million demic communities and districts) was above 80%, and the having clinically significant manifestations and the dis- geographical coverage (i.e. proportion of communities and ease was identified as the second most common cause of districts that were actually treated among the total num- long-term disability [7, 8]. ber of endemic communities and districts) was maintained In 1993 the International Task Force on Disease at 100% [15]. In 2011, a midterm impact assessment was Eradication identified LF as one of six diseases that conducted after three annual rounds of MDA in these 12 could be eradicated globally based on available diagnos- districts, and the results suggested progress was on track tic tools and strategies. The World Health Assembly to achieve LF elimination objectives in Sierra Leone [15]. passed resolution WHA 50.29 in 1997 calling for LF In 2013, a pre-transmission assessment survey (pre-TAS) elimination as a public health problem globally by the was conducted in the 12 districts that had received at least year 2020. Subsequently, the WHO launched the Global five effective rounds of LF MDA. This paper presents the Programme to Eliminate LF (GPELF) in 2000 to support pre-TAS survey results, in comparison with the baseline endemic countries and a Global Alliance for the Elimin- and midterm data and discusses whether the criteria for ation of LF (GAELF) was established [9]. The two princi- conducting a transmission assessment survey (TAS) for pal objectives are an interruption of LF transmission and stopping LF MDA had been met in districts. alleviation/prevention of LF-related disability and suffer- ing [9, 10]. According to the WHO recommendation, Methods the main strategy is annual mass drug administration Mass drug administration (MDA) of albendazole (400 mg) together with diethyl- Integrated annual onchocerciasis/LF MDA with iver- carbamazine (6 mg/kg) or ivermectin (200 μg/kg) to mectin plus albendazole was implemented from 2008 to those known at-risk populations eligible within endemic 2013 in all 12 co-endemic districts. MDA was areas [8–10]. Annual MDA with a minimum treatment district-wide covering all villages, towns and district coverage of 65% in the total at-risk population for at headquarter towns. Within villages, community drug least five years is required to achieve the objective distributors (CDDs) were literate members selected by (microfilaraemia prevalence to below 1%) [8–10]. In their communities and trained by district health workers 2015, among the 73 known LF endemic countries, 18 no to conduct MDA and report adverse events. The CDDs longer required MDA and were conducting post-MDA administered between 1 and 4 ivermectin tablets de- surveillance [1]. Togo was confirmed as the first African pending on the height of the person using a dose pole country to eliminate LF as a public health problem in while only one tablet of albendazole was administered to 2017 [11]. Globally, the estimate for people requiring LF each eligible person. District health workers supervised MDA has dropped from 1.41 billion in 2011 to 856.4 the CDDs with support from district health management million in 2016 [1]. teams (DHMT) and national NTDP staff. The CDTI In 2005, the Ministry of Health and Sanitation in Sierra plus albendazole strategy, which was based on volunteer Leone conducted nationwide LF mapping with support CDDs, could not work in the urban district headquarter from WHO and found that all 14 districts were endemic towns where people refused to accept medication from for LF while 12 rural districts (except Western Areas), volunteers without formal training. Therefore, students were co-endemic with onchocerciasis [12, 13]. The exist- in health and nursing institutions were trained to con- ing National Onchocerciasis Control Programme (NOCP) duct MDA in headquarter towns [16]. MDA was per- was expanded in 2007 to become the national integrated formed once a year between October and December. Neglected Tropical Disease Programme (NTDP) including Community registers used previously for onchocercia- LF, schistosomiasis and soil-transmitted helminthiasis sis MDA were modified to include albendazole and pro- [12, 14, 15]. An integrated LF/onchocerciasis MDA was vided to all targeted villages. The register captured all Koroma et al. Parasites & Vectors (2018) 11:334 Page 3 of 10 members of each community, including those eligible for through the preparation of thick blood film for micros- MDA and those not eligible. Before each MDA in rural copy was used [12, 15]. A fingertip blood sample (60 μl) communities (villages), CDDs conducted a pre-MDA cen- was collected from each participant between 22:00 h and sus and updated the community register. MDA details 02:00 h, smeared gently and uniformly in a circular were also captured in the registers. Simple tally sheets shape onto a slide and allowed to air dry at room were used in urban areas by health and nursing students temperature for 12–24 h. The next day, the dried smear for recording MDA data. Each level had a summary form was dehaemoglobinized through flooding with distilled for ease of reporting: CDDs and health/nursing students water for 3–5 min, air-dried again, fixed with methanol to the supervising staff of peripheral health unit (PHU), for 30–60 s, stained with GIEMSA for 10 min, and ex- PHUs to the DHMT, and DHMTs to the NTDP. amined for microfilariae (mf) under a light microscope by experienced technicians. Positive findings of mf were Survey site selection recorded, and individual density of infection was calcu- WHO guidelines were followed for each survey [17, 18]. lated and expressed as the number of mf per ml of At baseline (2007–2008), followingnationalmapping of blood. For quality control, all positive slides and 10% of LF using immunochromatographic test (ICT) cards, one the negative slides were preserved and examined later by site with the highest ICT prevalence in each district was an experienced researcher. selected as sentinel site (SS) and the baseline data on microfilariae (mf) were collected [12]. As the population Statistical analysis size in most districts was below 500,000, two districts were Data were recorded in Microsoft Excel and analysed in paired to represent a population close to one million de- SPSS (IBM, Version 23). Prevalence and density of mf pending on geographical proximity and epidemiological were calculated for all 12 districts and compared with the characteristics [12, 17, 18]. At midterm, SS and spot check midterm and baseline data previously published [12, 15]. sites (SCS) were selected and surveyed: one SS and one The 95% confidence intervals (CI) for prevalence were cal- SCS per pair of districts, as described previously [15]. culated using the Wilson score method without continuity During pre-TAS in the 12 rural districts, the same SSs as correction [19]. The arithmetic mean density of infection for midterm assessment were surveyed in Bo, Bonthe, with 95% CI was calculated for the total population exam- Kailahun, Koinadugu, Kono and Port Loko, together with ined and for positives-only. The Chi-square test was used different SCSs purposefully selected in Bombali, Kambia, to compare the differences in prevalence, and the Kenema, Moyamba, Pujehun and Tonkolili in consult- Kruskal-Wallis test was used to compare the differences ation with DHMTs and PHU staff from communities with in density. Differences in prevalence and density were high numbers of patients with hydrocoeles or lymph- considered significant when P <0.05 [12]. edema. The 2 districts in the Western Area did not imple- The total population used in rural areas was the total ment MDA until 2010 so were not eligible for pre-TAS in number of people recorded in community registers dur- 2013. In each of the pairs, an SS was selected in one dis- ing the pre-MDA census, while the total population used trict and an SCS in the other. Since Bombali was the only in urban areas was the figure projected from the 2004 district with greater than 1% mf prevalence at mid-term national census [20], with an annual growth rate of 2.5%. assessment after three effective rounds of MDA [15], two A point prevalence map showing geographical locations SCSs were selected in that district. of the survey sites and results was produced with ArcGIS software (ESRI, version 10.4) [12, 21]. Sampling and diagnosis In all surveys, convenience sampling was used at each site [12, 15]. Two-day training was conducted for all Results technicians before the study started to ensure standard- MDA results 2011–2012 isation of activities and data recording. Upon arrival in MDA results for 2008–2010 were published previously communities the survey teams first met with community [15], and are not shown in this paper, while MDA results leaders to obtain their approval, then meetings were held for 2011–2012 are shown in Table 1. In total, 14,253 vil- with the community to explain the study and its signifi- lages and urban areas were treated in the 12 districts cance. The coordinates of each study site were recorded each year in 2011–2012, which represents 100% geo- using hand-held global positioning system units. graphical coverage for endemic villages and urban areas. A minimum of 300 participants over five years of age Over four million people were targeted annually. Overall were required for pre-TAS [17], so if the sample sizes epidemiological coverage was 75.9% and 79.6% in 2011 could not be reached at the primary villages, the survey and 2012, respectively, and was over 65% in each district teams moved to neighbouring villages until the sample in each round. The overall programme coverage was sizes were met. Night blood survey methodology 94.9% and 93.6% in 2011 and 2012, respectively, and was Koroma et al. Parasites & Vectors (2018) 11:334 Page 4 of 10 Table 1 Lymphatic filariasis MDA results in 12 districts of Sierra Leone in 2011 and 2012. Geographical coverage of villages/urban areas was 100% in all 12 districts in 2011 and 2012 District 2011 2012 Population MDA Coverage (%) Population MDA Coverage (%) Eligable Total Treated Epidemiological Programme Eligable Total Treated Epidemiological Programme Bo 444,317 555,397 427,682 77.0 96.3 483,417 568,727 449,508 79.0 93.0 Bombali 390,424 488,030 366,980 75.2 94.0 424,781 499,743 399,794 80.0 94.1 Bonthe 118,597 148,246 112,424 75.8 94.8 128,703 151,416 120,640 79.7 93.7 Kailahun 343,508 429,386 335,567 78.2 97.7 373,737 439,691 349,889 79.6 93.6 Kambia 258,571 323,214 244,376 75.6 94.5 281,326 330,972 263,822 79.7 93.8 Kenema 488,245 610,307 463,162 75.9 94.9 531,550 625,354 501,280 80.2 94.3 Koinadugu 300,392 375,491 282,735 75.3 94.1 326,826 384,502 307,878 80.1 94.2 Kono 358,286 447,858 342,241 76.4 95.5 389,816 458,608 364,975 79.6 93.6 Moyamba 261,017 326,272 238,818 73.2 91.5 283,987 334,103 264,863 79.3 93.3 Port Loko 399,995 499,994 378,976 75.8 94.7 434,034 510,629 403,508 79.0 93.0 Pujehun 188,875 236,094 176,924 74.9 93.7 205,496 241,760 192,140 79.5 93.5 Tonkolili 341,039 426,299 325,639 76.4 95.5 370,702 436,121 345,643 79.3 93.2 Total 3,893,266 4,866,588 3,695,524 75.9 94.9 4,234,375 4,981,626 3,963,940 79.6 93.6 over 80% in each district in each round. Similar effective mf prevalence in two older age groups at midterm from MDA coverage was reported for 2008–2010 [15]. the baseline. At pre-TAS, while most districts showed continuous decrease from midterm in mf prevalence in Microfilaraemia prevalence all age groups, there was a rebound in mf prevalence in At pre-TAS a total of 4230 night blood samples were certain age groups in a number of districts, most evi- collected: males 2275 (53.8%), females 1955 (46.2%). The dently in the 15–30 years group in Bombali, Kailahun, pre-TAS results for each district are shown in Table 2 Koinadugu and Kono and in the > 30 years group in and compared to baseline and midterm by mf preva- Koinadugu which were all > 1%. lence, arithmetic mean mf density for persons tested positive only (AMD-positives) and arithmetic mean mf Microfilaraemia density density for all persons tested (AMD-all). At pre-TAS the overall AMD-all was 1.04 mf/ml (95% At pre-TAS the mf prevalence was 0.54% (95% CI: CI: 0.30–1.77 mf/ml) and overall AMD-positive was 0.36–0.81%), not significantly different from 0.3% at 137.12 mf/ml (95% CI: 88.80–185.44 mf/ml) as shown in midterm (χ = 3.741, df =1, P >0.05) but signifi- Table 2. For districts, AMD-all was below 1 mf/ml ex- cantly lower than 2.6% at the baseline, a decrease of cept Bombali, Kailahun and Koinadugu districts. There 79.2% (χ = 63.292, df =1, P < 0.0001). The mf prevalence was no statistically significant difference in mf density in in males 0.70% (95% CI: 0.43–1.14%) was almost twice that males vs females (H = 2.308, df =1, P > 0.05). in females 0.36% (95% CI: 0.17–0.74%), though the At pre-TAS, the overall AMD-all was not signifi- difference was not statistically significant (χ = 2.317, cantly higher than midterm (0.05 mf/ml) (H = 3.778, df =1, P > 0.05). Similarly, the mf prevalence by sex df =1, P > 0.05), but significantly lower than the had slightly increased from midterm (males 0.35%, χ =3.408, baseline (1.32 mf/ml), a reduction of 21.2% (H = 62.810, df =1, P > 0.05; females 0.25%, χ = 0.508, df =1, P >0.05) df =1, P < 0.0001). The overall AMD-positive (137.12 mf/ but decreased significantly from the baseline (males ml, 95% CI: 88.80–185.44) was significantly higher than 3.3%, χ = 42.579, df =1, P < 0.0001; females 2.0%, both midterm (17.59 mf/ml) (H = 16.625, df =1, χ = 24.165, df =1, P < 0.0001). P < 0.0001) and the baseline (50.90 mf/ml, 95% CI: 40.25– The trend of age prevalence in each district at base- 61.62) (H = 18.251, df =1, P < 0.0001). line, midterm and pre-TAS is shown in Fig. 1.The people tested at each survey point were divided into Eligibility of districts for conducting TAS three age groups: 5–14 years; 15–30 years; and > 30 Prevalence at both SS and SCS were below 1% in years. There were no baseline data for the 5–14 years Bo-Pujehun (0.3% and 0.3%, respectively), Bonthe-Moyamba age group as only people of 15 years and above were (0% and 0%, respectively), Kambia-Port Loko (0% and 0.3%, tested at baseline. All districts showed major decrease in respectively), and Kono-Tonkolili (0.6% and 0%, respectively) Koroma et al. Parasites & Vectors (2018) 11:334 Page 5 of 10 Table 2 Summary results of LF studies in 12 districts of Sierra Leone at baseline, midterm and pre-TAS Districts by Baseline survey 2007–2008 (95% CI) Midterm 2011 (95% CI) Pre-TAS 2013 (95% CI) Evaluation n mf Prev (%) AMD-all AMD-positive n mf Prev (%) AMD-all AMD-positive n mf Prev (%) AMD-all AMD-positive unit (mf/ml) (mf/ml) (mf/ml) (mf/ml) (mf/ml) (mf/ml) Overall 8233 2.6 (2.3–3.0) 1.32 (1.00–1.65) 50.90 (40.25–61.62) 6023 0.30 (0.19–0.47) 0.05 (0.03–0.08) 17.59 (15.64–19.55) 4230 0.54 (0.36–0.81) 1.04 (0.30–1.77) 137.12 (88.80–185.44) By Sex Male 3863 3.3 (2.8–3.9) 1.83 (1.21–2.44) 55.08 (39.00–71.15) 3170 0.35 (0.19–0.62) 0.06 (0.03–0.10) 18.18 (14.80–21.56) 2275 0.70 (0.43–1.14) 1.36 (0.08–2.64) 115.56 (60.68–170.43) Female 4370 2.0 (1.6–2.4) 0.88 (0.59–1.18) 44.76 (32.89–56.64) 2853 0.25 (0.12–0.51) 0.04 (0.01–0.07) 16.67 (-) 1955 0.36 (0.17–0.74) 0.66 (0.08–1.23) 183.33 (70.06–296.60) By district and sites 1 Bo 1005 2.0 (1.3–3.1) 1.97 (0.84–3.11) 99.17 (58.32–140.01) 500 0 (0–0.76) –– 350 0.29 (0.05–1.60) 0.29 (0.00–0.85) 100 (-) Pujehun 624 0 (0–0.6) –– 500 0 (0–0.76) –– 305 0.33 (0.06–1.83) 0.11 (0.00–0.32) 33.33 (-) 2 Bonthe 504 1.2 (0.6–2.6) 0.83 (0.02–1.63) 69.44 (13.68–125.21) 499 0.20 (0.04–1.13) 0.03 (0–0.10) 16.67 (-) 309 0 (0–1.23) –– Moyamba 500 1 (0.4–2.3) 0.67 (0–1.36) 66.67 (6.33–127.00) 500 0 (0–0.76) –– 330 0 (0.00–1.15) –– 3 Kambia 619 2.1 (1.2–3.6) 0.97 (0.23–1.71) 46.15 (17.04–75.27) 500 0.40 (0.11–1.45) 0.07 (0–0.16) 16.67 (-) 300 0 (0–1.26) –– Port Loko 500 4.4 (2.9–6.6) 3.53 (1.48–5.59) 80.30 (44.49–116.12) 499 0.20 (0.04–1.13) 0.03 (0–0.10) 16.67 (-) 357 0.28 (0.05–1.57) 0.56 (0.00–1.66) 200 (-) 4 Kono 875 2.4 (1.6–3.6) 1.11 (0.37–1.84) 46.03 (20.09–71.97) 499 0 (0–0.76) 0 0 320 0.63 (0.17–2.25) 0.89 (0.00–2.44) 141.67 (0.00–1518.17) Tonkolili 500 2.4 (1.4–4.2) 0.63 (0.24–1.03) 26.39 (17.99–34.79) 523 0.19 (0.03–1.08) 0.03 (0–0.10) 16.67 (-) 316 0 (0–1.20) –– 5 Bombali 2 –– – – –– – – 303 0 (0–1.25) –– Bombali 1 830 6.9 (5.3–8.8) 1.93 (1.28–2.57) 28.07 (21.70–34.44) 506 1.58 (0.80–3.09) 0.26 (0.08–0.45) 16.67 (-) 337 2.67 (1.41–5.00) 8.21 (0.00–16.93) 175.00 (57.95–292.05) Koinadugu 636 5.7 (4.1–7.7) 1.99 (0.95–3.04) 35.19 (19.83–50.54) 498 0.80 (0.31–2.05) 0.17 (0–0.34) 20.83 (7.57– 34.09) 305 0.98 (0.34–2.85) 1.15 (0.00–2.51) 116.67 (7.13–226.21) 6 Kailahun 624 2.6 (1.6–4.1) 2.08 (0.00–4.89) 81.25 (0.00–195.58) 499 0.20 (0.04–1.13) 0.03 (0–0.10) 16.67 (-) 385 1.56 (0.72–3.36) 1.69 (0.00–3.46) 108.33 (2.37–214.29) Kenema 1016 0.6 (0.3–1.3) 0.34 (0.00–0.70) 58.33 (4.42–112.24) 500 0 (0–0.76) –– 313 0 (0–1.21) –– Koroma et al. Parasites & Vectors (2018) 11:334 Page 6 of 10 Fig. 1 Age mf prevalence curve at baseline, midterm and pre-TAS in each district as shown in Fig. 2 and Table 2. These eight districts, control, as reported in some other countries [28, 29]. In therefore, qualified for conducting TAS to confirm Sierra Leone, ivermectin was used pre-conflict in limited whether LF MDA could be stopped. However, in space in the country [30], but large scale use through Bombali-Koinadugu districts, the prevalence at three CDTI did not start until 1995 as the Special Intervention sites was 0%, 2.7% and 1% and in Kailahun-Kenema it Zone of the African Programme of Onchocerciasis Con- was 1.6% and 0% at two sites. These four districts, trol, in meso- and hyper-endemic villages [13]. However, therefore, failed to meet the criteria for conducting due to the civil conflict between 1991–2002, CDTI did TAS and MDA had to continue for at least two add- not achieve satisfactory treatment coverage until 2005 itional rounds. and was expanded to accommodate district-wide LF MDA by adding albendazole in 2007–2008 [13]. There- Discussion fore, the prior ivermectin use in the 12 dsitricts may Our results showed that the criteria for initiating TAS have contributed to the reduction of LF prevalence. were achieved in eight of twelve districts after five effect- It was observed that mf prevalence and overall mf ive rounds of MDA. Mf prevalence declined significantly density had dropped significantly at the midterm survey from 2007–2008 to 2011 and sustained those gains be- compared to baseline [15] and then increased slightly at tween 2011 and 2013. This indicates that the NTDP pre-TAS. This observation could be due to the conveni- continued to make progress towards LF elimination ence sampling strategy that relies on volunteering, and since integrated onchocerciasis/LF MDA using ivermec- so different sets of the population might have been tin/albendazole was piloted in 2007. Many similar stud- tested. In addition, the highest mf prevalence was re- ies have been conducted in Kenya, Egypt and Cameroon corded at the purposefully selected SCSs, and particular that have shown a similar significant reduction in LF care had been taken to identify probable hotspots at prevalence and density after five to eight years of LF pre-TAS [31, 32]. MDA [22–25]. The results in Sierra Leone were also in Although not statistically significant, almost twice as line with the expectations of the GPELF [9, 10]. How- many males were tested mf positive as females. This ever, four districts still had mf prevalence of over 1% and may be explained by transmission dynamics as males failed to qualify for conducting TAS. may be more active and exposed to mosquito bites in Prior to MDA, the endemicity of LF in Sierra Leone the local context, especially since the launch of universal was one of the highest in Africa [26]. In the early 1990s, bednet coverage targetting women and children [33]. It surveys showed 34.8% mf prevalence in three villages of has also been suggested that females may be more resist- Moyamba district [27]. However, in 2007–2008, the ant to LF infection due to hormonal activity [33]. At pre-MDA mf prevalence for the 12 districts ranged from pre-TAS it was observed that prevalence and density 0 to 6.9% [12]. This significant reduction may have been were highest in more active age groups (15–30 years). partly due to the use of ivermectin for onchocerciasis This may have been due to the continued transmission Koroma et al. Parasites & Vectors (2018) 11:334 Page 7 of 10 Fig. 2 Geographical locations and point mf prevalence of each survey site and district categories for TAS qualification. Paired districts sharing sentinel sites and spot check sites are shown in same colours. Numeral figures at survey sites are point percentage MF prevalence for each site in those districts that failed to qualify for TAS and mos- than five annual MDAs while more than six annual quito biting rates are higher in these more active age MDAs may be needed for implementation units with a groups [33]. On the other hand, it had been observed high baseline prevalence [23, 25, 34, 35]. The marked re- that older adolescents and young adults were the most duction in prevalence and density in most of the districts non-compliant to MDA in urban settings in Sierra after five rounds may have been partly due to the rela- Leone. It may be that these groups were most concerned tively low baseline prevalence [12]. Recent scale-up of about their reproductive health (females unsure about insecticidal-treated bed nets (ITNs) and long-lasting in- whether or not they were pregnant at the time of MDA) secticidal nets (LLINs) distribution and use, and indoor and long-term fertility status, and they may be less aware residual spraying (IRS) for malaria in Sierra Leone may of the disease-risks than the older age groups who may have also benefited the LF results shown in this paper. have seen cases of lymphoedema and hydroceles fre- Over six million ITNs were distributed nationwide in quently as they were growing up. The results highlighted the past five years in Sierra Leone [36–38], and the per- the need of improved measures to reach the 15–30 years centage of households owning mosquito nets increased group in the future MDA in those districts that failed to from 40% in 2008 to 65% in 2013 [38]. IRS was also con- qualify for conducting TAS. ducted in selected chiefdoms (sub-district) of four dis- The number of MDA rounds needed to eliminate LF tricts: Bo, Bombali, Kono and Rural Western District depends on baseline infection levels, vectoral capacity, [38]. The benefit of use of ITNs, LLINs and IRS on LF the efficacy of the MDA regimen used (ivermectin plus elimination has been reported in different countries albendazole), and community adherence with MDA [3, 39–41]. On the other hand, the pre-TAS failure in [23, 25, 34, 35]. Elimination of LF is achievable in some Bombali and Koinadugu may be explained by the rela- implementation units with low baseline infection in less tively high baseline prevalence and density in the Koroma et al. Parasites & Vectors (2018) 11:334 Page 8 of 10 districts. It is also suggested that the pre-TAS failures positives-only; APOC: African Programme for Onchocerciasis Control; CDD: Community-directed drug distributor; CDTI: Community-directed may have been partly due to cross-border transmission treatment with ivermectin; CI: Confidence interval; CNTD: Centre for Neglected of LF as all four districts that failed are located along the Tropical Diseases; DHMT: District Health Management Team; GAELF: Global border (Bombali, Koinadugu and Kailahun with Guinea; Alliance for the Elimination of LF; GPELF: Global Programme to Eliminate LF; FTS: Filariasis test strip; ICT: Immunochromatographic test; IRS: Indoor residual and Kailahun and Kenema with Liberia) [42–44]. Both spraying; ITN: Insecticidal treated nets; LF: Lymphatic filariasis; LLIN: Long-lasting Guinea and Liberia had not yet succeeded in reaching insecticidal nets; MDA: Mass drug administration; MF: Microfilaraemia; 100% geographical coverage for LF MDA and high mf: Microfilariae; MOHS: Ministry of Health and Sanitation; NBS: Night blood survey; NOCP: National Onchocerciasis Control Programme; NTDP: Neglected prevalence rates were recorded in neighbouring Liberia Tropical Disease Programme; PHU: Peripheral health unit; Pre-TAS: Pre- prior to the 1980s [45, 46]. A similar problem of transmission assessment survey; SCS: Spot check site; SS: Sentinel site; cross-border transmission of LF through migration be- TAS: Transmission assessment survey; TBF: Thick blood film; USAID: United States Agency for International Development; WHO: World Health Organisation tween Thailand (far advanced with LF elimination) and Myanmar (in its early stages of LF elimination) has been Acknowledgements highlighted in several publications [43, 47, 48]. Kailahun The NTDP has received most of its funding from the USAID through its had a similar baseline mf prevalence to four other dis- former NTD Control Programme managed by RTI International and the current End in Africa Project managed by FHI 360, and technical support tricts that passed the pre-TAS but had remarkably differ- through Helen Keller International. Additional funding has been received ent challenges with cross-border migration with both from WHO and Sightsavers. The authors wish to thank the WHO for providing Guinea and Liberia. technical support to the NTDP and the survey team leaders: A Tia, S Saffa and F Sahr for the quality control. Thanks also go to the district health team and There are several possible limitations of the study. community participants for their collaboration. Districts were paired to meet the WHO recommenda- tion of having one SS and one SCS per one million Funding population: one district had an SS while the other had The baseline mapping surveys were funded by the WHO, and all subsequent an SCS. This led to fewer sites surveyed per implemen- impact assessments were funded by the USAID through its NTD Control Programme managed by RTI International and currently the End in Africa tation unit (district) as recommended. The results ap- Project managed by FHI 360. The contents are the responsibility of the plied to and affected the decision for two districts authors and do not necessarily reflect the views of USAID or the United (implementation units). In the case of Kenema district, States Government. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. although the mf prevalence was below 1% threshold at the site in the district, it could not be considered as hav- Availability of data and materials ing passed the pre-TAS because there was only one site All data generated or analysed during this study are either included in this within Kenema and the mf prevalence was above the 1% published article or are available from the corresponding author and can be made available with permission from the MOHS Sierra Leone. threshold in the other district of the pair. Furthermore, the districts were paired based on proximity and topo- Authors’ contributions graphic features, but may not be as similar in relation to JBK (2005–2009) and SS (2009–2014) are former NOCP/NTDP programme transmission dynamics. This district pairing strategy managers and designed and coordinated the studies and initial reports. AC, should be reconsidered, and each district should be sur- JP, MB and MS led the field work and data collection. JBK drafted the manuscript. JBK and YZ conducted the data analysis. YZ produced the point prevalence map. veyed separately as an implementation unit in the future. MH and YZ revised the manuscript. All authors read and approved the final Another limitation is that it was impossible to compare manuscript. baseline data for the ages 5–14 years because this age group was not studied at baseline per previous WHO Ethics approval and consent to participate guidelines [17, 18]. This pre-TAS was part of the monitoring and evaluation activities of the national LF elimination programme and was conducted by the NTDP of the MOHS Sierra Leone per WHO recommendations. Ethical approval for the Conclusions survey was obtained from the MOHS Research and Ethics Committee. There was a significant reduction of LF mf prevalence Informed oral consent was first obtained from village chiefs and then from each participant before samples were collected and their acceptance was and density after five annual LF MDAs across the 12 recorded on a form by the leader of the survey team, as literacy rates are rural districts in Sierra Leone that are co-endemic with low in the country. For participants under 15 years, consent was obtained onchocerciasis. Eight of 12 districts passed the pre-TAS from their parents. All participants were eligible for inclusion without discrimination on gender, social status, religion or ethnicity. Participants’ identities were with < 1% prevalence and qualified for a TAS. The other protected by collecting, recording and analysing data such that participants four districts that failed to qualify for TAS will need to remained anonymous. conduct two additional rounds of MDA before repeating the pre-TAS. These promising results for LF were pos- Consent for publication Although consent was obtained from participants before the study, data sible because of good community adherence to treat- collection was conducted such that participants remained anonymous during ment during MDA campaigns. data entry and analysis. No individual’s identity can be revealed upon publication. Abbreviations AFRO: WHO Regional Office for Africa; AMD-all: Arithmetic mean MF density Competing interests for entire population studied; AMD-positive: Arithmetic mean MF density for The authors declare that they have no competing interests. Koroma et al. 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Parasites & VectorsSpringer Journals

Published: Jun 4, 2018

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