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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2023 Aug 21;378(1887):20220280. doi: 10.1098/rstb.2022.0280

Lymphatic filariases and soil-transmitted helminthiases in Sri Lanka: the challenge of eliminating residual pockets of transmission

Nilmini T G A Chandrasena 1,, I E Gunaratna 4, Dileepa Ediriweera 2, N R de Silva 3
PMCID: PMC10440162  PMID: 37598710

Abstract

Sri Lanka has successfully met the challenge of controlling both lymphatic filariasis (LF) and soil-transmitted helminthiases (STH) as public health problems. The primary public health strategy for combatting both conditions has been preventive chemotherapy. The national programme for the elimination of LF implemented five annual rounds of mass chemotherapy in the endemic districts from 2002 to 2006 using a combination of diethylcarbamazine and albendazole. The overall microfilaria rate declined from 0.21% in 2001 before the mass chemotherapy, to 0.06% in 2016, at declaration of elimination of LF as a public health problem by the World Health Organization. Currently Sri Lanka is in the phase of post-validation surveillance. Achieving control of STH has been more difficult. Mass deworming programmes have been implemented for nearly a century, and national-level surveys reported prevalence rates declining from 6.9% in 2003 to 1% in 2017. However, neither of these infections has been completely eliminated. A situation analysis indicates continued transmission of both among high-risk communities. This paper explores the reasons for persistence of transmission of both LF and STH in residual pockets and the measures that are required to achieve long-term control, or perhaps even interrupt transmission in Sri Lanka.

This article is part of the theme issue ‘Challenges and opportunities in the fight against neglected tropical diseases: a decade from the London Declaration on NTDs’.

Keywords: lymphatic filariasis, soil-transmitted helminthiasis, control strategies, elimination as a public health problem, interruption of transmission

1. Introduction

Lying just 6° north of the Equator, with a lush, tropical climate and two monsoon seasons each year, Sri Lanka (known as Ceylon until 1972) has been, for centuries, highly endemic for many parasitic infections, including lymphatic filariasis (LF) and soil-transmitted helminthiasis (STH) [1,2]. Invading armies and suitable environmental conditions led to the establishment of an endemic zone of Bancroftian filariasis in the southwestern coastal areas with, scattered foci of Brugian filariasis in other parts of the country [3]. Hookworm was first identified in the late ninteenth century and an island-wide survey conducted in the 1920s found over 90% of the general population to be infected with it [2].

Diverse control strategies have been used by the health authorities since the first half of the twentieth century. Early LF control measures adopted by the Anti-Filariasis Campaign (AFC), established in 1947 by the Ministry of Health, focused mainly on control of the mosquito vectors, Culex quinquefasciatus and Mansonia species. Destruction of larval host plants in swamp habitats successfully eliminated Brugian filariasis by the late 1960s, but Bancroftian filariasis remained persistent in three of the country's nine provinces, at varying levels of endemicity [3,4].

In 2002, the AFC changed its control strategy, to align itself with the WHO's Global Programme to Eliminate Lymphatic Filariasis [5]. Sri Lanka's national programme for elimination of LF implemented five rounds of mass drug administration (MDA) annually from 2002 to 2006 in the three endemic provinces (Northwestern, Western and Southern), with a population of 10.7 million as of 2002, using the two-drug combination of diethylcarbamazine and albendazole (DA). Three further rounds of mop-up MDA were administered from 2014 to 2016 in foci with persistent transmission [6]. Access to specialized treatment and health education for patients with lymphoedema was provided free of charge by the network of filaria clinics distributed in the endemic areas. In 2016, Sri Lanka became one of the first countries to be declared to have eliminated LF as a public health problem in the Southeast Asian region [7]. The microfilaria (MF) prevalence rates have declined from 0.21% prior to launch of the MDA programme to 0.03% at present [8].

Similarly, the public health impact of STH infections (i.e. ascariasis, trichuriasis and hookworm infections caused by Necator americanus, but not Ancylostoma duodenale) was well recognized and extensive mass deworming programmes were first conducted in the 1930s [9]. Although a dedicated, vertical-control programme like the AFC was not established for STH control, deworming programmes for school children and antenatal mothers were implemented through the Family Health Bureau, the Health Ministry arm responsible for delivery of maternal and child health services. These specific programmes, combined with gradual improvements in housing and sanitation, as well as in general health literacy, resulted in a slow but steady downward drift in prevalence of STH. A national survey of non-high-risk groups among schoolchildren found a national prevalence of 6.9% in 2003, and in 2017 the national level prevalence of STH was estimated to be approximately 1%.

Although LF and STH infections are no longer considered as public health problems in Sri Lanka, they have not been eliminated completely either. This paper provides a situation analysis of their current epidemiology, an overview of present control strategies together with monitoring and surveillance measures, and an assessment of the way forward for long-term interruption of transmission i.e. true national elimination of LF and STH.

2. Situation analysis

(a) . Post-validation surveillance for lymphatic filariasis

Although ongoing surveillance during the post-validation phase is stipulated as a WHO requirement, there is minimal technical guidance from WHO on how this should be done.

In Sri Lanka, the principal objective of post-validation surveillance (PVS) has been to detect, map and treat residual infections (MF carriers) in the population and reduce the reservoir of infection and thereby the risk of transmission, and prevent recrudescence and re-establishment of infection. This has three arms: entomological, parasitological and disease surveillance.

Entomological surveillance is routinely conducted by field and laboratory staff under the supervision of regional medical officers for filariasis control, for both C. quinquefasciatus and Mansonia species. Adult mosquitoes are collected through indoor hand collections, gravid traps or cattle-baited net traps. All collected mosquitoes are either dissected or subjected to polymerase chain reaction (PCR) to identify mosquito positivity for parasite larval stages L1, L2 and L3. Findings from mosquito dissections are used to calculate infected and infective mosquito rates. PCR findings are used to calculate pool positive rates. These entomological surveillance data are used by the national programme to prioritize communities for MF surveys to detect and treat MF carriers but not for vector control.

The detection of filarial larvae of any stage in mosquitoes indicates the presence of residual infection (MF carriers) among the human population. The prevalence of L3 infective larvae in vector mosquitoes is a sensitive indicator of ongoing transmission, especially during the PVS period, when very low microfilaria counts may evade detection by blood smear examination [10].

Entomological surveillance is focused mainly in previously endemic districts and to a lesser extent in nonendemic districts. Infected mosquitoes carrying larval parasitic stages (L1, L2 and L3 larvae) have been detected in six of the eight endemic districts during the period 2016–2020 as well as in three non-endemic districts. However, in 2021, infective mosquitoes carrying L3 filarial larvae were detected only in the three endemic districts of Kalutara, Galle and Matara (figure 1a,b) [11].

Figure 1.

Figure 1.

(a) Infected rate of Culex mosquitoes in the eight endemic districts, 2016–2021. Source: AFC Health Bulletin 2016–2021. (b) Infective rate of Culex mosquitoes in the eight endemic districts, 2016–2021. Source: AFC Health Bulletin 2016–2021.

Parasitological surveillance in the endemic districts is usually initiated on the basis of findings in vector surveys. The main diagnostic method used for parasitological surveillance is the thick night blood smear. The MF rate and MF density are used as monitoring indicators of ongoing transmission. Immigrants from endemic countries are screened using rapid antigen test kits at visa renewal or through special work-site night blood surveys.

The AFC has documented cases of both indigenous and imported Bancroftian filariasis during PVS as public health problems [11]. Human infections have been diagnosed mostly within districts that were formerly recognized for their high endemicity [12]. A declining trend in MF rate and MF densities was noted among the indigenous MF-positives while the imported MF-positives had higher densities, reflecting their higher transmission potential and infectivity [11]. Infection parameters for Bancroftian filariasis (MF and circulating filaria antigen (CFA) rates) were found to be significantly higher among adult males, who represented the bulk (>80%) of residual infections [13,14]. A combination of factors such as higher exposure to infective mosquitoes, higher susceptibility to infection and lower compliance with MDA have been suggested as reasons for adult male preponderance [14].

District-wise, MF prevalence rates have remained well below the recommended 1% threshold in all districts, with a steady decline from 2016 to 2020. The highest has been 0.3%, recorded in Galle district in 2016, declining to 0.03 in 2020 [11]. Surveillance activities were temporarily interrupted in 2020 owing to the COVID-19 pandemic and resumed in the latter part of 2021 in a more targeted manner. Slightly higher MF rates were recorded in 2021, in the districts of Galle (0.05), Matara (0.04) and Kurunegala (0.01), perhaps owing to the targeted nature of the surveys.

(i) . Disease surveillance

A total of 22 filaria clinics cater to the 11.6 million residents in the three endemic provinces as of 2021. The clinic registries document an average of 600–700 new lymphoedema cases per year accessing morbidity management services in endemic areas during the PVS, with the majority presenting with early-stage disease (26 and 56% in stages 1 and 2) [11].

Thus, multiple indicators may be used to detect ongoing residual transmission in an area. These include infection parameters such as MF rate, CFA rate, and filaria antibody rate among children born after the MDA, and entomological parameters such as vector infection and infective rates and vector pool positivity rate for filarial DNA.

(b) . Residual lymphatic filariasis infections

The geographical distribution of LF is highly focal. Epidemiological models suggest that, with multiple rounds of preventive chemotherapy, the distribution may become even more heterogeneous [12]. Pockets of persistent transmission were detected in cross-community surveys conducted 6 years after cessation of MDA in 2006, when several subdistrict health administrative units in the district of Galle had MF and CFA rates that exceeded the stipulated end-point criteria for elimination. Filaria antibody rates in school children and filaria DNA in mosquitoes also exceeded the end-point criteria in many of these pockets [13]. Having detected antibodies among children who were not exposed to MDA during their lifetime is a sensitive indicator for ongoing transmission. These southern foci of residual transmission were covered by annual mop-up MDAs with DA from 2014 to 2016. Surveys were repeated in several sentinel sites 2–3 years later, after WHO validation in 2016. They provided evidence of improved infection parameters in some regions without any interventions while, in other areas in the south, infection levels exceeded the thresholds despite supplementary MDAs [12,14].

Subsequent surveys conducted by the AFC in 2019–2021 continue to provide evidence of residual transmission, mainly along the western and southern coastal border. These residual cases of Bancroftian filariasis are mostly aggregated along the southwestern coastal border, with most cases in the districts of Galle and Matara in the Southern Province, and to a lesser extent in Colombo in the Western Province (see electronic supplementary material, figure S1).

The annual MF rates have been consistently below 0.5% (WHO-recommended threshold is less than 1%) in all endemic districts during the 6 years of PVS. In a few small subdistrict health administrative units situated in the past high endemic regions, the MF rates exceeded 0.5% (conservative threshold) but rarely exceeded the 1% threshold. These data suggest negligible transmission of Bancroftian filariasis in most areas except for a few high-risk hotspots. In such hotspots, considerable amounts of residual transmission may persist, and the trends of these residual infections is difficult to predict.

The reasons for persistence of transmission after multiple rounds of PC (preventive chemotherapy) are multifactorial. Diethylcarbamazine and albendazole suppress microfilaraemia, but do not kill the adult worms which may recover from sterility with cessation of PC [15]. Moreover, the coastal towns in the districts of Galle and Matara, where persistent transmission is mostly seen, were highly endemic in the past [16]. These high-baseline prevalence rates often require longer cycles of MDA [1719].

Furthermore, considerably more than the anticipated 4–6 rounds of MDA may be required if programme coverage is sub-optimal (less than 65% PC coverage) [20] and in favourable transmission conditions [21]. Low compliance rates were documented in a few focal areas within the district of Colombo with persistent transmission [22,23]. The environmental variables (climatic and physiographical) in the southwest coastal region are highly favourable for transmission of Bancroftian filariasis. The physiographical factors in the densely populated coastal towns (Colombo, Galle and Matara) with poor infrastructure for drainage and sanitation, and industrial activities (coconut coir industry), contribute to high vector densities. The favourable climatic variables expedite parasite maturation and enhance vector longevity, thus providing ideal conditions for continued transmission of LF.

Sporadic cases of Brugian filariasis have been detected in all three endemic provinces during the post-MDA period and during PVS [24], but a general pattern of coastal clustering with higher occurrence of cases in the Puttalam and Kalutara districts is evident (see electronic supplementary material, figure S1). The enhanced surveillance that occurred during the post-MDA period and which continues during PVS have probably led to detection of the re-emergent Brugian filariasis, since most individuals who have tested positive are asymptomatic. Reports suggest that the re-emerged Brugia malayi is sub-periodic and of zoonotic origin, probably representing spill-over transmission from the principal reservoir hosts, which are domestic and stray dogs and cats [25,26]. The strain of B. malayi appears to be a genetic variant with very low detection rates by the Brugia rapid antibody test (sensitivity 25%) used in serological screening [27].

(c) . Soil-transmitted helminthiasis infections in high-risk communities

Like LF, STH infections are also known to be focal in nature. A review of the literature on STH infections in Sri Lanka, carried out about 20 years ago, identified two types of communities at high risk, despite declining prevalence in the rest of the country: slum areas of larger cities and towns, and tea and rubber plantations [9]. Thus, while a national survey carried out in 2003 found the overall combined prevalence of STH infections among primary school children to be 6.9% [28], a subsequent survey of primary school children in the plantation sector found 29.0% to have one or more STH infections, and 11.6% of the children had infections of moderate–heavy intensity [29].

The presence of pockets of high prevalence was confirmed by the national STH survey of 2017, which used multistage stratified cluster sampling of children attending primary schools in each of the nine provinces of Sri Lanka as well as primary schools serving low-income settlements in urban areas and the plantation sector. Risk of STH was modelled using generalized linear mixed effects models, and prevalence maps were developed to enable informed decision-making at the smallest health administrative level in the country (figure 2) [30].

Figure 2.

Figure 2.

Estimated soil-transmitted helminthiasis (STH) prevalence in Sri Lanka (adapted from [30]). Grey lines indicate district boundaries.

The parasitological survey showed that the transmission of STHs had continued to decline, with a combined national prevalence of approximately 1% among primary school children. As anticipated, prevalence in the high-risk communities surveyed was higher: approximately 2.6% in urban slums, and 9.0% in the plantation sector. Ascariasis was encountered in schools serving non-high-risk communities in only one province. The prevalence of ascariasis was much higher in the plantation sector communities compared with urban slums. By contrast, the prevalence of trichuriasis was relatively higher in the urban slums compared with the plantation sector. Low-intensity trichuriasis was seen more frequently than ascariasis in the non-high-risk communities, in four provinces. Low-intensity hookworm infections were also seen in the plantation sector communities and in non-high-risk communities in five provinces, but not in the urban slum communities.

Although the above-mentioned national surveys did not include adults, occasional studies have looked for hookworm infections in women of reproductive age. In a study that assessed the productivity of women tea pluckers in 2001, 10.3% of the 248 examined were found to have hookworm infections, all of light intensity [31].

No studies have been conducted to date in Sri Lanka to assess the continued efficacy of mebendazole or albendazole against the STHs. However, a small, randomized placebo-controlled study was conducted about 10 years ago, to evaluate the efficacy of mebendazole polymorphs against hookworm infection [32]. This study found that a single 500 mg dose of mebendazole, either as polymorph C alone, or as a mixture of polymorphs A and C, reduced faecal egg count rates by more than 80%; neither preparation was effective in achieving cure.

The highly heterogeneous pattern of infection described above probably results from a complex combination of factors, which include faecal contamination of soil because of promiscuous defaecation in communities with poor sanitation, conditions in the physical environment that allow eggs and larvae to remain viable, as well as the varying sensitivity of each helminth species to the benzimidazole anthelmintics and differences in the health-seeking behaviour in each type of community.

3. Strategies to control transmission

(a) . Lymphatic filariasis

During the phase of post-elimination as a public health problem, Sri Lanka has adopted a ‘test and treat’ approach wherein a 12-day course of diethylcarbamazine is administered together with a single dose of albendazole, to microfilaraemics detected during surveillance activities as per treatment guidelines and followed until clearance of parasites. The same strategy is adopted for both Bancroftian and Brugian filariasis. Community-based screening to identify indigenous cases and screening immigrants in their work settings are the main activities adopted to test humans.

Vector control strategies are no longer routinely practised although entomological surveys are carried out for both larvae and adult mosquitoes. High larval densities are controlled through environmental modifications and use of biological predators (larvivorous fish). Lack of intersectoral collaboration has hindered the efforts taken to clear water bodies of aquatic flora. Application of adulticidal chemicals in the control of other mosquito-borne infections such as dengue may have a collateral effect in reducing LF vector populations. Use of bed nets is encouraged in the endemic region through community awareness programmes.

(b) . Soil-transmitted helminthiasis infections

In 2012, the Ministry of Health issued guidelines for deworming children and pregnant women in the community setting for a 5-year period commencing 2013 [33]. These guidelines recommended biannual treatment with single-dose mebendazole for all children in three provinces (Uva, Sabaragamuwa and Central provinces) and annual treatment for children in all other provinces. During this period, however, paediatricians expressed concerns regarding the inappropriate, continued use of routine periodic deworming of children as a public health measure, and recommended that control programmes should be restricted to known high-risk communities such as those in the plantation sector [34]. The mebendazole used for the deworming programme was locally manufactured and procured by the Ministry of Health, with no donor funding.

Revised Guidelines on de-worming children and pregnant women against soil-transmitted helminths in community setting 2019–2022 [35] were issued in the light of findings from the 2017 national survey, using an approach that combined a parasitological survey with a geostatistical model to facilitate scaling down from a province-based national programme to one that targeted smaller administrative areas at risk of continued transmission. For those districts categorized as high and intermediate risk (basically those that had significant numbers of high-risk communities), the guidelines recommended continuation of routine annual deworming of pre-school-aged children and children in primary schools for a further 4 and 2 years, respectively. The guidelines also recommended discontinuation of routine deworming of children in districts categorized as low risk, as well as discontinuation of routine antenatal deworming of pregnant mothers in all districts. To support transition to individual case management of those with STH infections, the guidelines also provided advice on clinical management of severely anaemic pregnant mothers from high-risk communities, and several other additional measures to control STH transmission. These additional measures include: ensuring availability of water-sealed latrines for the safe disposal of faeces in all households even in high-risk communities; encouraging the use of footwear to prevent hookworm infection; and greater attention to preventive measures such as sanitation, personal hygiene and relevant health education.

4. Monitoring and surveillance

Even after national control programmes have achieved their targets, when transmission continues in residual pockets where environmental conditions remain conducive, it is essential to monitor prevalence in order to ensure that transmission does not bounce back after preventive chemotherapy programmes have been discontinued. This is exemplified by what happened with STH infections in the plantation sector of Sri Lanka. After a survey showed greater than 90% prevalence, biannual mass deworming targeting children aged 3–18 years was started in 1994 [36]. However, it was discontinued after about a decade, ostensibly owing to lack of funds, with no provision for continued surveillance. Four years after cessation of the programme, reassessment of the status of STH infections found a combined prevalence of 29.0%, while 11.6% of children had infections of moderate–heavy intensity [29].

By contrast, the AFC has continued a rigorous programme of entomological and parasitological surveillance and maintains a registry of patients with chronic disease. However, the continued use of night blood films as the principal means of diagnosing human infection is unsatisfactory. The peak periodicity of Bancroftian microfilariae is between 10 pm and 2 am, but the collection of blood usually takes place between 8 and 11 pm. It is likely that this reduces sensitivity and poses an especial problem in low-endemic settings like Sri Lanka. The blood volumes used to make the thick smears are measured approximately (three drops rather than 60 µl), which further compromises their quality. Although the use of filarial antigen test strips could rectify most of these shortcomings, the AFC has continued to rely on night blood smears because of the additional expense involved.

Another important consideration is that the surveillance data are not used optimally. Development of a comprehensive, georeferenced, digital database would enable the use of a geostatistical model to identify high-risk pockets, which can then be targeted for administration of IDA. Figure 3 shows the possible areas for occurrence of Bancroftian filariasis in Sri Lanka, derived from MaxEnt ecological niche modelling using georeferenced W. bancrofti microfilaria-positive patients' data from 2019 to 2021 (see electronic supplementary material for details of methods [3740]). This can also be used to target vector control measures when infection rates reach threshold levels.

Figure 3.

Figure 3.

Occurrence probability of W. bancrofti infections in Sri Lanka (MaxEnt ecological niche modelling). Grey lines indicate district boundaries.

Several approaches may be used to monitor the impact of STH control programmes. Community-based surveys that use qPCR as the diagnostic tool, such as used in the DeWorm3 trial, are the most accurate, but they are expensive, and currently unaffordable for programmatic purposes in a developing country context [41]. School-based cluster surveys that use the Kato–Katz technique as a diagnostic tool, as recommended by WHO [42], are less expensive than community-based surveys but nevertheless may cost about US$10 per child tested [43]. Integration with transmission assessment surveys for lymphatic filariasis may further reduce costs but may not be always feasible [44]. Geostatistical modelling that takes into account baseline prevalence and treatment coverage can be used to reduce the sample size required for surveys, as can the lot quality assurance approach. A sentinel site approach is probably the least expensive and most feasible in the context of a developing country that is scaling down its STH control programme.

With discontinuation of the routine deworming programmes, the Ministry of Health has taken steps to establish a sentinel surveillance system for STH infections to be carried out in the Colombo Municipal Council area, and in the districts of Nuwara Eliya, Badulla, Kegalle and Rathnapura, which all have large plantation-sector populations. Proposed surveillance tools include community-based assessment of prevalence of STH infections in the Colombo Municipal Council area and school-based assessment in the plantation-sector communities.

5. Way forward for long-term interruption of transmission

(a) . Strategies to interrupt transmission of lymphatic filariasis

WHO's 2030 targets for LF, as set out in the Roadmap for neglected tropical diseases 2021–2030, still focus on its elimination as a public health problem. The core intervention strategies include MDA with ivermectin, diethylcarbamazine and albendazole (IDA); vector control; case management of patients with lymphoedema; accessibility to water, sanitation, and hygiene (WASH) [45].

The superior efficacy of a single dose of triple therapy IDA compared with the dual regimen DA in clearing MF from the blood and sustaining the reduction for almost 3 years after PC administration have been well demonstrated by clinical trials [15,46].

The prevailing distribution of residual microfilaraemia and vector infection rates in Sri Lanka suggest that the ‘test and treat’ strategy alone may not suffice to further reduce or eliminate residual -transmission. An expanded treatment approach using the more efficacious triple drug combination, IDA, targeted at high-risk communities residing in foci with persistent ongoing transmission, along with re-introduction of a vector control component, is likely to accelerate the elimination of Bancroftian filariasis in Sri Lanka. Implementation of MDAs that target communities comprising the smallest high-risk administrative unit, which in the Sri Lankan context would be the Grama Niladhari (GN) division is an alternative strategy. Such a targeted approach of high-risk communities may enable capture of systematic non-compliers and administration of directly observed drug treatment may overcome non-adherence to treatment. Fine-scale mapping of residual infection would be a prerequisite for such a strategy.

However, it must be noted that interrupting the transmission of the re-emergent Brugian filariasis in Sri Lanka will require a very different approach, given its zoonotic nature and different vector species. A multidisciplinary approach combining veterinary control programs (sentinel animal surveys and mass treatment with ivermectin) and environmental management to eliminate vector breeding sites by clearance of water bodies of larval host plants (salvinia and pistia) is planned.

(b) . Strategies to interrupt transmission of soil-transmitted helminthiases

The WHO's 2030 targets for STH control, as set out in its Roadmap 2021–2030, relate to morbidity control, with elimination of STH infections as a public health problem (defined as reaching less than 2% proportion of STH infections of medium-to-high intensity, as assessed using the Kato–Katz technique) [45]. Core strategic interventions recommended by WHO include preventive chemotherapy that targets pre-school and school-aged children and women of child-bearing age, provision of facilities for adequate sanitation and waste management, improved hygiene practices, case management of infected persons and education for behavioural change targeting at-risk populations.

The ongoing DeWorm3 trial, conducted by the British Natural History Museum in India, Malawi and Benin, is designed to test the feasibility of moving beyond morbidity control, to focus on breaking the transmission of STH infections through community-wide MDA targeting all ages. For the purposes of the trial, breaking transmission is defined as reaching a prevalence of <2%, as detected by PCR, at least 2 years after the final round of MDA. This cluster-randomized trial, conducted at multiple sites in India, Benin and Malawi, compares the impact of twice-yearly MDA delivered over 3 years with standard of care according to national guidelines for STH control [47].

While the final results from this trial are not yet available, preliminary analyses have shown a clear relationship between the impact of community-wide MDA and the mean prevalence at a site, such that the sites with the highest baseline prevalence experienced the greatest drop in prevalence [48]. Using an approach that adopted a combination of statistical and mathematical methods to forecast the outcome of the trial, lower prevalences were found to be associated with higher degrees of aggregation. When worm populations are more highly aggregated, it becomes more difficult for all worms in all individuals to be killed, given imperfect drug efficacy and limited coverage. The authors conclude that in terms of reaching infected people with chemotherapy, MDA will become less effective both therapeutically and economically, especially if compliance is low, and to achieve elimination, both monitoring and treatment strategies will need to take into account parasite aggregation at small scales.

These findings from the DeWorm3 trial underscore the findings in Sri Lanka, that decisions regarding scaling down of a national programme must take into consideration the existence of residual pockets of ongoing transmission. These are usually communities where poverty is greater than in the rest of the country, where health literacy as well as housing and sanitation are poorer and promiscuous defaecation more common. If MDA is to be continued in residual pockets of transmission, decisions regarding the most appropriate anthelmintic should take into consideration available data regarding the persistent parasite species and known drug efficacy against such species.

Further operational research is required to strengthen surveillance and response measures with fine-scaled mapping of areas with residual transmission of both LF and STH for targeted intervention, develop spatial models of transmission to identify optimal intervention strategies, and identify trends in infection parameters. In-depth study of the characteristics of persistent parasite carriers (demographic, socioeconomic, compliance with MDA), estimation of the disease burden of LF (lymphoedema and hydrocoele) and ways of integrating MMDP services to the health system, and risk factors of B. malayi transmission in Sri Lanka are also important aspects where further research is required.

6. Conclusion

As more and more endemic countries achieve the targets set by WHO for the elimination of LF as a public health problem, and the control of morbidity due to STH, they are likely to encounter the same issues that Sri Lanka faces at present. Residual pockets of infection in conditions that are conducive to continued transmission of the causative parasite must be identified and targeted for continued implementation of control measures together with monitoring and surveillance, even after national targets have been achieved. This is important, both in terms of ensuring that such communities also experience the same health benefits that accrue from elimination of these age-old parasitic infections, and to eliminate the risk of resurgence of infection, from areas with continued transmission, in other parts of the country that have become free of the infections.

Acknowledgements

We wish to thank the Director of the Anti Filariasis Campaign and the field staff for the support extended.

Ethics

This work did not require ethical approval from a human subject or animal welfare committee.

Data accessibility

Data are provided as electronic supplementary material [49].

Authors' contributions

N.T.G.A.C.: writing—original draft; I.E.G.: data curation, formal analysis, validation, visualization, writing—review and editing; D.E.: formal analysis, methodology, software, validation, visualization, writing—review and editing; N.R.d.S.: conceptualization, project administration, writing—original draft.

All authors gave final approval for publication and agreed to be held accountable for the work performed herein.

Conflict of interest declaration

We declare that we have no competing interests.

Funding

This work did not receive any financial support.

References

  • 1.Abdulcader MH, Sasa M. 1966. Epidemiology and control of bancroftian filariasis in Ceylon. Jpn J. Exp. Med. 36, 609-646. [PubMed] [Google Scholar]
  • 2.Uragoda CG. 1987. A history of medicine in Sri Lanka: from the earliest times to 1948. Colombo, Sri Lanka: Sri Lanka Medical Association. [Google Scholar]
  • 3.Lambrecht FL. 1974. Entomological aspects of filariasis control in Sri Lanka. Bull. Wld Health Org. 51, 133-143. [PMC free article] [PubMed] [Google Scholar]
  • 4.Dissanaike AS. 1961. Filariasis in Ceylon then (1961) and in Sri Lanka now (1990–30 years on). Ann. Trop. Med. Parasitol. 85, 123-129. ( 10.1080/00034983.1991.11812538) [DOI] [PubMed] [Google Scholar]
  • 5.World Health Organization. 2000. Preparing and implementing a national plan to eliminate lymphatic filariasis (in countries where onchocerciasis is not co-endemic), WHO/CDS/CPP/CEE 200016. Geneva, Switzerland: World Health Organization.
  • 6.Gunaratna IE, et al. 2018. Impact of enhanced MDA with DEC plus albendazole for elimination of lymphatic filariasis in coastal Galle district, Sri Lanka. Am. J. Trop. Med. Hyg. 99, 612. ( 10.4269/ajtmh.abstract2018) [DOI] [Google Scholar]
  • 7.World Health Organization. 2016. Maldives and Sri Lanka eliminate lymphatic filariasis. See https://www.who.int/southeastasia/news/detail/03-06-2016-maldives-and-sri-lanka-eliminate-lymphatic-filariasis#:~:text=New%20Delhi%20%2D%20In%20a%20significant,of%20stigma%2C%20discrimination%20and%20poverty.
  • 8.De Silva NR, Arizono N, Chai J-Y, Nawa Y, Takahashi Y. 2005. Soil-transmitted helminth infections in Sri Lanka. In Food-borne helminthiasis in Asia, pp. 289-294. Chiba, Japan: Federation of Asian Parasitologists. [Google Scholar]
  • 9.Anti-Filariasis Campaign. 2022 Annual statistical bulletin 2016–2021. Colombo, Sri Lanka: Ministry of Health Nutrition and Indigenous Medicine.
  • 10.NTD Modelling Consortium Lymphatic Filariasis Group. 2019. The roadmap towards elimination of lymphatic filariasis by 2030. Insights from quantitative and mathematical modelling. Gates Open Res. 3, 1538. ( 10.12688/gatesopenres.13065.1) [DOI]
  • 11.World Health Organization. 2012. Report of the Expert Mission to Sri Lanka for Verification of elimination of Lymphatic Filariasis, SEA-CD-245. Geneva, Switzerland: World Health Organization.
  • 12.Rao RU, Nagodavithana KC, Samarasekara SD, Gross CW, Punchihewa MW, Dassanayaka TDM, Ranasinghe USB, Mendis D, Weil GJ. 2018. Comprehensive assessment of a hotspot with persistent Bancroftian filariasis in coastal Sri Lanka. Am. J. Trop. Med. Hyg. 99, 735-742. ( 10.4269/ajtmh.18-0169) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Rao RU, Nagodavithana KC, Samarasekara SD, Wijegunawardane AD, Premakumara WDY, Perera SN, Settinayake S, Miller JP, Weil GJ. 2014. A comprehensive assessment of lymphatic filariasis in Sri Lanka six years after cessation of mass drug administration. PLoS Negl. Trop. Dis. 8, e3281. ( 10.1371/journal.pntd.0003281) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Rao RU, Nagodavithana KC, Samarasekara SD, Dassanayaka TDM, Punchihewa MW, Ranasinghe USB, Weil GJ. 2017. Reassessment of areas with persistent lymphatic filariasis nine years after cessation of mass drug administration in Sri Lanka. PLoS Negl. Trop. Dis. 11, e0006066. ( 10.1371/journal.pntd.0006066) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Weil GJ, Jacobson GA, King JD. 2021. A triple-drug treatment regimen to accelerate elimination of lymphatic filariasis: from conception to delivery. Int. Health 13, S60-S64. ( 10.1093/inthealth/ihaa046) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Weerasooriya MV, Weerasooriya TR, Gunawardane NK, Samarawickrame WA, Kimura E. 2001. Epidemiology of Bancroftian filariasis in three suburban areas of Matara, Sri Lanka. Ann. Trop. Med. Parasitol. 95, 263-273. ( 10.1080/00034980120051287) [DOI] [PubMed] [Google Scholar]
  • 17.Jambulingam P, Subramanian S, de Vlas SJ, Vinubal C, Stalk WA. 2016. Mathematical modelling of lymphatic filariasis elimination programmes in India: required duration of mass drug administration and post-treatment level of infection indicators. Parasites Vectors 9, 501. ( 10.1186/s13071-016-1768-y) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Smith ME, Singh BK, Irvine MA, Stolk WA, Subramanian S, Hollingsworth TD, Michael E. 2017. Predicting lymphatic filariasis transmission and elimination dynamics using a multi-model ensemble framework. Epidemics 18, 16-28. ( 10.1016/j.epidem.2017.02.006) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Burgert-Brucker CR, et al. 2020. Risk factors associated with failing pre-transmission assessment surveys (preTAS) in lymphatic filariasis elimination programs: results of a multi-country analysis. PLoS Negl. Trop. Dis. 14, e0008301. ( 10.1371/journal.pntd.0008301) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Aye NN, Lin Z, Lon KN, Linn NYY, Nwe TW, Mon KM, Ramaiah K, Betts K, Kelly-Hope LA. 2018. Mapping and modelling the impact of mass drug adminstration on filariasis prevalence in Myanmar. Infect. Dis. Poverty 7, 56. ( 10.1186/s40249-018-0420-9) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Srividya A, Subramaniun S, Sadanandane C, Vasuki V, Jambulingam P. 2018. Determinants of transmission hotspots and filarial infection in households after eight rounds of mass drug administration in India. Trop. Med. Int. Health 23, 1251-1258. ( 10.1111/tmi.13143) [DOI] [PubMed] [Google Scholar]
  • 22.Wijegunawardana NDAD, Gunawardene YINS, Manamperi A, Senarathne H, Abeyewickreme W. 2012. Geographic information system (GIS) mapping of lymphatic filariasis endemic areas of Gampaha District, Sri Lanka based on epidemiological and entomological screening. SE Asian J. Trop. Med. Public Health 43, 557-566. [PubMed] [Google Scholar]
  • 23.Weerasooriya MV, Yahatugoda CT, Wickramasinghe D, Gunawardane NK, Dharmadasa RA, Vidanapathirana KK, Weerasekara SH, Samarawickrame WA. 2007. Social mobilization, drug coverage and compliance and adverse reactions in a mass drug administration (MDA) programme for the elimination of lymphatic filariasis in Sri Lanka. Filaria J. 6, 11. ( 10.1186/1475-2883-6-11) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Anti-Filariasis Campaign. 2017 Annual statistical bulletin 2016. Colombo, Sri Lanka: Ministry of Health and Indigenous Medicine.
  • 25.Mallawarachchi CH, Chandrasena TGAN, Premaratna R, Mallawarachchi SMNSM, de Silva NR. 2018. Human infection with sub-periodic Brugia spp. in Gampaha district, Sri Lanka; a threat to filariasis elimination status? Parasite Vectors 11, 68. ( 10.1186/s13071-018-2649-3) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Mallawarachchi CH, Chandrasena NTGA, Wickremesinghe S, Premaratna R, Mallawarachchi NSMSM, Gunawardane NYIS, de Silva NR. 2018. A preliminary survey of filarial parasites in dogs and cats in Sri Lanka. PLoS ONE 13, e0206633. ( 10.1371/journal.pone.0206633) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Mallawarachchi CH, Chandrasena TGAN, Withanage GP, Premaratna R, Mallawarachchi SMNSM, Gunawardane NY, Dasanayake R, de Silva NR. 2021. Molecular characterization of a reemergent Brugia malayi parasite in Sri Lanka suggestive of a novel strain. BioMed. Res. Int. 2021, 9926101. ( 10.1155/2021/9926101) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Pathmeswaran A, Jayatissa R, Samarasinghe S, Fernando A, de Silva RP, Thattil RO. 2005. Health status of primary schoolchildren in Sri Lanka. Ceylon Med. J. 50, 46-50. ( 10.4038/cmj.v50i2.1567) [DOI] [PubMed] [Google Scholar]
  • 29.Gunawardena N, Kumarendran B, Ebenezer R, Gunasingha MS, Pathmeswaran A. 2011. Soil-transmitted helminth infections among plantation-sector schoolchildren in Sri Lanka: prevalence after ten years of preventive chemotherapy. PLoS Negl. Trop. Dis. 5, e1591. ( 10.1371/journal.pntd.0001341) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Ediriweera DS, et al. 2019. Reassessment of the prevalence of soil-transmitted helminth infections in Sri Lanka to enable a more focused control programme: a cross-sectional national school survey with spatial modelling. Lancet Glob. Health 7, e1237-e1246. ( 10.1016/S2214-109X(19)30253-0) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Selvaratnam RR, de Silva LDR, Pathmeswaran A, de Silva NR. 2003. Nutritional status and productivity of Sri Lankan tea pluckers. Ceylon Med. J. 48, 114-118. ( 10.4038/cmj.v48i4.3326) [DOI] [PubMed] [Google Scholar]
  • 32.Gunawardena NK, Kumarendran B, Manamperi NH, Senarathna BP, Silva M, Pathmeswaran A, de Silva NR. 2013. Randomized placebo-controlled trial of the efficacy of mebendazole polymorphs in the treatment of hookworm infections. Am. J. Trop. Med. Hyg. 89, 313. See https://www.researchgate.net/publication/258218298_RANDOMIZED_PLACEBO-CONTROLLED_TRIAL_OF_THE_EFFICACY_OF_MEBENDAZOLE_POLYMORPHS_IN_THE_TREATMENT_OF_HOOKWORM_INFECTIONS. [Google Scholar]
  • 33.Ministry of Health. 2012. Guidelines on de-worming children and pregnant women in community setting 2013–2016. Colombo, Sri Lanka: Family Health Bureau, Ministry of Health, Nutrition and Indigenous Medicine. See https://fhb.health.gov.lk/images/FHB%20resources/ChildNutrition/CIRCULAR/Deworming%20guideline-English.pdf
  • 34.Mettananda S, de Silva DGH. 2017. Anaemia in children: are we using the correct prevention strategies? Ceylon Med. J. 62, 73-76. ( 10.4038/cmj.v62i2.8469) [DOI] [PubMed] [Google Scholar]
  • 35.Ministry of Health. 2018. Guidelines on de-worming children and pregnant women in community setting 20192022. Colombo, Sri Lanka: Family Health Bureau, Ministry of Health, Nutrition and Indigenous Medicine. See https://fhb.health.gov.lk/images/FHB%20resources/ChildNutrition/CIRCULAR/Deworming%20Guideline%20for%202019-2022%20%20%20English,Sinhala,Tamil.pdf.
  • 36.Sorensen E, Ismail M, Amarasinghe DK, Hettiarachchi I, Dassenaieke TS. 1996. The prevalence and control of soil-transmitted nematode infections among children and women in the plantations in Sri Lanka. Ceylon Med. J. 41, 37-41. [PubMed] [Google Scholar]
  • 37.Grinnell J. 1917. The niche-relationships of the California thrasher. Auk 34, 427-433. ( 10.2307/4072271) [DOI] [Google Scholar]
  • 38.Peterson AT, Papes M, Eaton M. 2007. Transferability and model evaluation in ecological niche modelling: a comparison of GARP and Maxent. Ecography. 30, 550-560. ( 10.1111/j.0906-7590.2007.05102.x) [DOI] [Google Scholar]
  • 39.Phillips SJ, Anderson RP, Schapire RE. 2006. Maximum entropy modelling of species geographic distributions. Ecol. Modell. 190, 231-259. ( 10.1016/j.ecolmodel.2005.03.026) [DOI] [Google Scholar]
  • 40.Delong ER, Delong DM, Clarke-Pearson DL. 1988. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44, 837-845. ( 10.2307/2531595) [DOI] [PubMed] [Google Scholar]
  • 41.Dunn JC, et al. 2020. The increased sensitivity of qPCR in comparison to Kato-Katz is required for the accurate assessment of the prevalence of soil-transmitted helminth infection in settings that have received multiple rounds of mass drug administration. Parasites Vectors 13, 324. ( 10.1186/s13071-020-04197-w) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.World Health Organization. 2011. Helminth control in school age children: a guide for managers of control programmes, 2nd edn. Geneva, Switzerland: World Health Organization. [Google Scholar]
  • 43.Assefa LM, Crellen T, Kepha S, Kihara JH, Njenga SM, Pullan RL, Brooker SJ. 2014. Diagnostic accuracy and cost-effectiveness of alternative methods for detection of soil-transmitted helminths in a post-treatment setting in western Kenya. PLoS Negl. Trop. Dis. 8, e2843. ( 10.1371/journal.pntd.0002843) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Gunawardena S, et al. 2014. Integrated school-based surveillance for soil-transmitted helminth infections and lymphatic filariasis in Gampaha district, Sri Lanka. Am. J. Trop. Med. Hyg. 90, 661. ( 10.4269/ajtmh.13-0641) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.World Health Organization. 2020. Ending the neglect to attain the sustainable development goals: a road map for neglected tropical diseases 2021–2030. Geneva, Switzerland: World Health Organization. [Google Scholar]
  • 46.Abelazm M, Abdelazeem BMD, Badr H, Gamal M,. Ashraf M, Abd-elsalam S. 2022. Efficacy and safety of triple versus dual therapy for lymphatic filariasis: a systematic review and meta-analyasis. Trop. Med. Int. Health 27, 226-235. ( 10.1111/tmi.13727) [DOI] [PubMed] [Google Scholar]
  • 47.Ásbjörnsdóttir KH, et al. 2018. Assessing the feasibility of interrupting the transmission of soil-transmitted helminths through mass drug administration: the DeWorm3 cluster randomized trial protocol. PLoS Negl. Trop. Dis. 12, e0006166. ( 10.1371/journal.pntd.0006166) [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Truscott JE, et al. 2021. Forecasting the effectiveness of the DeWorm3 trial in interrupting the transmission of soil-transmitted helminths in three study sites in Benin, India and Malawi. Parasites Vectors 14, 67. ( 10.1186/s13071-020-04572-7) [DOI]
  • 49.Chandrasena NTGA, Gunaratna IE, Ediriweera D, de Silva SR. 2023. Lymphatic filariases and soil-transmitted helminthiases in Sri Lanka: the challenge of eliminating residual pockets of transmission. Figshare. ( 10.6084/m9.figshare.c.6751764) [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

Data are provided as electronic supplementary material [49].


Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

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