Lymphatic filariasis (LF) is a neglected mosquito-borne parasitic disease caused by three species of filarial parasites—Wuchereria bancrofti, Brugia malayi and Brugia timori [1]. In May 1997, the World Health Assembly passed a resolution calling for the global elimination of LF as a public health problem by the year 2020. The World Health Organisation (WHO) subsequently launched the Global Programme to Eliminate Lymphatic Filariasis (GPELF) in 2000 to facilitate this aim [2]. In 1999, the Pacific Programme for the Elimination of Lymphatic Filariasis (PacELF) was formed to coordinate regional efforts toward elimination in the 22 Pacific Island countries and territories (PICTs) by 2020, utilising a strategy of annual mass drug administration (MDA) of a single dose of diethylcarbamazine (DEC) plus albendazole for the entire at-risk population [3].

The WHO criteria for ceasing MDA after a minimum of five effective annual rounds (coverage exceeding 65% of the total population) in areas where Aedes mosquitos are the primary vector is <1% antigenemia in a transmission assessment survey (TAS) of 6- to 7-year-old children. Critical cut-off values are calculated based on sample sizes designed so that a TAS evaluation unit (EU) has at least a 75% chance of passing if antigenemia is 0.5% and no more than 5% chance of passing if antigenemia is ≥1% [4]. Prior to the development of the TAS, PacELF had established separate criteria for ceasing MDA if <1% filarial antigenemia (<2% upper 95% CI) across all age groups, based on the results of a population-based cluster survey (C-survey).

American Samoa is an unincorporated territory of the USA. The population of 54,454 (in 2015) inhabits the islands of Tutuila, Aunu’u, Ofu-Olosega and Ta’u. The capital, Pago Pago, is located on Tutuila, the largest island, where >95% of the population reside. The territory was partitioned from neighbouring Samoa in 1899: however, the two communities continue to share strong family, cultural, linguistic and economic bonds. LF in American Samoa is caused by the diurnally sub-periodic Wuchereria bancrofti, transmitted predominantly by the day-biting mosquito Aedes polynesiensis, with the night-biting Aedes samoanus as a secondary vector [5–7].

LF prevalence surveys have been conducted in American Samoa since 1923, with microfilaremia (Mf) prevalence in pre-PacELF surveys as high as 21% in 1962 (n = 1000). MDA with DEC (6 mg/kg monthly for a total of 72 mg/kg over a year) was undertaken in 1963 and 1965. A follow-up survey in 1968 found Mf prevalence had decreased to 0.3% (n = 1053 across 13 villages) [3]. No further MDA interventions were recorded until the commencement of PacELF and the national elimination programme in 1999, when a nationwide convenience survey of 18 villages established a baseline prevalence of 16.5% (n = 3018) filarial antigenemia by immunochromatographic card test (ICT) [3]. Seven rounds of annual MDA followed during 2000–2006, targeting the whole population except pregnant women, children less than 2 years old and the severely ill [8].

MDA coverage in American Samoa was initially poor, ranging from 19% in 2000 to 49% in 2002. From 2002 to 2005, the national programme was independently evaluated using a variety of formative research methods including focus groups with drug distributors (programme directors, nurses, health assistants and volunteers); a multi-stage household cluster survey of community knowledge, attitudes and practices; and key informant interviews with church leaders. The programme evaluation resulted in significant changes to community mobilisation, behaviour change communication and drug delivery strategies. Notably, the evaluation identified the involvement of churches as a key driver of improved programme coverage, with over half of the population receiving treatment in conjunction with church attendance [9]. Coverage increased to 71% in 2003 and was sustained at a relatively high level in 2004 (65%), 2005 (67%) and 2006 (70%) [9].

A significant decrease in LF antigen prevalence was observed in sentinel villages between 2001 and 2006, coinciding with the improvements in MDA participation and coverage [10]. Two spot check village surveys in 2006 (a total of four villages) found higher prevalence outside of sentinel villages [8, 10, 11].

This paper reports on the results of a 2007 population-based PacELF C-survey and compares the proportion of antigen-positive adults in 2007 with those found in a 2010 study for corresponding villages. We aimed to identify potential risk factors for infection in 2007 and examine small-scale changes in antigenemia over time by comparing village-level adult seroprevalence between the 2007 and 2010 surveys. Furthermore, we aimed to reflect on how these small-scale variations in disease transmission may affect post-MDA surveillance practices and strategies.

Both the 2007 and 2010 studies showed a broad distribution of a few infected individuals with some clustering within villages, demonstrating that significant geographic heterogeneity can exist even in such a small island setting. This widespread, low-level distribution has also been demonstrated in a 2011 molecular xenomonitoring study [16]. A subsequent study that compared results of the 2010 human seroprevalence study and the 2011 entomology study provided evidence for good concordance between results from serology and molecular xenomonitoring during post-MDA surveillance in American Samoa [17].

The 2007 survey results did not meet the PacELF criterion of filarial antigenemia <1% (upper CI <2%) for ceasing MDA. The PacELF technical working group recommended that American Samoa undertake an additional round of MDA in 2008; however, this was not accomplished because of limited resources. Even in the absence of additional MDA, American Samoa conducted and passed a TAS in 2011, with a school-based survey of 1st and 2nd graders on Tutuila (n = 949, approximating to the 6- to 7-year-old age group) identifying two ICT-positive individuals (0.21%), below the critical cut-off value of six individuals. The two ICT-positive individuals attended the same school on Tutuila, but lived in different villages [18]. A subsequent 2010 seroepidemiological study of adults (using samples originally collected for a leptospirosis study) found evidence of spatial clustering of antigen-positive individuals in two villages on Tutuila (Fagali’i and Ili’ili), suggesting possible residual foci of transmission post-MDA. One of the villages included the school where the two antigen-positive children were identified in the 2011 TAS. Analysis of the demographic data indicated that adult males and recent migrants were at higher risk of LF antigenemia and demonstrated antibody positivity. This association suggests adults may serve as the primary reservoirs for continued transmission, despite low prevalence in younger age groups [15].

TAS and the PacELF C-survey are not designed to provide village-level prevalence estimates, but rather estimates of mean prevalence across an evaluation unit of one or more districts, which was a territory-wide estimate in this island setting. The comparisons between surveys confirm that these cross-sectional survey methods may not always provide an accurate reflection of antigenemia at the smaller-scale village level as expected, given the limited number of persons selected per village. Foci of residual transmission may not be identified which could then serve as areas of potential resurgence. Discrepancies in filarial antigenemia prevalence within some villages between 2007 and 2010 may suggest that foci of local transmission have developed in some villages and declined in others over a relatively short time period. However, these discrepancies could also be explained by limitations in the sampling method, sample sizes and tests used for the comparison.

The findings should be considered in light of the study’s limitations. Although both surveys utilised a similar random spatial sampling method, the 2007 study included multiple adults from the majority of households, while the 2010 study only included one person from the majority of households. No adjustment for clustering within households (which would have widened the confidence intervals around the prevalence estimate) was made for the 2007 dataset, although at the observed level of prevalence it would be expected to have had negligible effect. A further limitation is that the 2007 survey used ICT, while in 2010, stored serum samples collected for a different survey were tested for Og4C3 antigen [15]. Both tests measure circulating filarial antigen, but comparison is hampered by lack of a true gold standard. A multi-country comparison of ICT and Og4C3 antigen in multiple field laboratories concluded that although positive concordance was unexpectedly low at individual level, there was no difference in the prevalence estimates given by the two tests at a population level [19]. More recent studies have shown that concordance between the two tests is much greater when using serum/plasma (as done in this study) rather than dried blood spots for Og4C3 antigen testing [20].

The variability in village-level antigenemia within the 2007 and 2010 surveys suggests that there remains a significant gap in knowledge regarding LF transmission dynamics at small spatial scales. Further research and a greater understanding of these transmission dynamics, their impact on LF elimination efforts and how to accurately assess significant residual infection may become increasingly important as more countries move into the post-MDA phase and continue to work toward elimination. This research should include further longitudinal studies in villages or areas in which increases or a lack of decline in prevalence has been observed.

In American Samoa specifically, programmatic priorities to support the elimination of LF should include ongoing investigation and surveillance of hotspots identified during surveys, targeted testing and treatment of known high-risk groups and the comparison of TAS results in children against prevalence in older age groups.