de Souza et al. Parasites & Vectors  (2015) 8:488 
DOI 10.1186/s13071-015-1091-z
RESEARCH Open Access
The impact of residual infections on
Anopheles-transmitted Wuchereria bancrofti after
multiple rounds of mass drug administration
Dziedzom K. de Souza1, Rashid Ansumana2,3, Santigie Sessay4, Abu Conteh4, Benjamin Koudou2, Maria P. Rebollo5,
Joseph Koroma2, Daniel A. Boakye1 and Moses J. Bockarie2*
Abstract
Background: Many countries have made significant progress in the implementation of World Health Organization
recommended preventive chemotherapy strategy, to eliminate lymphatic filariasis (LF). However, pertinent challenges
such as the existence of areas of residual infections in disease endemic districts pose potential threats to the
achievements made. Thus, this study was undertaken to assess the importance of these areas in implementation
units (districts) where microfilaria (MF) positive individuals could not be found during the mid-term assessment
after three rounds of mass drug administration.
Methods: This study was undertaken in Bo and Pujehun, two LF endemic districts of Sierra Leone, with baseline
MF prevalence of 2 % and 0 % respectively in sentinel sites for monitoring impact of the national programme.
Study communities in the districts were purposefully selected and an assessment of LF infection prevalence was
conducted together with entomological investigations undertaken to determine the existence of areas with
residual MF that could enable transmission by local vectors. The transmission Assessment Survey (TAS) protocol
described by WHO was applied in the two districts to determine infection of LF in 6–7 year old children who
were born before MDA against LF started.
Results: The results indicated the presence of MF infected children in Pujehun district. An. gambiae collected in
the district were also positive for W. bancrofti, even though the prevalence of infection was below the threshold
associated with active transmission.
Conclusions: Residual infection was detected after three rounds of MDA in Pujehun – a district of 0 % Mf
prevalence at the sentinel site. Nevertheless, our results showed that the transmission was contained in a small
area. With the scale up of vector control in Anopheles transmission zones, some areas of residual infection may
not pose a serious threat for the resurgence of LF if the prevalence of infections observed during TAS are below
the threshold required for active transmission of the parasite. However, robust surveillance strategies capable of
detecting residual infections must be implemented, together with entomological assessments to determine if
ongoing vector control activities, biting rates and infection rates of the vectors can support the transmission of
the disease. Furthermore, in areas where mid-term assessments reveal MF prevalence below 1 % or 2 % antigen
level, in Anopheles transmission areas with active and effective malaria vector control efforts, the minimum 5
rounds of MDA may not be required before implementing TAS. Thus, we propose a modification of the WHO
recommendation for the timing of sentinel and spot-check site assessments in national programs.
Keywords: Lymphatic filariasis, Wuchereria bancrofti, Residual transmission, Hotspots, Sierra Leone
* Correspondence: Moses.Bockarie@lstmed.as.uk
2Centre for Neglected Tropical Diseases, Liverpool School of Tropical
Medicine, Liverpool, UK
Full list of author information is available at the end of the article
© 2015 de Souza et al. 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.
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 2 of 8
Background out when an implementation unit (District) has completed
The Global Program to Eliminate Lymphatic Filariasis five effective rounds of annual MDA and the prevalence
(GPELF) targets the elimination of LF as a public health of MF is less than 1 % in all sentinel and spot check sites
problem by the year 2020, through mass drug adminis- in the districts [24]. TAS is based on antigenemia preva-
tration (MDA) in endemic implementation units (IU), lence (in children) that may persist after transmission has
with the aim of interrupting transmission and stopping been interrupted. Interpretation of these endpoints is also
the spread of infection in all endemic areas. [1]. While confounded by the size of the evaluation unit, focality of
many countries have made significant progress in reducing the disease and movement of infected individuals from
transmission intensity and incidence of infection through endemic areas to non-endemic areas. Despite the fact that
community-wide treatments, there remain significant pro- Sierra Leone had only implemented three effective rounds
grammatic challenges to interrupting parasite transmission. of MDA for LF, this study was undertaken to investigate
These include effective implementation of the preventive the significance of residual infections for the outcome
chemotherapy strategy in urban settings, [2, 3] and the ex- of TAS in areas of Anopheles-transmitted LF previously
istence of areas of residual infection [4–6] that may precipi- treated with Ivermectin, and with active vector control
tate the spread of infection after the conditions for stopping activities.
MDA have been met [7, 8].
Implementing MDA is a critical challenge for the GPELF, Methods
especially in countries affected by conflict. Among the four Ethics statement
LF endemic countries (Sierra Leone, Liberia, Guinea and Approval for the study was obtained from the ethics
Cote d’Ivoire) recently affected by conflict in West Africa, review committee of the Liverpool School of Tropical
only Sierra Leone was implementing MDA (with Ivermec- Medicine and the Ministry of Health – Sierra Leone.
tin and Albendazole) in 2011. All 14 districts in Sierra Prior to conducting the survey and obtaining informed
Leone were endemic for LF antigen before MDA started in consent, repeated community meetings were held in all
2008 [9, 10]. Nevertheless, after three rounds of treatment of the villages to communicate the purposes of the study
(2008–2010), a midterm progress evaluation following and answer questions at the individual and community
WHO guidelines revealed that the microfilaria prevalence level. Informed consent to participate in the study was
in people five years and older was reduced to 0 % in five obtained from all individuals 18 years or older. Consent
districts [9]. The other nine districts had microfilaria was obtained from a parent or guardian of younger indi-
(MF) prevalence below 1 % in sentinel sites with the viduals. Informed consent was also received from mos-
exception of one district. The overall average MF preva- quito collectors, 18 years and above, after which they
lence, before and after the three MDAs, were 2.4 % and were trained in safe and scientifically reliable mosquito
0.3 % respectively [9]. collection. Consent was also sought from the head of the
LF and onchocerciasis are co-endemic in 12 of the 14 households where mosquito sampling was carried out.
districts in Sierra Leone. Prior to the initiation of MDA for For the Transmission Assessment Surveys (TAS), the
LF in Sierra Leone in 2007, many people in the implemen- communities where the schools were located were in-
tation units co-endemic for both diseases had received formed of the purpose of the study, in their local language.
more than 5 rounds of treatment with Ivermectin through Due to low literacy rates, informed oral consent was ob-
the community directed intervention (CDI) implemented tained from the community leaders, as well as parents and
by the African Programme for Onchocerciasis Control guardians of each child participating in the study. The
(APOC) [11]. Treatment for onchocerciasis and, scaling up names of consenting parents and their children were
of bed net distribution in Sierra Leone [12, 13] may have recorded, and only the principal investigators of the study
impacted LF prevalence because Ivermectin alone is also had access to this information. The data was analysed and
effective against LF [14–16], and treated bed nets dramatic- reported, to exclude any directly identifiable information,
ally reduce exposure to mosquito bites [17]. Furthermore, in order to maintain the anonymity of the parents and
in Sierra Leone as in other countries in West Africa, LF is children.
transmitted solely by the malaria carrying Anopheles
mosquitoes [18]. Anopheles-transmitted LF is highly focal Study sites
[19–21] and synchronous with intense malaria transmission This study was conducted in the Pujehun and Bo Districts
[21, 22]. Malaria control efforts targeting Anopheles mos- of Sierra Leone. Bo town is the second largest city and an
quitoes therefore have the potential to significantly impact important mining centre in Sierra Leone, whereas Pujehun
on LF transmission in West Africa, as was possibly the case is a less populated, semi-urban area. These districts are
in the interruption of LF transmission in Togo [23]. located in the rainforest area in the Southern Province, with
WHO recommends that a Transmission Assessment farming as an important socio-economic activity. Baseline
Survey (TAS) to determine when to stop MDA be carried MF (2007–8) and midterm (2011) surveys failed to identify
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 3 of 8
Table 1 Surveillance for LF in study sites in Pujehun and Bo Districts. *Schools in these communities were part of the TAS survey
District Site Females Males Total Tested ICT Positive (%)
Pujehun Sahn Malem 124 226 350 0 (0.0)
Karlu* 188 162 350 1 (0.3)
Gbondapi 192 158 350 3 (0.9)
Sumbuya Bessima 31 32 63 0 (0.0)
Kondorwahun 65 92 157 0 (0.0)
Vaama* 144 127 271 1 (0.4)
Total 744 797 1542 5 (0.3)
Bo Njala Komboya 164 186 350 3 (0.9)
Nyandeyama 144 183 327 6 (1.8)
Nengbema* 153 197 350 0 (0.0)
Mendewa 126 160 286 0 (0.0)
Total 587 726 1313 9 (0.7)
any MF positive individual in one of the two districts stud- Thus, mosquitoes were collected using the Pyrethrum
ied (Pujehun), which was maintained in this district, and Spray method, Exit Traps and Human Landing Collec-
the number of MF positive individuals in the second district tions, and processed as previously described [25]. Briefly,
(Bo) reduced from 2.0 % to zero after three rounds of DNA was extracted from pooled mosquitoes using the
MDA [9, 10]. Communities in the districts were visited Qiagen DNeasy tissue kit (Qiagen CA) extraction method.
to assess their sizes and distances from the district cap- This was followed by PCR to detect W. bancrofti DNA
itals, in order to plan the entomological investigations. using the method of Ramzy and colleagues [26]. A positive
The number of households was determined from the and negative control was included in all reactions and
community data. Based on this information study com- samples testing positive for W. bancrofti were confirmed
munities were purposefully selected to maximize the using a second PCR. Positive samples were also confirmed
collection of mosquitoes, taking into consideration lo- using the slightly modified loop-mediated isothermal
gistic demands. Six communities in the Pujehun Dis- amplification (LAMP) method for detecting W. bancrofti
tricts and four communities in the Bo District were DNA [27]. In each household surveyed for mosquitoes,
selected for the study (Table 1). The coordinates of the we collected information on the number of people living
communities and distance from the district capital were in the house and the number of people who used ITN the
recorded using a Garmin Handheld GPS. The map of night before the collection. From this information ITN
the study communities was drawn in ArcGIS version 10 usage rates were determined for each community.
(ESRI). While this study was not meant to undertake Transmis-
sion Assessment Surveys (TAS) [24], the TAS protocol was
Sample collection applied in the two districts because it is a statistically strong
Assessment for LF prevalence was conducted in the method to determine infection prevalence of LF in children
study communities using the Binax Now ICT card. as an indicator of active transmission in the district. TAS
Altogether, 1542 individuals were surveyed in the for LF is undertaken to determine whether infection has
Pujehun District while 1313 individuals were surveyed been reduced to levels below which transmission cannot be
in the Bo District. Samples were collected from indi- sustained, allowing for a decision to stop MDA. As such,
viduals aged between 6–65 years of age. children aged 6–7 years were sampled from various schools
Entomological surveys were also undertaken to deter- selected using the TAS protocol, and tested for LF antigen
mine the existence of active transmission in study areas, and microfilaria. Some schools in the LF assessment sites
and also study the importance of local transmission. formed part of the schools selected using the TAS protocol.
Table 2 TAS summary results for school children in Pujehun and Bo Districts [25]
District No. of Schools No. of Children Surveyed Males (%) Females (%) No. MF Positive No. Ag. Positive (%) Critical Cut-off Value
for Ag positives
Pujehun 31 1503 659 (43.8 %) 844 (56.2 %) 4 10 (0.67 %) 18
Bo 30 1564 682 (43.6 %) 882 (56.4 %) 0 3 (0.16 %) 18
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 4 of 8
Table 3 School clusters positive during the TAS survey
Names of schools Town/Village Total Tested No. of Ag. Positives (%) No. of MF Positives (%)
Pujehun Roman Catholic school Potoru-Zimmi Rd 50 3 (6.0) 2 (4.0)
United Muslim Association Tongay/Pujehun 42 3 (7.1 %) 0
SLC Primary School Boma 50 1 (2.0) 1 (2.0)
SLC Primary School Karlu* 50 1 (2.0) 1 (2.0)
SLC Primary School Mano Gbojeima 50 1 (2.0) 0
Roman Catholic school Zimmi Makpele 50 1 (2.0) 0
Bo S.D.A. Samamie Bo 59 1 (1.7) 0
UMC Jembeh Jembeh 52 1 (1.9) 0
UMC Primary School Benduma 49 1 (2.0) 0
Statistical analysis the recommended prevalence for stopping MDA in the
Infection in the vector population was calculated using the districts, antigen levels were ≥ 2 % in some of the school
Poolscreen v2.0 [28] to determine the maximum likelihood clusters used in the TAS protocol (Table 3).
of infection together with the associated 95 % CIs. From The entomological surveys revealed that low num-
the ICT and TAS survey, the prevalence (%) of antigenemia bers of An. gambiae were caught in the study villages
and microfilaremia was calculated as the number of positive and processed for W. bancrofti infection (Table 4). In
people divided by the number of people examined. Pujehun, a total of 259 An. gambiae mosquitoes were
processed for W. bancrofti infection in 21 pools (pool
Results range 3–20). Despite the low numbers of mosquitoes
The cross sectional surveys revealed that out of the six collected and processed, molecular xenomonitoring
communities surveyed in Pujehun district, three were revealed two pools positive for W. bancrofti DNA,
positive for W. bancrofti infection using ICT cards with a Maximum Likelihood Infection (MLI) estimate
(Table 1). In Bo, two communities out of four were of 0.79 % (Table 4), in communities where antigen
positive for antigen. The total antigen prevalence in the positive individuals were identified (Fig. 1). In Bo, 791
districts was 0.3 % (5/1542) and 0.7 % (9/1313) in the mosquitoes were collected and no positive mosquitoes
Pujehun and Bo districts respectively. were detected. The ITN usage in the districts was also
Following the TAS protocol, ten antigen and four MF estimated to be 66.1 % (193/292) in Pujehun and
positive children were identified in the Pujehun district 49.3 % (621/1260) in Bo.
(Table 2) [25], while only three antigen positive children
were detected in Bo. No MF positive children were de- Discussion
tected in Bo. The antigen levels following the school The results of the antigen prevalence survey revealed that
cluster surveys were 0.67 % and 0.16 % in Pujehun and levels were below the thresholds that signify sustainable
Bo respectively. Despite the antigen levels being below transmission [25]. However, it is worth mentioning that
Table 4 Xenomonitoring results from Pujehun and Bo Districts
Districts Sites ITN Usage (%) No. of mosquitoes No. of pools Pools positive (MLI %) 95 % CI
Pujehun Sahn Malen 30/59 (50.8) 65 5 0 -
Karlu* 22/37 (59.5) 75 5 1 (1.42) 0.044 - 7.1
Gbondapi 31/46 (67.4) 18 2 0 -
Sumbuya Bessima 35/73 (47.9) 14 2 0 -
Kundorwahun 42/44 (95.5) 36 2 0 -
Vaama 33/33 (100.0) 51 5 1 (2.04) 0.064 - 10.1
Total 193/292 (66.1) 259 21 2 (0.79) 0.094 - 2.76
Bo Njala Komboya 53/146 (36.3) 135 8 0 -
Nyandeyama 213/343 (62.1) 492 26 0 -
Nengbema 174/232 (75.0) 80 5 0 -
Mendewa 181/539 (33.6) 84 6 0 -
Total 621/1260 (49.3) 791 45 0 -
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 5 of 8
Fig. 1 Map of survey sites in Pujehun District
even though the antigen levels were below the recom- establish what can be considered a hotspot in LF trans-
mended levels for the entire districts, antigen levels were ≥ mission. We considered a hotspot to be: 1. an area
2 % in some of the school clusters used in the TAS proto- where MF carriers persisted after 3 or more rounds of
col, with similar observations made in Sri Lanka and MDA when the sentinel site prevalence is less than 1 %;
Zanzibar [5, 29]. During the mapping surveys in 2008, 2. school clusters with antigen prevalence of > 2 % in
Pujehun was one of the districts with low endemicity of 6–7 year olds, following TAS. The existence of areas
antigenemia (4 %), with no microfilaria detected [10]. of residual transmission in Pujehun District (Fig. 1)
Nonetheless, our study revealed the existence of areas illustrates the focality of Anopheles-transmitted LF
with residual transmission in Pujehun district with and challenges faced in selecting high risk areas for
evidence of active but highly focal transmission of LF sentinel site and spot check surveys, and the need
through the detection of MF in children and uptake of for adopting more statistically robust sampling strat-
MF by LF vectors. While areas of residual transmission egies and reviewing the size of the evaluation unit
may be termed as hotspots, it is important to clearly for TAS [4].
Fig. 2 Modification of the WHO recommendation [1] for timing of sentinel and spot-check site assessments in national programmes. * Likely, but
not necessary, to be conducted regardless of assessment results
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 6 of 8
The low numbers of mosquitoes collected in the study areas of possible transmission did not result in resurgence
areas is probably the result of the high ITN usage in the of the disease [36, 37, 41]. Before China was certified free
study areas (66.1 % and 49.3 % in Pujehun and Bo respect- of LF in 2007, studies had shown that despite the presence
ively). There has been an increased use of insecticide of residual MF prevalence in the population, transmission
treated nets through mass ITN distribution campaigns in was considered to have been interrupted [42, 43]. This
Sierra Leone and in the Pujehun and Bo Districts [12, 13]. does lead us to operate on the hypothesis that the thresh-
By 2010, 67.2 % LLIN usage was reported in the study old for active transmission of LF in areas where Anopheles
areas [13]. Prior to this, the use of ITN has never been mosquitoes exhibit facilitation is higher compared to areas
tried in forest zones, and the introduction of ITN in Bo where Culex mosquitoes are principal vectors. As such,
district followed earlier studies to evaluate the Anopheline these observations bring into question the importance of
ecology and behaviour, to understand the role of the areas with residual infections on the elimination of LF.
vectors in malaria epidemiology and formulate appropri-
ate strategies for the area [30–33]. Conclusion
The detection of positive mosquitoes in areas positive From this study and other reports from elsewhere, we
for antigen in humans indicates possible on-going trans- conclude that the existence of areas of residual transmis-
mission, and similar results have been obtained in the sion will not necessarily lead to the spread of Anopheles
American Samoa [34]. These results support the evidence transmitted LF infection, where the vectors exhibit facili-
that molecular xenomonitoring can be an effective tool in tation. What should be emphasized is the value of xeno-
post-MDA surveillance [5, 34]. While there is currently no monitoring in determining if ongoing vector control
existing target threshold for monitoring parasite DNA activities, biting rates and infection rates of the vectors
prevalence in Anopheline vectors [5, 35], 0.25 % has been can support the transmission of the disease. Additional
suggested as the maximum infection prevalence expected control strategies may then be implemented based on
to sustain transmission by Culex species [5]. Studies are the evidence obtained from the xenomonitoring surveys
required to determine cut-off threshold for Anopheles in these areas. Furthermore, it may not be necessary to
mosquitoes. Further, given that Culex mosquitoes are complete the minimum 5 rounds of MDA before imple-
more efficient LF vectors than Anopheles, we advocate the menting TAS, when mid-term assessments reveal MF
establishment for different cut-offs for these species by prevalence below 1 % or 2 % antigen level, in Anopheles
TAS, as the current algorithm for choosing TAS design is transmission areas with active and effective malaria vector
similar in areas where LF is transmitted by Anopheles and control efforts. Implementing 2 additional rounds of
Culex species [24]. MDA before TAS in these areas will require significant
In Sierra Leone, as in the other countries in West resources that can better be directed to other areas with
Africa, lymphatic filariasis is transmitted by the malaria more pressing needs. Thus we propose a modification
carrying Anopheles mosquitoes and Culex species play (Fig. 2) of the WHO recommendation for the timing of
little or no role in the transmission of the disease [18]. sentinel and spot-check site assessments in national pro-
Very early studies elsewhere have shown that where LF grams [1], depending on whether LF endemic areas have a
transmission by Anopheles mosquitoes was interrupted history of Ivermectin treatment and/or implement vector
through vector control alone, transmission never resumed. control strategies which may differ in various countries,
The control of vectors through house-spraying with through ITN/LLIN distribution or Indoor Residual Spray.
residual insecticides resulted in the sustained interruption
of LF by the Anopheles punctulatus group in Solomon Competing interests
The authors declare that they have no competing interests.
Islands [36] and parts of Papua New Guinea [37], and
cases of LF resurgence only detected in countries where Authors’ contributions
Culex mosquitoes were the vectors, including Zanzibar in Conceived and designed the experiments: DKdS, BGK, MPR, DAB, MJB.
Performed the experiments: DKdS, RA, SS, AB. Analysed the data: DKdS, RA,
United Republic of Tanzania [7, 8, 29]. As suggested by SS, AB, BGK, MPR, JBK, DAB, MJB. Contributed reagents/materials/ analysis
Webber, vector biting rates of Anopheline mosquitoes less tools: MJB, DAB. Wrote the paper: DKdS, RA, SS, AB, BGK, MPR, JBK, DAB, MJB.
than 0.66 bites/man/h are unlikely to sustain the transmis- All authors read and approved the final manuscript.
sion of LF [36], and malaria control efforts targeting the Acknowledgement
Anopheles mosquito therefore have the potential to impact This study was supported by the Filarial Programs Support Unit, through
LF transmission in Africa [23, 38], except in areas where funds from DFID. We are also grateful to the study communities and
participants, for accepting to take part in this study. A special thank-you to
some species of Anopheline mosquitoes have the potential all field and laboratory workers for their participation in this study.
to exhibit the phenomenon of limitation [39, 40]. As such,
what is the significance of areas of residual transmission Author details1Noguchi Memorial Institute for Medical Research, University of Ghana,
on the elimination of LF? Studies elsewhere, including Legon, Ghana. 2Centre for Neglected Tropical Diseases, Liverpool School of
Mali in West Africa, have shown that the existence of Tropical Medicine, Liverpool, UK. 3Mercy Hospital Research Laboratory, Bo,
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 7 of 8
Sierra Leone. 4Ministry of Health and Sanitation, Freetown, Sierra Leone. 5Task 19. Chesnais CB, Missamou F, Pion SD, Bopda J, Louya F, Majewski AC, et al. A
Force for Global health, Atlanta, USA. case study of risk factors for lymphatic filariasis in the Republic of Congo.
Parasit Vectors. 2014;7:300–0.
Received: 28 July 2015 Accepted: 11 September 2015 20. Cano J, Rebollo M, Golding N, Pullan R, Crellen T, Soler A, et al. The global
distribution and transmission limits of lymphatic filariasis: past and present.
Parasit Vectors. 2014;7(1):466.
21. Kazura JW, Bockarie MJ. Lymphatic filariasis in Papua New Guinea:
References interdisciplinary research on a national health problem. Trend Parasitol.
1. WHO. Lymphatic Filariasis: a handbook for national elimination 2003;19(6):260–3.
programmes. Geneva, Switzerland: World Health Organization; 2013. 22. Slater HC, Gambhir M, Parham PE, Michael E. Modelling Co-Infection with
2. Njomo DW, Mukoko DA, Nyamongo NK, Karanja J. Increasing Coverage in Malaria and Lymphatic Filariasis. PLoS Comput Biol. 2013;9(6), e1003096.
Mass Drug Administration for Lymphatic Filariasis Elimination in an Urban 23. Sodahlon YK, Dorkenoo AM, Morgah K, Nabiliou K, Agbo K, Miller R, et al. A
Setting: a Study of Malindi Town, Kenya. PLoS ONE. 2014;9(1), e83413. Success Story: Togo Is Moving toward Becoming the First Sub-Saharan
3. Weerasooriya M, Yahathugoda C, Wickramasinghe D, Gunawardena K, African Nation to Eliminate Lymphatic Filariasis through Mass Drug
Dharmadasa R, Vidanapathirana K, et al. Social mobilisation, drug coverage Administration and Countrywide Morbidity Alleviation. PLoS Negl Trop Dis.
and compliance and adverse reactions in a Mass Drug Administration 2013;7(4), e2080.
(MDA) Programme for the Elimination of Lymphatic Filariasis in Sri Lanka.
24. WHO. Monitoring and epidemiological assessment of mass drug
Filaria J. 2007;6(1):11.
administration in the global programme to eliminate lymphatic filariasis: a
4. Swaminathan S, Perumal V, Adinarayanan S, Kaliannagounder K, Rengachari
manual for national elimination programmes. In: WHO, editor. In: WHO/
R, Purushothaman J. Epidemiological Assessment of Eight Rounds of Mass
HTM/NTD/PCT/2011. 4th ed. Geneva: WHO; 2011. p. 1–79.
Drug Administration for Lymphatic Filariasis in India: Implications for
25. de Souza DK, Sesay S, Moore MG, Ansumana R, Narh CA, Kollie K, et al. No
Monitoring and Evaluation. PLoS Negl Trop Dis. 2012;6(11), e1926.
Evidence for Lymphatic Filariasis Transmission in Big Cities Affected by
5. Rao RU, Nagodavithana KC, Samarasekera SD, Wijegunawardana AD,
Conflict Related Rural–urban Migration in Sierra Leone and Liberia. PLoS
Premakumara WDY, Perera SN, et al. A Comprehensive Assessment of
Negl Trop Dis. 2014;8(2), e2700.
Lymphatic Filariasis in Sri Lanka Six Years after Cessation of Mass Drug
Administration. PLoS Negl Trop Dis. 2014;8(11), e3281. 26. Ramzy RMR, Farid HA, Kamal IH, Ibrahim GH, Morsy ZS, et al. A polymerase
6. Brady M, GAELF. Seventh meeting of the Global Alliance to Eliminate chain reaction-based assay for detection of Wuchereria bancrofti in human
Lymphatic Filariasis: reaching the vision by scaling up, scaling down, and blood and Culex pipiens. Trans R Soc Trop Med Hyg. 1997;91:156–60.
reaching out. Parasit Vectors. 2014;7(1):46. 27. Takagi H, Itoh M, Kasai S, Yahathugoda TC, Weerasooriya MV, et al.
7. Harb M, Faris R, Gad AM, Hafez ON, Ramzy RM. The resurgence of lymphatic Development of loop-mediated isothermal amplification method for
filariasis in the Nile delta. Bull World Health Organ. 1993;71:49–54. detecting Wuchereria bancrofti DNA in human blood and vector
8. Sunish IP, Rajendran R, Mani TR, Munirathinam A, Tewari SC, Hiriyan J, et al. mosquitoes. Parasitol Int. 2011;60:493–7.
Resurgence in filarial transmission after withdrawal of mass drug 28. Katholi C, Toé L, Merriweather A, Unnasch T. Determining the prevalence of
administration and the relation between antigenaemia and microfilaraemia- Onchocerca volvulus infection in vector populations by PCR screening of
a longitudinal study. Trop Med Int Health. 2002;7:59–69. pools of black flies. J Infect Dis. 1995;172:1414–7.
9. Koroma JB, Sesay S, Sonnie M, Hodges MH, Sahr F, Zhang Y, et al. Impact of 29. Rebollo MP, Mohammed KA, Thomas B, Ame S, Ali SM, Cano J, et al.
Three Rounds of Mass Drug Administration on Lymphatic Filariasis in Areas Cessation of Mass Drug Administration for Lymphatic Filariasis in Zanzibar
Previously Treated for Onchocerciasis in Sierra Leone. PLoS Negl Trop Dis. in 2006: Was Transmission Interrupted? PLoS Negl Trop Dis. 2015;9(3),
2013;7(6), e2273. e0003669.
10. Koroma J, Bangura M, Hodges M, Bah M, Zhang Y, Bockarie M. Lymphatic 30. Bockarie MJ, Service MW, Barnish G, Maude GH, Greenwood BM. Malaria in
filariasis mapping by Immunochromatographic Test cards and baseline a rural area of Sierra Leone. III. Vector ecology and disease transmission.
microfilaria survey prior to mass drug administration in Sierra Leone. Parasit Ann Trop Med Parasitol. 1994;88(3):251–62.
Vectors. 2012;5(1):10. 31. Bockarie MJ, Service MW, Toure YT, Traore S, Barnish G, Greenwood BM. The
11. Hodges ME, Koroma JB, Sonnie M, Kennedy N, Cotter E, MacArthur C. ecology and behavior of the forest form of Anopheles gambiae s.s.
Neglected tropical disease control in post-war Sierra Leone using the Parassitologia. 1993;35:5–8.
Onchocerciasis Control Programme as a platform. International Health. 32. Bockarie MJ. Vector ecology and malaria transmission in southern Sierra
2011;3(2):69–74. Leone. Liverpool: UK: University of Liverpool; 1992.
12. Bennett A, Smith SJ, Yambasu S, Jambai A, Alemu W, Kabano A, et al. 33. Bockarie MJ, Service MW, Barnish G, Toure YT. Vectorial capacity and
Household Possession and Use of Insecticide-Treated Mosquito Nets in entomologica; inoculation rates of Anopheles gambiae in a high rainfall
Sierra Leone 6 Months after a National Mass-Distribution Campaign. PLoS forested area of southern Sierra Leone. Trop Med Parasitol. 1995;46:164–71.
One. 2012;7(5), e37927. 34. Schmaedick MA, Koppel AL, Pilotte N, Torres M, Williams SA, Dobson SL,
13. Gerstl S, Dunkley S, Mukhtar A, Maes P, De Smet M, Baker S, et al. Long- et al. Molecular Xenomonitoring Using Mosquitoes to Map Lymphatic
lasting insecticide–treated net usage in eastern Sierra Leone – the success Filariasis after Mass Drug Administration in American Samoa. PLoS Negl
of free distribution. Trop Med Int Health. 2010;15(4):480–8. Trop Dis. 2014;8(8), e3087.
14. Dunyo SK, Nkrumah FK, Simonsen PE. Single-dose treatment of Wuchereria 35. Farid HA, Morsy ZS, Helmy H, Ramzy RM, El Setouhy M, Weil GJ. A critical
bancrofti infections with ivermectin and albendazole alone or in appraisal of molecular xenomonitoring as a tool for assessing progress
combination: evaluation of the potential for control at 12 months after toward elimination of Lymphatic Filariasis. Am J Trop Med Hyg.
treatment. Trans R Soc Trop Med Hyg. 2000;94(4):437–43. 2007;77(4):593–600.
15. Dunyo SK, Nkrumah FK, Simonsen PE. A randomized double-blind placebo- 36. Webber RH, Southgate BA. The maximum density of anopheline
controlled field trial of ivermectin and albendazole alone and in mosquitoes that can be permitted in the absence of continuing
combination for the treatment of lymphatic filariasis in Ghana. Trans R Soc transmission of filariasis. Trans R Soc Trop Med Hyg. 1981;75:499–506.
Trop Med Hyg. 2000;94(2):205–11. 37. Bockarie M. Can lymphatic filariasis be eradicated in Papua New Guinea?
16. Simonsen PE, Magesa SM, Dunyo SK, Malecela-Lazaro MN, Michael E. The Papua New Guinea Med J. 1994;37:61–4.
effect of single dose ivermectin alone or in combination with albendazole 38. Kelly-Hope LA, Molyneux DH, Bockarie MJ. Can malaria vector control
on Wuchereria bancrofti infection in primary school children in Tanzania. accelerate the interruption of lymphatic filariasis transmission in Africa;
Trans R Soc Trop Med Hyg. 2004;98(8):462–72. capturing a window of opportunity? Parasit Vectors. 2013;6:39.
17. Mutuku FM, King CH, Mungai P, Mbogo C, Mwangangi J, Muchiri EM, et al. 39. Amuzu H, Wilson M, Boakye D. Studies of Anopheles gambiae s.l (Diptera:
Impact of insecticide-treated bed nets on malaria transmission indices on Culicidae) exhibiting different vectorial capacities in lymphatic filariasis
the south coast of Kenya. Malar J. 2011;10:356–6. transmission in the Gomoa district, Ghana. Parasit Vectors. 2010;3(1):85.
18. de Souza DK, Koudou B, Kelly-Hope L, Wilson MD, Bockarie MJ, Boakye DA. 40. Boakye D, Wilson M, Appawu M, Gyapong J. Vector competence, for
Lymphatic filariasis vectors and the implications for accelerated elimination Wuchereria bancrofti, of the Anopheles populations in the Bongo district of
of Anopheles-transmitted filariasis in West Africa. Parasit Vectors. 2012;5:259. Ghana. Ann Trop Med Parasitol. 2004;98(5):501–8.
de Souza et al. Parasites & Vectors  (2015) 8:488 Page 8 of 8
41. Coulibaly YI, Dembele B, Diallo AA, Konate’ S, Dolo H, Coulibaly SY, et al.
The impact of six annual rounds of mass drug administration on Wuchereria
bancrofti infections in humans and in mosquitoes in Mali. Am J Trop Med
Hyg. 2015. doi:10.4269/ajtmh.14-0516.
42. De-jian S, Xu-li D, Ji-hui D. The history of the elimination of lymphatic
filariasis in China. Infectious Diseases of Poverty. 2013;2(1):30.
43. Shi ZJ. Study on the transmission threshold of filariasis. Chin J Parasitol
Parasit Dis. 1994;12(1):1–6.
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