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| ABSTRACT |
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| INTRODUCTION |
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Lymphatic filariasis is a disabling, disfiguring disease caused by parasitic worms and is ranked globally as one of the most common cause of permanent disability.2 It is estimated that 120 million people are infected in at least 80 countries throughout the tropics and sub-tropics.3
There is a body of evidence that suggests that elimination of LF is feasible; examples include Japan, Taiwan, South Korea, and the Solomon Islands using either vector control, diethylcarbamazine citrate (DEC), or a combination of them.4 New tools are available now that make elimination of LF even more of a possibility: the development of single-dose, two-drug treatment regimens, capable of reducing microfilaremia (MF) to zero or near zero for periods of one year or more and a new antigen test that can be used at any time of day in the field to identify the decrease in circulating adult worm antigen of Wuchereria bancrofti.5
As long ago as 1927, a prevalence of 31% for lymphatic filariasis infection was reported in males more than 12 years of age in Vanuatu.6 This is that last known survey in the country before a recent survey in 19971998 conducted by the Department of Health reported an MF prevalence of 2% and an LF antigen prevalence of 5% (Taleo G, unpublished data). Infection was higher in males than females and the province with the highest prevalence was Penama in the northern region of the country. An additional study in 19997 confirmed W. bancrofti as the parasite and Anopheles farauti as the main vector. This study also reported the peak microfilarial time as nocturnal, with two peak times of 10:00 PM and 4:00 AM. Furthermore, the timing of the vector activity was found to correspond with peak MF circulation time.
The purpose of this study was to conduct a midterm evaluation of the Vanuatu lymphatic filariasis elimination campaign and to present the methodology used.
| MATERIALS AND METHODS |
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60 years of age, 7 tablets) to be distributed annually for five years from 2000 to 2004 (pregnant women, babies less than two years of age, and sick and elderly individuals were excluded) and vector control. Vector control is based primarily on the use of bed nets in the intensified malaria control program. The filariasis program is also supported by a health education campaign that includes the training of health staff and of communities, and a political awareness program. Study site. All fieldwork described was carried out in Vanuatu, an archipelago in a north-south chain of islands extending some 800 km in the southern Pacific Ocean. The population of Vanuatu is 186,678 (national census, 1999). Three-quarters of the population live in rural areas supported by subsistence agriculture. Men are the heads of household and every village has a chief. Local traditional healers play an important role in the communities, and perceptions of disease are often linked to cultural explanations. The official languages are English, French, and Bislama, but more than 113 distinct languages are used in the archipelago. Cultures and traditions also vary markedly between islands.
This study was reviewed and approved by the Liverpool School of Tropical Medicine Ethics Committee and the Vanuatu Ministry of Health, having been recommended by the World Health Organization Pacific Elimination of Filariasis Secretariat. Verbal consent was obtained from the village chiefs before blood surveys were carried out.
Parasitologic survey. The four provinces with the highest recorded prevalence of LF in the baseline survey were chosen for follow-up blood studies. Within each of these provinces, the two villages with the highest prevalence of filariasis were selected as sentinel sites. These were Sola and Mosina in Torba Province, Wanur and Sakau in Penama Province, Orap and Unmet in Malampa Province, and Port Resolution and South River in Tafea Province. Two other villages, Redcliffe in Penama Province and Lingarak in Malampa Province, were selected for spot testing. Criteria for selecting the villages for spot testing were that they had not previously received intervention from research teams, as well as being areas of known high malaria prevalence. The reason for selecting areas of high malaria prevalence was that a previous study in Vanuatu had shown a positive correlation between malaria and filariasis prevalence (G. Taleo, unpublished data). All individuals more than 10 years of age in the villages were asked to come for a blood test (except in Port Resolution where the only first 300 only were examined). Furthermore, opportunistic testing of individuals coming to laboratories for malaria tests in the two urban areas of Vila (Efate Province) and Santo (Sanma Province) was also carried out.
All participants had a 100-µL blood sample taken during the day for the detection of W. bancrofti antigen using Binax (Portland, ME) immunochromatographic card tests (ICTs) and results were read at 10 minutes. All cases with a positive ICT result had an additional 60-µL night blood sample taken for detection of MF using the three-line blood smear method of Sasa.4 Blood was taken from finger pricks between 9:00 PM and midnight to coincide with the peak circulation time of the MF.7 Participants were also asked whether they normally used a bed net and whether they had used a bed net the previous night to ascertain the extent of bed net use. All participants testing positive in the antigen test were treated with albendazole and DEC.
Knowledge, attitudes, and practices (KAP) surveys. Two KAP surveys were carried out: one with health workers involved in distributing the medicine and another with the community. A structured written questionnaire was prepared and administered to all health workers attending the 2002 MDA workshop. Participants completed the questionnaires in writing anonymously. The questionnaire was designed locally based on results from semi-structured interviews carried out with heath workers earlier that year and was pre-tested.
A community KAP survey was carried out between April and June 2002. This questionnaire was prepared based on results from a baseline qualitative study on filariasis that was conducted in Vanuatu in 1999 before the start of the MDA (Secretariat of the Pacific Community, Anse Vata, New Caledonia, unpublished data). Questions were translated into Bislama and the questionnaire was pilot tested before implementation. The questionnaire was administered verbally to persons more than 16 years of age by health workers trained in administering the questionnaires and the results were recorded.
Statistical analysis. Statistical analysis was carried out using EpiInfo version 6 (Centers for Disease Control and Prevention, Atlanta, GA). Comparisons of prevalence of infection and the study population and general population were made using a chi-square test for significance. Mean MF density was compared using the Kruskal-Wallis test. The prevalence of MF and antigenemia in sentinel sites was standardized by age and sex using the total population of people tested in each village before and after the start of the MDA as the standard population. The KAP survey results were first analyzed by obtaining percentages and associations were tested using the chi-square test.
| RESULTS |
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2 = 127, degrees of freedom [df] = 1, P < 0.001) (Table 2
2 = 177, df = 1, P < 0.001) (Table 2
2 = 6.4, df = 1, P < 0.012) from the mean of 1,248 (geometric mean = 284) found during the baseline survey in 1998 (this mean excludes Wanur village because MF in slides were not quantified there during the 1998 baseline survey). Nurses recorded coverage when the MDAs were conducted. During the first MDA in 2000, average coverage across all sentinel sites was 73% (range = 5390%) and it increased the following year to 77% (range = 6490%).
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Knowledge, attitudes, and practices survey. Health workers component. A total of 106 questionnaires were completed. Some problems were reported by health workers in receiving the right amount of medicine, registration books, health education material, and receiving funds on time. However, the health workers involved in the program believed that the program was run well. Approximately 50% of the nurses interviewed reported encountering the following problems with the community during the MDA: 1) people feel healthy and do not see why they need to take medication; 2) false rumors make people afraid of taking the medicine; 3) people express concern over the large number of tablets that they have to swallow, which can be up to 10 in some cases; 4) people are afraid of the side effects; and 5) people want to take the medication home to have after they have eaten and before going to bed at night.
A total of 74% of nurses interviewed reported observing people take their medicine in 2000 and 94% reported this in 2001. Approximately 22% of nurses reported conducting the MDA house-to-house survey in 2000 and 29% in 2001, while approximately 65% in 2000 and 82% in 2001 gathered the community together in one place within the village. Nurses occasionally combined these methods of distribution.
Community survey component. A total of 1,632 questionnaires were completed by the community across all six provinces. Eight hundred nineteen of these were completed in South Ambae Island in Penama Province, which was previously identified as having the highest prevalence of filariasis in the country (Taleo G, unpublished data).
A total of 93% of the people surveyed said that they were given the drugs and 99% of all people given drugs swallowed them. A total of 98% of the people surveyed said they were happy to continue taking part in the MDA for another three years. The main reason (87%) people took the drugs was to protect themselves from LF. Few people said they took the drugs to stop the spread of it in the community, or to eliminate transmission. Only a small minority (4%) did not know why they were taking the medicine. The most common reason (37%) given by people not taking part in the MDA was that they missed the drug distribution. Reasons for missing the distribution included being on the home farm, traveling at the time of distribution, and because the nurse did not come to their house. Only 3% reported not taking part in the MDA because they were afraid of the drugs and their side effects.
Overall, 85% of people said they were aware beforehand of the date the drugs were to be distributed in their area, usually having been informed by a health worker. Other means whereby this information was communicated included the church, chief, word-of-mouth, posters, the radio, the Rotary Club, the police, and schoolteachers. Within the main town of Port Vila, 37% of the people interviewed heard about the program on the radio, whereas in other areas surveyed this was not an important means of communication. Those who had heard in advance of the drug distribution were significantly more likely to also report having taken part in the MDA (
2 = 29, df = 1, P < 0.001).
A total of 56% of the people surveyed knew that filariasis was transmitted by mosquitoes and 26% said they did not know how it was transmitted. Other answers included through malaria, by sexual transmission, through the MDA drugs, by swimming in dirty rivers, through food, and cultural-related beliefs such as stepping in someones footprint or sleeping by a certain stone. Persons who knew that the infection was transmitted by mosquitoes were significantly more likely to also report taking part in the MDA than persons who did not understand how the infection was transmitted (
2 = 10, df = 1, P = 0.001). When asked what was the best way to avoid getting filariasis 72% of people responded, "to take the medicine" This answer was also significantly associated with having taken part in the MDA (
2 = 15, df = 1, P < 0.001). Only 14% of the people mentioned using a bed net as a form of prevention for filariasis. When asked what you can do once someone has symptoms of LF, the most common answer (35%) was that they did not know. There were also many people (34%) who thought the disease could be treated with western medicine. Less than 1% responded that hygiene was important. Other answers included using traditional medicine, isolating the infected person, and the use of prayer and faith.
| DISCUSSION |
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Prevalence of microfilaremia was shown to have decreased by 93% to 0% in villages with a baseline prevalence of less then 8% and to between 4% and 1% in villages with a baseline prevalence between 20% and 30%. This is a clear indication that the intervention is working and that Vanuatu is on track to eliminate LF as a public health problem. Diethylcarbamazine alone or in combination with ivermectin has been demonstrated to be effective in significantly reducing prevalence and density of microfilaremia in other south Pacific countries: in Samoa three annual treatments of DEC achieved an estimated 80% reduction in the prevalence of microfilaremia.8 Similar results were obtained after a five-year annual treatment program in Fiji9 and in the Dreiker district of Papua New Guinea10 where a four-year MDA campaign using DEC alone or DEC plus ivermectin resulted in a reduction of microfilaria prevalence by 8698%. The study carried out in Papua New Guinea, which is also an area where Anopheles is the main vector, similarly reported that transmission of LF decreased substantially following four rounds of MDA in a test population of 2,500 residents, and that new infections in children were almost completely prevented.
In this study, 74% of persons surveyed in sentinel sites responded that they had used a bed net the previous night. The government of Vanuatu has vigorously pursued malaria control and in the last decade effort has concentrated on the provision of permethrin-treated bed nets, resulting in a sharp decrease in reported malaria cases. It is believed that bed nets also play an important role in reducing filarial transmission. Since filariasis is transmitted by the same anopheline mosquito throughout the archipelago, a valuable control synergy, in the form of bed net use, has been established.
Evidence for the usefulness of vector control as an adjunct to chemotherapy is increasing. House spraying with DDT has led to complete interruption of the transmission of W. bancrofti by mosquitoes of the An. punctualatus complex in the Solomon Islands.11 The use of polystyrene beads in Culex-transmitted filariasis has been shown to increase the impact of LF control programs when combined with mass drug distribution in both Zanzibar and India.1214 Studies in Kenya showed that when treated bed nets were introduced into 6 of the 12 villages studied, the number of bites per villager per year was reduced 23% and the annual transmission of lymphatic filariasis was reduced 92%.15 Similarly, a study of the impact of untreated bed nets on the prevalence of W. bancrofti infection and disease in the human population of Baga-bag Island, Papua New Guinea, where filariasis is transmitted by An. farauti, found that bed net users had a lower prevalence of W. bancrofti microfilaremia, antigenemia, and hydrocele than non-users.16
The use of the W. bancrofti antigen ICT has simplified the diagnosis of LF. These tests are highly sensitive when compared with thick blood films, can be used at any time of day, are simple enough for field use by people with minimal training, and results are available within 10 minutes.17 This has made them the test of choice for community surveys. The drawback is that it is not known for how long filarial antigenemia will persist in the absence of microfilaremia and ICTs give no indication of parasite load. The call has already been made for alternative tests that are easy to use and more accurately reflect the amount of ongoing transmission.18 The method used in this evaluation survey sought to make the best of available tests: surveying the whole population first during the day using ICTs and then following-up positive cases only with night blood film tests. For the purpose of a mid-term evaluation in which the objective is to assess whether prevalences of filarial infection are decreasing as expected and not to look for evidence of elimination of transmission, the method used in this survey of first screening with ICTs and following-up positive cases with MF tests is proposed for discussion and further research.
Including measures of process as well as outcome in this mid-term evaluation allowed program managers to ascertain the strengths and problem areas of the program. The program thus benefits from learning from experience and program delivery is continually improved. Several nurses reported receiving insufficient drug supplies to complete the MDA. However, this problem was partly overcome by health centers sharing drugs and with top-up supplies available at the provincial and national level.
Reported coverage by nurses during the MDA in villages ranged from 53% to 90% and self-reported coverage during this survey ranged from 77% to 98%. There are various possible reasons for the difference between these reported coverages. Nurses included people absent from the village and children less than two years of age in the denominator, but these people were not included during this survey. Also, interviewees may have been inclined to give a positive answer to please the health staff conducting the interviews. This potential bias in the reporting system might be overcome by using interviewers who were not from the Ministry of Health. However, results should ensure program managers that coverage results being reported by nurses after MDAs are not being greatly overestimated.
The Vanuatu program showed high levels of community participation with more than 90% of people questioned reporting that they had received the drugs during the last MDA. Previous research on filariasis MDA control programs in the Philippines, Thailand, Malaysia, and Indonesia show that to achieve high levels of coverage it is important to have easy access to the program and to have health education that increases understanding of the program, therefore minimizing fear of side effects.19 These findings support this conclusion, which shows that persons with knowledge of the disease and with prior knowledge of the date for distribution were more likely to take part in the MDA.
Although nurses in Vanuatu reported that they face problems with people being afraid of taking the medicine because of the large number of pills or because of side effects, this survey suggests that the percentage actually refusing treatment because of this reason is small (3% of those interviewed). In some areas, rumors circulated that the drugs would give you filariasis or that the government was trying to sterilize the population through the distribution of the drug. This was also encountered during mass distribution of ivermectin for onchocerciasis in Guatemala.20 Easy access to the program in Vanuatu was achieved through taking the drugs to the communities and by working together with the village chiefs and religious leaders to ensure that people were aware of the program. Ingestion of drugs was also maximized through the use of directly observed therapy.
The Vanuatu program is based on a strategy of directly observed therapy at the community level and complimented by the use of bed nets; a strong research-based information, education, and communication campaign; strong political support; and commitment from partners. The results of this mid-term evaluation show high coverage was maintained for the first two years of this campaign and resulted in a significant decrease in antigen prevalence, as well as MF prevalence and intensity of microfilaremia due to W. bancrofti.
Received December 9, 2004. Accepted for publication May 25, 2005.
Acknowledgments: We thank the Vector Borne Disease Control Unit staff, malaria supervisors, microscopists and laboratory technicians, nurses, and the community who all willingly gave of their time and effort to enable this study. We are also grateful to Kazuyo Ichimori and the PacELF team for their assistance, the Japanese International Cooperation Agency for supplying ICT kits, and several colleagues for their constructive comments on the drafts of the manuscript.
Financial support: This study was supported by GlaxoSmithKline.
Disclosure: Margaret Fraser currently works for the Liverpool Lymphatic Filanasis Support Centre, which is supported by grants from GlaxoSmithKline, the Department of International Development (United Kingdom), and the Bill & Melinda Gates Foundation. This statement is being made in the interest of full disclosure and not because the author considers this to be a conflict of interest.
* Address correspondence to Margaret Fraser, Vector Borne Disease Unit, Vanuatu Ministry of Health, Private Mail Bag 009, Port Vila, Vanuatu. E-mail: margaret.fraser{at}liverpool.ac.uk ![]()
Authors address: Margaret Fraser, George Taleo, Fasihah Taleo, James Yaviong, Morris Amos, Mark Babu, and Morris Kalkoa, Vector Borne Disease Unit, Vanuatu Ministry Of Health, Private Mail Bag 009, Port Vila, Vanuatu, E-mail: margaret.fraser{at}liverpool.ac.uk.
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