AJTMH Tropical Medicine and Hygiene News
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Am. J. Trop. Med. Hyg., 68(4 suppl), 2003, pp. 38-43
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (13)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by PHILLIPS-HOWARD, P. A.
Right arrow Articles by HAWLEY, W. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by PHILLIPS-HOWARD, P. A.
Right arrow Articles by HAWLEY, W. A.
Related Collections
Right arrow Epidemiology
Right arrow Helicobacter
Right arrow Malaria
Right arrow Medical Entomology

IMPACT OF PERMETHRIN-TREATED BED NETS ON THE INCIDENCE OF SICK CHILD VISITS TO PERIPHERAL HEALTH FACILITIES

PENELOPE A. PHILLIPS-HOWARD, BERNARD L. NAHLEN, KATHLEEN A. WANNEMUEHLER, MARGARETTE S. KOLCZAK, FEIKO O. TER KUILE, JOHN E. GIMNIG, KRIS OLSON, JANE A. ALAII, AMOS ODHACHA, JOHN M. VULULE, AND WILLIAM A. HAWLEY
Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia; Centre for Vector Biology and Control Research, Kenya Medical Research Institute, Kisumu, Kenya; Department of Infectious Diseases, Tropical Medicine & AIDS, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands; Office of Preventive Health, Kenyan Ministry of Health, Nairobi, Kenya


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
During a randomized controlled trial of insecticide (permethrin)-treated bed nets (ITNs) in an area with intense malaria transmission in western Kenya, we monitored 20,915 sick child visits (SCVs) by children less than five years of age visiting seven peripheral health facilities. The SCVs were monitored over a four-year period both before (1995–1996) and during the intervention (1997–1998). Results are used to estimate the effect of ITNs on the burden of malaria in this community and to evaluate the potential role of these facilities in assessment of the impact of large-scale public health interventions. Compared with baseline, a 27% greater reduction in the incidence of SCVs was seen in ITN villages than in control villages (37% versus 10%; P = 0.049). A similar reduction was observed in SCVs diagnosed as malaria (35% reduction in ITN villages versus 5% reduction in controls; P = 0.04). Two-hundred sixteen SCVs per 1,000 child-years were prevented; three-fourths of these were in children less than 24 months old. As a consequence of lack of laboratory facilities, severe anemia was rarely (< 2%) diagnosed, regardless of intervention status. No effect of ITNs on the incidence of respiratory tract infections, diarrhea, and other commonly diagnosed childhood illnesses was observed. The ITNs reduced the number of SCVs due to malaria, but had no effect on other illnesses. Routine statistics from these facilities provided useful information on trends in malaria incidence, but underestimated the burden of severe anemia.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Randomized controlled trials of insecticide (permethrin)-treated bed nets (ITNs) and curtains have demonstrated their efficacy in reducing child mortality in various transmission settings in Africa.1–5 Other studies have shown that ITNs reduce by approximately half the risk of malaria parasitemia, clinical malaria, and severe anemia in these areas.6–9 Morbidity studies associated with ITNs use active surveillance, thus allowing measurement of disease-specific incidence. While these studies provide useful estimates of the protective efficacy of ITNs on malaria morbidity, they provide no information on the actual number of sick children seeking care at peripheral health facilities, which is an important indicator of the public health burden of malaria in endemic areas.

Most morbidity studies associated with ITNs have relied on active surveillance. However, routine active surveillance to monitor efficacy is problematic for large-scale control programs.10,11 In contrast, routine passive surveillance by national programs, while simple and cheap, is generally considered less reliable, though efforts are underway to strengthen district level surveillance.12 During the course of a randomized controlled trial of ITNs in western Kenya, we analyzed data from peripheral health facilities to determine the impact of ITNs on all-cause and malaria-associated sick child visits (SCVs). We also explore the potential role of these facilities for passive morbidity surveillance in this rural setting.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study site and population. The study population, design, and methods used in the trial are described elsewhere.13,14 Briefly, randomization of ITNs to residents living in half of the villages was conducted through public lottery held during a district-wide meeting to launch the intervention in August 1996. Bed nets (Siamdutch Mosquito Netting Co., Bangkok, Thailand) pre-impregnated with a target dose of 0.5 g of permethrin/m2 of netting were distributed in Asembo during the fourth quarter of 1996 to cover all sleeping places (beds or mats) in 40 of the 79 villages. Bed nets were re-treated biannually by the study staff. The mortality trial was conducted from January 1997 to December 1998, but was extended for morbidity studies to March 1999 when control households received bed nets. The project achieved a bed net coverage rate of 1.46 persons per bed net, and an adherence rate (persons directly observed to be sleeping under bed nets) of 66% in children less than five years old.15

Passive surveillance in peripheral health facilities. A passive surveillance system was established in 13 of 15 peripheral health facilities in Asembo. Three-fourths of these facilities were government funded. Drugs were equally available to peripheral health facilities serving control and ITN villages and all facilities served both control and ITN-treated communities. Two facilities that did not routinely examine at least five sick children each day were excluded. Monitoring began in June 1996 with the assignment of one project staff per facility who interviewed the caregiver accompanying each sick child using a pre-coded questionnaire. In addition to demographic information and data on ITN use, details of the child’s illness were recorded using local disease terminology based upon baseline ethnographic studies. At the end of each day, the staff member transcribed to the questionnaire data from facility records on symptoms, diagnosis, and treatment of each child. Project staff did not participate in diagnosis or provide treatment or advice. Facility personnel were unaware of the randomization status of children. Retrospective review of SCVs prior to intervention was conducted in each facility. Project recorders transcribed all visits listed in health facility registers by date of visit, child’s name, age, village of residence, diagnosis, and treatment.16 Of 13 health facilities surveyed, seven that monitored SCVs continuously from January 1995 through March 1999 were selected for this analysis. The period January 1995 to December 1996 is the pre-intervention period; January 1997 to March 1999 is the intervention’ period, and for simplicity of reporting, January 1998–March 1999 is referred to as 1998.

Statistical analysis. Surveillance forms were collected weekly, checked, coded, and forwarded to the Kenya Medical Research Institute/Centers for Diseases Control and Prevention main office for data entry. Analysis was performed using Statistical Analysis System (SAS System for Windows, Release 8.01; SAS Institute, Cary, NC). The incidence of SCVs was calculated as the number of visits per 1,000 child-years. Each child could contribute multiple times to the numerator. The denominator was based on census data for the ITN study for the first quarter of 1997. The analysis assumed that the population remained constant over the intervention period regardless of intervention status.

All analysis was based on intention to treat. Data from children residing in four villages that were split into two for purposes of randomization were therefore excluded from the analysis, since their randomization status could not be accurately determined from village names. Preliminary analysis of pre-intervention data showed that the incidence of SCVs was higher in villages randomized to receive ITNs, compared with subsequent control villages. This complicated the interpretation of post-intervention comparisons between ITN and control villages since analysis had to take into account historical differences: the change in incidence was expressed as a percentage reduction; 100 x (1 - incidence rate ratio [IRR])%, where the ratio represents incidence during the intervention divided by pre-intervention rate. The difference in the percentage reduction in ITN and control villages was defined as the ITN-associated reduction: 100 x (IRRcontrol villages - IRRITN villages)%. The statistical significance of the differences over time between ITN and control villages was assessed using the Wald chi-square statistic of the interaction term between randomization status (ITN or control village) and time effect (pre- or during intervention). A significant interaction term indicates that the change over time is different between the ITN and control villages. The impact of ITNs by age group and by intervention study year (1997 versus 1998) was assessed using analogous interaction terms.

We estimated the potential number of SCVs prevented by ITNs per 1,000 child-years by multiplying the estimate of the bed net-associated reduction described earlier by the crude overall incidence rate in the entire pre-intervention study population. The potential rather than the actual number of visits prevented was calculated because use of the latter would have overestimated the effect of ITNs due to the unequal pre-intervention distribution of SCVs between subsequent ITN and control villages.

Poisson regression using GEE methods in the GENMOD procedure in SAS software was used. Because the trial used village as the unit of randomization, all P values and 95% confidence intervals were corrected for clustering at this level, assuming an exchangeable correlation structure for measures from the same village. Two sided P values < 0.05 were considered statistically significant.

Ethical clearance. The ITN trial was reviewed and approved by the institutional review boards of the Kenya Medical Research Institute (Nairobi, Kenya) and the Centers for Disease Control and Prevention (Atlanta, GA).


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Between January 1995 and March 1999, children 0–59 months old made 23,898 visits to the seven peripheral health facilities. Of these visits, 2,983 (12.4%) were excluded since village of residence could not be determined. Of the 20,915 SCVs used in the analysis, 11,378 were made in the two years pre-intervention and 9,537 were made during the intervention period. Nearly half (9,352; 44.7%) of the SCVs involved children less than 12 months old, 5,221 (25.0%) were 12–23 months old, and 6,342 (30.3%) were 24–59 months old. Monthly SCV incidence for the entire study population over the four-year monitoring period showed distinct seasonal trends in child morbidity (Figure 1Go). The SCVs generally increased 2–3 months following biannual peaks in rainfall. Between 55% and 80% of the SCVs were diagnosed as malaria (Figure 1Go).



View larger version (48K):
[in this window]
[in a new window]
  		    FIGURE 1. Trends in rainfall, sick child visits, and diagnoses of malaria and anemia at seven peripheral health facilities, before and during the insecticide-treated bed net intervention.

 
Impact of ITNs on all cause SCVs. In the pre-intervention period, the incidence of SCVs was higher among children from villages randomized to receive ITNs compared with those from villages randomized to the control arm (IRR = 1.41, 95% confidence limits [CL] = 0.81–2.44). Following the introduction of ITNs in 1997, the IRR (95% CL) decreased to 0.86 (0.56–1.31) in the first year, and increased again in the second year to 1.11 (0.75–1.66) (Figure 2Go). Overall, the IRR (95% CL) was 0.97 (0.66–1.44) during the intervention period. When we compared intervention and pre-intervention rates, the SCV incidence decreased by 27% more in ITN villages (37% [95% CL = 26–46]) than in control villages (10% [95% CL = -23–34]) (P = 0.049) (Table 1Go). The ITN-associated reduction in SCV incidence was significantly greater in 1997 than in 1998 (P = 0.0048) (Table 2Go). Although the reduction in incidence of SCVs associated with ITN use did not differ by age, many more SCVs were prevented in young children because the absolute number of SCVs is higher in this group (Table 1Go). Thus, three-fourths of 216 potential SCVs prevented occurred in infants and children less than 24 months of age.



View larger version (37K):
[in this window]
[in a new window]
  		    FIGURE 2. Incidence per 1,000 child months of sick child visits to seven peripheral health facilities before and during the insecticide-treated bed net intervention, by intervention status. The two solid lines represent the ratio of the incidence during and before the intervention period. Each quarter from January 1997 onwards is compared with the average incidence in the same quarter in 1995 and 1996. The dashed horizontal line represents the reference incidence ratio of 1. RR = rate ratio.

 

View this table:
[in this window]
[in a new window]
 
TABLE 1
Reduction in incidence of overall sick child visits in insecticide-treated bed net (ITN) and control villages
 

View this table:
[in this window]
[in a new window]
 
TABLE 2
Age-adjusted reductions in incidence of overall sick child visits in insecticide-treated bed net (ITN) and control villages by study year*
 
A total of 19,999 prescriptions for antimalarials, antipyretics, and antibiotics were issued to sick children following the introduction of bed nets. Of 10,617 sick child visits with drug treatment recorded, a total of 7,748 (73%) were prescribed chloroquine, 749 (7.1%) were prescribed sulfadoxine-pyrimethamine (SP), and 508 (4.8%) were prescribed amodiaquine. Only 28 (<1%) were given quinine. Eighty-six percent of all antimalarial treatments issued was chloroquine, 8.3% was SP, 5.6% was amodiaquine, and less than 1% was quinine. There was no significant difference in the frequency of treatment with an effective antimalarial by intervention status.

The incidence of prescriptions was reduced 30% more in ITN than control villages in parallel with the same overall reduction in the incidence of sick child visits. Thus, sick children from both from ITN and control villages who attended a health facility were each issued an average of 2.1 drugs per illness episode. Similarly, of children diagnosed with malaria, an average of 2.4 drugs were issued per malaria episode diagnosed, again regardless of their randomization status.

Impact of ITNs by diagnosis. Similar to the overall number of SCVs, a 30% greater reduction in the incidence of SCVs diagnosed as malaria was observed among visits from children living in ITN villages (30% versus 5%; P = 0.04) (Table 3Go). Diagnoses of severe malnutrition and anemia were rare and constituted only 1% and 2% of all SCVs, respectively, among children from the entire study population. The incidence of anemia, diarrhea, malnutrition, respiratory tract infections, and other illnesses in any age group also decreased with time, and this decrease was greater in intervention villages. However, none of these differences were statistically significant. Comparison by diagnosis of the potential number of SCVs prevented shows that the greatest reduction was in children diagnosed with malaria (Figure 3Go).


View this table:
[in this window]
[in a new window]
 
TABLE 3
Reduction in incidence by diagnosis in insecticide-treated bed net (ITN) and control villages*
 


View larger version (12K):
[in this window]
[in a new window]
  		    FIGURE 3. Potential number by diagnosis of sick child visits prevented following the introduction of insecticide –treated bed nets in children less than five 5 years of age. URTI = pper respiratory tract infection.

 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this study, we evaluated the impact of ITNs on SCVs to peripheral health facilities in rural western Kenya. Prior to intervention, the incidence of SCVs was higher in villages randomized to subsequently receive ITNs than in those villages destined to be controls. During the intervention, this trend reversed. Though incidence of SCVs in children less than five years old decreased in both ITN and control areas during the intervention phase, the extent of this decrease was substantially greater in ITN compared with control villages. The proportional reduction in SCVs was similar in all age groups, but the greatest benefit in terms of absolute number of SCVs prevented was in children less than 24 months of age, particularly in infants.

The reduction in SCVs from bed net villages was higher in the first year of the study compared with the second year, but it is possible, for a variety of reasons, that this does not reflect an actual decrease in efficacy. In May–September 1998, the number of SCVs decreased markedly in both ITN and control villages, possibly due to reduced rainfall during this part of the year,13 resulting in lower malaria transmission. Lower malaria transmission may also have resulted from a strong community effect by ITNs observed in this study, reducing malaria associated morbidity in children living within 300 meters of intervention villages (25% of the control population).17 A stronger community effect in the second study year resulting from the cumulative effects of insecticide on reducing mosquito densities over time may also partly explain the reduced morbidity in the control villages in the second year.17 In addition, because this analysis was based on data generated from routine statistics, we used a fixed denominator over time. However, the ITNs were found to have a marked impact on mortality in the first year in Asembo (reduction of 34%).18 Thus, the overall number of children, particularly infants, in ITN villages, but not in control villages, increased over time, as more children survived the first year to contribute to the second year. The use of a fixed, instead of time-dependent, denominator will thus underestimate the true denominator, leading to an overestimate of the incidence of SCVs in ITN villages in the second year, and thus an underestimate of the efficacy measurement. Other possible explanations for this apparent decrease in efficacy are the Hawthorne effect,19 and selective survival; high-risk children in control villages may die in the first year, and the surviving cohort contributing to the second year consists of a healthier selection of older children. Time to re-treatment with insecticide is unlikely to be a contributing factor because most delayed re-treatment occurred in Gem, not Asembo.18 It is unlikely that delayed acquisition of immunity resulting in increased malaria morbidity in older children played a role since no shift in the age distribution of SCVs over time was observed. There was also no evidence that the reduction in malaria resulted in increased morbidity due to other non-malaria related illnesses (replacement morbidity).

It is unlikely that our results were influenced by the type of health facility or the type of antimalarial treatment issued by these facilities. The health facilities were equally dispersed between intervention and control villages and none exclusively served children randomized into either intervention of control. Data from this, and the baseline study of diagnosis and prescribing practices,16 illustrated that the 86% of the sick children visiting health facilities received chloroquine, which was the first-line treatment of uncomplicated malaria at the time of the study. Sulfadoxine-pyrimethamine was made available as first line treatment of uncomplicated, microscopically confirmed Plasmodium falciparum malaria to children participating in longitudinal monitoring in the 19 cohort villages.13 However, the villages were randomized equally between intervention and control arms in both the cohort and remaining villages.14

Although none of the clinics had facilities for microscopy or assessment of hemoglobin concentrations, we found a significant reduction in the proportion of SCVs diagnosed to have malaria, but no reduction in the proportion of diagnosis for other common childhood illnesses including respiratory tract infection, diarrhea, measles, or helminth infection. This overall result is consistent with findings of detailed cross-sectional and longitudinal surveys in the same population,20 suggesting that statistics gleaned from peripheral health facilities can provide useful estimates of efficacy of public health interventions in this rural setting. An ITN trial in coastal Kenya also showed that records from Kilifi district hospital could be used to detect a reduction in crude hospital admission rates, malaria admissions, and severe malaria admissions. An important advantage of passive surveillance through routine facilities is that an estimate of the effect of an intervention on actual numbers of children seeking health care may be obtained.

This study also illustrates the limitations of statistics from rural health facilities for monitoring of illnesses requiring laboratory diagnosis. Malaria is one of the main causes of severe anemia in this area, particularly in young children.21–23 In concurrent cross-sectional surveys, the prevalence of any anemia (hemoglobin level <11 g/dL) and severe anemia (hemoglobin level < 7 g/dL) was 70% and 6.9%, respectively, with 34% of children exhibiting detectable pallor.23 In the same study, a reduction of 39% in severe anemia in children less than three years old was associated with ITN use,20 and in a birth cohort of 900 infants a reduction of 60% was observed.23 However, no reduction in anemia was reflected in health statistics. This was most likely due to the low prevalence of anemia detected (2%) in the absence of laboratory capabilities. With this diagnostic limitation, it is unlikely than anemia can effectively be used as a key indicator for measuring the impact of a malaria control intervention through rural health facilities.

Two important conclusions can be drawn from this study. First, and most important, is the observation that ITN use was associated with a reduction of 27% in SCVs at peripheral health facilities, reflecting substantial amelioration of the malaria burden on both the children of Asembo and the health care system of Asembo. Second, we confirmed that passive surveillance in peripheral health facilities provided information on disease trends that was sufficiently sensitive to detect a substantial ITN-related reduction in malaria-associated SCVs (though not anemia) among pre-school children.

Acknowledgments: We thank the health facility recorders and data entry staff for their contribution to this study, and Caleb Ouma and Gideon Ogude for their supervisory assistance. We are grateful to the residents of Asembo for their cooperation. Dr. Kevin DeCock is thanked for his comments on the manuscript. Kathleen A. Wannemuehler acknowledges administrative support from the Oak Ridge Institute for Science and Education (Oak Ridge, TN). This paper is published with the permission of the Director of the Kenya Medical Research Institute.

Financial support: The bed net project was funded by the United States Agency for International Development.

Disclaimer: The opinions or assertions contained in this manuscript are the private ones of the authors and are not to be construed as official or reflecting the views of the U.S. Public Health Service or Department of Health and Human Services. Use of trade names is for identification only and does not imply endorsement by the U.S. Public Health Service or Department of Health and Human Services.

Authors’ addresses: Penelope A. Phillips-Howard, Kathleen A. Wannemuehler, Margarette S. Kolczak, Feiko O. ter Kuile, John E. Gimnig, Kris Olson, and William A. Hawley, Division of Parasitic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Mailstop F-22, 4770 Buford Highway, Atlanta, GA 30341. Bernard L. Nahlen, Roll Back Malaria, World Health Organization, Avenue Appia 20, 1211 Geneva 27, Switzerland. Jane A. Alaii, Amos Odhacha, and John M. Vulule, Centre for Vector Biology and Control Research, Kenya Medical Research Institute, PO Box 1578, Kisumu, Kenya.


REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. D’Alessandro U, Olaleye BO, McGuire W, Langerock P, Bennett S, Aikins MK, Thomson MC, Cham MK, Cham BA, Greenwood BM, 1995. Mortality and morbidity from malaria in Gambian children after introduction of an impregnated bednet programme. Lancet 345: 479–483.[ISI][Medline]
  2. Binka FN, Kubaje A, Adjuik M, Williams LA, Lengeler C, Maude GH, Armah GE, Kajihara B, Adiamah JH, Smith PG, 1996. Impact of permethrin impregnated bednets on child mortality in Kassena-Nankana district, Ghana: a randomized controlled trial. Trop Med Int Health 1: 147–154.[ISI][Medline]
  3. Nevill CG, Some ES, Mung’ala VO, Mutemi W, New L, Marsh K, Lengeler C, Snow RW, 1996. Insecticide-treated bednets reduce mortality and severe morbidity from malaria among children on the Kenyan coast. Trop Med Int Health 1: 139–146.[ISI][Medline]
  4. Habluetzel A, Diallo DA, Esposito F, Lamizana L, Pagnoni F, Lengeler C, Traore C, Cousens SN, 1997. Do insecticide-treated curtains reduce all-cause child mortality in Burkina Faso? Trop Med Int Health 2: 855–862.[ISI][Medline]
  5. Schellenberg JR, Abdulla S, Nathan R, Mukasa O, Marchant TJ, Kikumbih N, Mushi AK, Mponda H, Minja H, Mshinda H, Tanner M, Lengeler C, 2001. Effect of large-scale social marketing of insecticide-treated nets on child survival in rural Tanzania. Lancet 357: 1241–1247.[ISI][Medline]
  6. Lengeler C, 2000. Insecticide-treated bednets and curtains for preventing malaria. Cochrane Database Syst Rev 320: CD000363 .
  7. Snow RW, Molyneux CS, Njeru EK, Omumbo J, Nevill CG, Muniu E, Marsh K, 1997. The effects of malaria control on nutritional status in infancy. Acta Trop 65: 1–10.[ISI][Medline]
  8. Habluetzel A, Cuzin N, Diallo DA, Nebie I, Belem S, Cousens SN, Esposito F, 1999. Insecticide-treated curtains reduce the prevalence and intensity of malaria infection in Burkina Faso. Trop Med Int Health 4: 557–564.[ISI][Medline]
  9. Abdulla S, Schellenberg JA, Nathan R, Mukasa O, Marchant T, Smith T, Tanner M, Lengeler C, 2001. Impact on malaria morbidity of a programme supplying insecticide treated nets in children aged under 2 years in Tanzania: community cross sectional study. BMJ 322: 270–273.[Abstract/Free Full Text]
  10. Lengeler C, Snow RW, 1996. From efficacy to effectiveness: insecticide-treated bednets in Africa. Bull World Health Organ 74: 325–332.[ISI][Medline]
  11. D’Alessandro U, Olaleye B, Langerock P, Bennett S, Cham K, Cham B, Greenwood BM, 1997. The Gambian National Impregnated Bed Net Programme: evaluation of effectiveness by means of case-control studies. Trans R Soc Trop Med Hyg 91: 638–642.[ISI][Medline]
  12. World Health Organization, 1999. Integrated Disease Surveillance in the WHO African Region. A Regional Strategy for Communicable Diseases 1999–2003. Geneva: World Health Organization, Regional Office for Africa.
  13. Phillips-Howard PA, Nahlen BL, Alaii JA, ter Kuile FO, Gimnig JE, Terlouw DJ, Kachur SP, Hightower AW, Lal AA, Schoute E, Oloo AJ, Hawley WA, 2003. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya. I: Development of infrastructure and description of study site. Am J Trop Med Hyg 68(Suppl 4): 3–9.[Abstract/Free Full Text]
  14. Phillips-Howard PA, ter Kuile FO, Nahlen BL, Alaii JA, Gimnig JE, Kolczak MS, Terlouw DJ, Kariuki SK, Shi YP, Kachur SP, Hightower AW, Vulule JM, Hawley WA, 2003. The efficacy of permethrin-treated bed nets on child mortality and morbidity in western Kenya. II: Study design and methods. Am J Trop Med Hyg 68(Suppl 4): 10–15.[Abstract/Free Full Text]
  15. Alaii JA, Hawley WA, Kolczak MS, ter Kuile FO, Gimnig JE, Vulule JM, Odhacha A, Oloo AJ, Nahlen BL, Phillips-Howard PA, 2003. Factors affecting use of permethrin-treated bed nets during a randomized-controlled trial in western Kenya. Am J Trop Med Hyg 68(Suppl 4): 137–141.[Abstract/Free Full Text]
  16. Phillips-Howard PA, Wannemuehler KA, ter Kuile FO, Hawley WA, Kolczak MS, Odhacha A, Vulule JM, Nahlen BL, 2003. Diagnostic and prescribing practices in peripheral health facilities in rural western Kenya. Am J Trop Med Hyg 68(Suppl 4): 44–49.[Abstract/Free Full Text]
  17. Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, Nahlen BL, Gimnig JE, Kariuki SK, Kolczak MS, Hightower AW, 2003. Community-wide effects of permethrin-treated bed nets on child mortality and malaria morbidity in western Kenya. Am J Trop Med Hyg 68(Suppl 4): 121–127.[Abstract/Free Full Text]
  18. Phillips-Howard PA, Nahlen BL, Kolczak MS, Hightower AW, ter Kuile FO, Alaii JA, Gimnig JE, Arudo J, Vulule JM, Odacha A, Kachur SP, Schoute E, Rosen DH, Sexton JD, Oloo AJ, Hawley WA, 2003. Efficacy of permethrin-treated bed nets in the prevention of mortality in young children in an area of high perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68(Suppl 4): 23–29.[Abstract/Free Full Text]
  19. Mayo E, 1949. The Social Problems of an Industrial Civilization. London: Routledge.
  20. ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, Kolczak MS, Kariuki SK, Shi YP, Kwena AM, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria and all cause morbidity in young children in an area of intense perennial malaria transmission in western Kenya: Cross-sectional survey. Am J Trop Med Hyg 68(Suppl 4): 100–107.[Abstract/Free Full Text]
  21. McElroy PD, Ter Kuile FO, Lal AA, Bloland PB, Hawley WA, Oloo AJ, Monto AS, Meshnick SR, Nahlen BL, 2000. Effect of Plasmodium falciparum parasitemia density on hemoglobin concentrations among full-term, normal birth weight children in western Kenya, IV. The Asembo Bay Cohort Project. Am J Trop Med Hyg 62: 504–512.[Abstract]
  22. Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, New-bold C, Gupta S, Marsh K, 1997. Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349: 1650–1654.[ISI][Medline]
  23. ter Kuile FO, Terlouw DJ, Kariuki SK, Phillips-Howard PA, Mirel LB, Hawley WA, Friedman JF, Shi YP, Kolczak MS, Lal AA, Vulule JM, Nahlen BL, 2003. Impact of permethrin-treated bed nets on malaria, anemia and growth in infants in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68(Suppl 4): 68–77.[Abstract/Free Full Text]



This article has been cited by other articles:


Home page
 Am J Trop Med HygHome page
P. E. OKELLO, W. VAN BORTEL, A. M. BYARUHANGA, A. CORREWYN, P. ROELANTS, A. TALISUNA, U. D'ALESSANDRO, and M. COOSEMANS
Variation in malaria transmission intensity in seven sites throughout Uganda.
Am J Trop Med Hyg, August 1, 2006; 75(2): 219 - 225.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
K. ADAZU, K. A. LINDBLADE, D. H. ROSEN, F. ODHIAMBO, P. OFWARE, J. KWACH, A. M. VAN EIJK, K. M. DECOCK, P. AMORNKUL, D. KARANJA, et al.
HEALTH AND DEMOGRAPHIC SURVEILLANCE IN RURAL WESTERN KENYA: A PLATFORM FOR EVALUATING INTERVENTIONS TO REDUCE MORBIDITY AND MORTALITY FROM INFECTIOUS DISEASES
Am J Trop Med Hyg, December 1, 2005; 73(6): 1151 - 1158.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
P. A. PHILLIPS-HOWARD, F. O. TER KUILE, B. L. NAHLEN, J. A. ALAII, J. E. GIMNIG, M. S. KOLCZAK, D. J. TERLOUW, S. K. KARIUKI, Y. P. SHI, S. P. KACHUR, et al.
THE EFFICACY OF PERMETHRIN-TREATED BED NETS ON CHILD MORTALITY AND MORBIDITY IN WESTERN KENYA II. STUDY DESIGN AND METHODS
Am J Trop Med Hyg, April 1, 2003; 68(90040): 10 - 15.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
P. A. PHILLIPS-HOWARD, B. L. NAHLEN, M. S. KOLCZAK, A. W. HIGHTOWER, F. O. TER KUILE, J. A. ALAII, J. E. GIMNIG, J. ARUDO, J. M. VULULE, A. ODHACHA, et al.
EFFICACY OF PERMETHRIN-TREATED BED NETS IN THE PREVENTION OF MORTALITY IN YOUNG CHILDREN IN AN AREA OF HIGH PERENNIAL MALARIA TRANSMISSION IN WESTERN KENYA
Am J Trop Med Hyg, April 1, 2003; 68(90040): 23 - 29.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
J. ARUDO, J. E. GIMNIG, F. O. TER KUILE, S. P. KACHUR, L. SLUTSKER, M. S. KOLCZAK, W. A. HAWLEY, A. S. S. ORAGO, B. L. NAHLEN, and P. A. PHILLIPS-HOWARD
COMPARISON OF GOVERNMENT STATISTICS AND DEMOGRAPHIC SURVEILLANCE TO MONITOR MORTALITY IN CHILDREN LESS THAN FIVE YEARS OLD IN RURAL WESTERN KENYA
Am J Trop Med Hyg, April 1, 2003; 68(90040): 30 - 37.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
P. A. PHILLIPS-HOWARD, K. A. WANNEMUEHLER, F. O. TER KUILE, W. A. HAWLEY, M. S. KOLCZAK, A. ODHACHA, J. M. VULULE, and B. L. NAHLEN
DIAGNOSTIC AND PRESCRIBING PRACTICES IN PERIPHERAL HEALTH FACILITIES IN RURAL WESTERN KENYA
Am J Trop Med Hyg, April 1, 2003; 68(90040): 44 - 49.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
F. O. TER KUILE, D. J. TERLOUW, S. K. KARIUKI, P. A. PHILLIPS-HOWARD, L. B. MIREL, W. A. HAWLEY, J. F. FRIEDMAN, Y. P. SHI, M. S. KOLCZAK, A. A. LAL, et al.
IMPACT OF PERMETHRIN-TREATED BED NETS ON MALARIA, ANEMIA, AND GROWTH IN INFANTS IN AN AREA OF INTENSE PERENNIAL MALARIA TRANSMISSION IN WESTERN KENYA
Am J Trop Med Hyg, April 1, 2003; 68(90040): 68 - 77.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
J. A. ALAII, H. W. VAN DEN BORNE, S. P. KACHUR, H. MWENESI, J. M. VULULE, W. A. HAWLEY, M. I. MELTZER, B. L. NAHLEN, and P. A. PHILLIPS-HOWARD
PERCEPTIONS OF BED NETS AND MALARIA PREVENTION BEFORE AND AFTER A RANDOMIZED CONTROLLED TRIAL OF PERMETHRIN-TREATED BED NETS IN WESTERN KENYA
Am J Trop Med Hyg, April 1, 2003; 68(90040): 142 - 148.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
V. WISEMAN, W. A. HAWLEY, F. O. TER KUILE, P. A. PHILLIPS-HOWARD, J. M. VULULE, B. L. NAHLEN, and J. MILLS
THE COST-EFFECTIVENESS OF PERMETHRIN-TREATED BED NETS IN AN AREA OF INTENSE MALARIA TRANSMISSION IN WESTERN KENYA
Am J Trop Med Hyg, April 1, 2003; 68(90040): 161 - 167.
[Abstract] [Full Text] [PDF]

Home page
 Am J Trop Med HygHome page
W. A. HAWLEY, F. O. TER KUILE, R. S. STEKETEE, B. L. NAHLEN, D. J. TERLOUW, J. E. GIMNIG, Y. P. SHI, J. M. VULULE, J. A. ALAII, A. W. HIGHTOWER, et al.
IMPLICATIONS OF THE WESTERN KENYA PERMETHRIN-TREATED BED NET STUDY FOR POLICY, PROGRAM IMPLEMENTATION, AND FUTURE RESEARCH
Am J Trop Med Hyg, April 1, 2003; 68(90040): 168 - 173.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (13)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by PHILLIPS-HOWARD, P. A.
Right arrow Articles by HAWLEY, W. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by PHILLIPS-HOWARD, P. A.
Right arrow Articles by HAWLEY, W. A.
Related Collections
Right arrow Epidemiology
Right arrow Helicobacter
Right arrow Malaria
Right arrow Medical Entomology

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS