Malaria transmission dynamics surrounding the first nationwide long-lasting insecticidal net distribution in Papua New Guinea

Abstract

Background: The major malaria vectors of Papua New Guinea exhibit heterogeneities in distribution, biting behaviour and malaria infection levels. Long-lasting, insecticide-treated nets (LLINs), distributed as part of the National Malaria Control Programme, are the primary intervention targeting malaria transmission. This study evaluated the impact of LLINs on anopheline density, species composition, feeding behaviour, and malaria transmission.

Methods: Mosquitoes were collected by human landing catch in 11 villages from East Sepik Province and Madang Province. Mosquitoes were collected for 3 years (1 year before distribution and 2 years after), and assayed to determine mosquito species and Plasmodium spp. infection prevalence. The influence of weather conditions and the presence of people and animals on biting density was determined. Determinants of biting density and sporozoite prevalence were analysed by generalized estimating equations (GEE).

Results: Mosquito biting rates and entomological inoculation rates decreased significantly after the distribution. Plasmodium falciparum and P. vivax sporozoite prevalence decreased in year 2, but increased in year 3, suggesting the likelihood of resurgence in transmission if low biting rates are not maintained. An earlier shift in the median biting time of Anopheles punctulatus and An. farauti s.s. was observed. However, this was not accompanied by an increase in the proportion of infective bites occurring before 2200 hours. A change in species composition was observed, which resulted in dominance of An. punctulatus in Dreikikir region, but a decrease in An. punctulatus in the Madang region. When controlling for village and study year, An. farauti s.s., An. koliensis and An. punctulatus were equally likely to carry P. vivax sporozoites. However, An. punctulatus was significantly more likely than An. farauti s.s. (OR 0.14; p = 0.007) or An. koliensis (OR 0.27; p < 0.001) to carry P. falciparum sporozoites.

Conclusions: LLINs had a significant impact on malaria transmission, despite exophagic and crepuscular feeding behaviours of dominant vectors. Changes in species composition and feeding behaviour were observed, but their epidemiological significance will depend on their durability over time.

Fig. 1

Map of study villages. Madang coastal (purple), Madang inland (blue) and Dreikikir (red) field sites

Fig. 2

Madang region monthly rainfall and biting rates. Madang airport monthly rainfall (a) and mean nightly man biting rates in (b) coastal Madang (n = 5093), (c) inland Madang (n = 2804). The arrows represent LLIN distribution dates in the community. Each village had a similar sampling effort between years 1 and 2 (August 2008–July 2010). However, in year 3 (August 2010–November 2011), only Matukar and Dimer were sampled

Fig. 3

Species composition before and after LLIN distribution. PCR confirmed anopheline species composition for Matukar (n = 1182 pre-LLIN, n = 430 post-LLIN), Dimer (n = 1417 pre-LLIN, n = 272 post-LLIN), Yauatong (n = 722 pre-LLIN, n = 324 post-LLIN), Nanaha (n = 738 pre-LLIN, n = 83 post-LLIN)

Fig. 4

Biting time before and after LLIN distribution. Boxes indicate first to third quartile and median hours of biting activity. Whiskers represent fifth to 95th percentiles. Year 1 was before LLIN distribution and years 2 and 3 were after. Boxes carrying the same letter were not statistically different (Bonferroni adjusted alpha = 0.007)) when comparing median biting times using Mann–Whitney U tests. Albulum year 1 n = 874, year 2 n = 383; Peneng year 1 n = 715, year 2 = 103; Ngahmbule year 1 n = 596, year 2 = 100; Yauatong year 1 n = 2818, year 2 n = 672, year 3 n = 464; Matukar year 1 n = 2187, year 2 n = 187; Mirap year 1 n = 1191, year 2 n = 328

Fig. 5

Man biting rate and entomological inoculation rate. Panels on the left show mean nightly biting rate (± SEM) in villages from each region. Asterisk indicates villages which experienced a significant reduction between years 1 (pre-LLIN) and 2 or 3 (post LLIN) (Bonferonni adjusted alpha = 0.003). Panels on the right show entomological inoculation rate (infective bites/person/year) with P. falciparum and P. vivax in year 1 (pre-LLIN), 2 and 3 (post-LLIN) for each region

Fig. 6

Plasmodium spp. sporozoite prevalence in dominant anophelines