Table 2.
Review of Determinants of Residual Malaria Transmission in Cambodia, Lao People’s Democratic Republic, Myanmar, Thailand, Vietnam, Papua New Guinea, and the Solomon Islands
| Location and References | Ecotype, Annual Parasite Incidence (per 1000) or Malaria Prevalence, % | Vector Control | Human-Vector Interaction | |||||
|---|---|---|---|---|---|---|---|---|
| Access to ITN or LLIHN, % | Use of ITN or LLIHN, % | IRS coverage, % | Human Behavior Methods and Information Collected | Entomological Methods | Timing of Entomology and Human Behavior Data Collection | Human Exposure to Malaria Vectors | ||
| Cambodia: Incardona et al (2007) [61]; Gryseels et al (2015) [19]; Durnez et al (2013 [40] and 2018 [62]) | Forest plots and villages in Eastern region: Borkeo and O’Chum districts, Rattanakiri Province; ……………. Forest plots in Western region: Pailin province |
LLIN ownership: 98.5% (Gryseels et al [19]); 68.4% (Rattanakiri); CMS for Rattanakiria: 39.4 (2007), 63.7 (2010), and 99.3% (2013) …………… 69.2% (Pailin); 81.8% (Pursat) CMS for Pailina: 38% (2007), 67.8% (2010) and 100% (2013) |
70.7% (Forest workers) (Durnez et al [62]); 79.1% reported, 69.5% observed (Gryseels et al [19]); 95% (Durnez et al [62]) …………. 66.3% (Forest workers) |
ND | In-depth interviews and participant observations.in Ratanakiri Province; CMS: households interviews using pretested questionnaires | Outdoor HLC in 2 intervention and 2 control villages; from 1700 to 2200 h, 1700 to 0800 h, and 1900 to 0600 h |
Rattanakiri—survey 1 (4 surveys): July–August 2009, July–November 2010, July–August 2011; survey 2 (8 surveys) every 2 mo between April and October 2012 and 2013 | Early human-biting proportion of Anopheles dirus s.l. in villages: 39%–48% and forest: 24%–26% (Pursat); Anopheles minimus s.l./Anopheles aconitus and Anopheles maculatus s.l.: 54.4% and 56.6% (in Rattanakiri); 26.9% and 32.9% (villages in Pailin and west Pursa), respectively; EIR before 2200 h: 0.52 |
| Xieng-Ngeun and Nane districts, Luang Prabang Province, Lao PDR: Tangena (2017) [42] ……………... Laman District, Sekong Province, Lao PDR: Vythilingam et al (2003 [63] and 2005 [64]); Nonaka et al (2010) [65]; Killeen (2014) [8] |
4 Rural habitats: secondary forests, mature rubber plantations, immature rubber plantations, and villages; API: NA, as few malaria cases were imported every year; forest clearing in river valley landscape, fertile plain patterned with a patchwork rice fields and mixed fruit orchards; parasite prevalence: 10.5%–11.8% (2000) |
90% (Ownership) ……………... August 2008: 2 ITNs per household |
NA ……………… August 2008: 94% |
ND ……… ND |
Rapid participatory rural appraisals to study daily and monthly activities of the rubber workers and villagers ……………….. Cross-sectional surveys, questionnaire-based interviews, blood examinations among farmers and household members |
Outdoor human double-net trap (HDN) during day (0600–1800 h) and evening (1800–0600 h) …………………... Indoor and outdoor HLC, 1800–0600 h |
Mosquito collections: 9 mo, from July 2013 to July 2014; human behavior studies: November 2013 and July 2015 …………………….. HLC in August and October 2000, April and October 2001; household surveys March (dry season) and August (rainy season) in 2008 |
Exposure to malaria vectors is 1.3 times (95% CI, 1.2–1.4) higher in forest habitats; lower risk of malaria in rubber plantations at night (OR, 0.9; 95% CI, 0.8–1.0), living and working in rubber plantations (0.6, 0.4–1.0), or staying in villages …………………………………... Staying overnight in farming huts was not associated with an increased risk of malaria infection in settings with ITNs widely used in farming huts (Nonaka et al [65]); proportion of human exposure to A. dirus that occurs indoors for both unprotected residents (πh,i, 0.91) and LLIN users (πh,i,n, 0.4) (Killeen et al [8]) |
| Tha Song Yang District, Tak Province, Thailand: Edwards et al (2019) [44] | 2 Villages, 1 hamlet; API: 148 and 278; parasite prevalence: 0.27%–0.89% | Population access to an ITN: 80.5% | Adults: 79.5%; children aged 5–18 y old: 82.5% | 71.4% | Transect surveys; direct observations and qualitative analysis using GPS trackers | Indoor and outdoor HLC and cow-baited trap 1800–0600 h | Mosquito collections: June–November 2016; Malaria survey: September 2016 |
Indoor exposure 88%–93% for LLIN nonuser and 33%–45% for user Indoor users of LLINs during median sleep time: 45%–67% |
| Son Thai, Khanh Hoa Province, Vietnam: Edwards et al (2019) [45] …………….. Nam Tra My district, Quang Nam Province, Vietnam: Thanh et al (2015) [66] …………….. B Giap Map national forest, Binh Phuoc Province, Vietnam: Son et al (2017) [67]; Ngo et al (2014) [68] |
1 Village, farm huts, forest plots; malaria prevalence: 1.71% (unpublished data, NIMPE) ……………… 4 Villages in a remote forested valley; prevalence: 7.8% (range, 3.9%–10.9%) ……………… Conservation park of rare and precious fauna and flora species, 260 km2, 700 m asl; Pf incidence of ranger population: 479/1000/y |
Population access to ITN in HH: 91.5% ……………... % households with netsb: 23.3%; % HH with 1–2 persons per net: 6% …………….. NA |
Farm huts: 44.4%; forest: 12.1%; regular use in farm huts: 72.7%; forest: 25% ……………… ND ……………… All rangers tend to sleep in hammocks with or without bed net |
2.9% ……… Regular IRS due to unpopularity of bed nets ……… NA |
Transect surveys; direct observations and in-depth interviews; GPS trackers; record time sleep and wake-up time ……………… Malaria survey and interviews on the different outdoor activities in and outside the community, sleeping habits, and malaria prevention measures ……………….. ND; feasibility study of malaria prophylaxis |
Indoor and outdoor HLC, 1800– 0600 h; after July 2016: 1600–0600 h; cow-baited net trap: 1800–0600 h …………………... ND ………………….. Indoor CDC light traps; outdoor and indoor HLC from 1800 to 0600 h |
Mosquito collections: June–November 2016 survey; September 2016 ……………………... No entomological surveys …………………… Parasitological and clinical surveys; mosquito collections: May–September 2016 |
Outdoor biting in the forest and indoor biting at the farm hut were highest during 20:00–21:00 h; 48% of biting by mosquitoes occurred before 9 PM in the farm huts: 45% of A. dirus (s.l.) and 100% of A. maculatus (s.l.) biting) …………………………………... ND ………………………………… A. dirus (84%) was most prevalent and preferentially anthropophilic, biting outdoors before 2200 h (similar to Trung et al [2005] [69]); exposure not estimated |
| Ma Noi and Phuoc Binh communes, Ninh Thuan Province, Vietnam: Erhart et al (2005) [70]; Van Bortel et al (2010) [71]; Thanh et al (2019) [66]; Grietens et al (2010 [72] and 2012 [73]) …………….. Phuoc Chien Commune, Vietnam: Sanh et al (2008) [74] |
Ra-Glai villagers along the road with a second home at their slash-and-burn fields in the forest Parasite prevalence: 13.3% ……………… Phuoc Chien commune: malaria positivity rate: 32.1% (2003) and 15.5% (2006) |
Median coverage: 2.5 people per bed net; December 2004: 7000 LLIHNs individually distributed to all residents (≥10 y old) in intervention clusters for 70% coverage of intervention population ………….. Households with ≥1ITN: central region, 18.9%; south, 8.9% (DHS [83]) |
Bed net use in village: 84.6%; in forest fields: 52.9%; overall LLIHN use at night in village: 56%; in forest fields: 20.7% (evening) and 6.4% (at night) ……………… Children <5 y old who slept under an ITN the previous night: 25.1% (central) and 7.4% (south) (DHS [83]) |
NA ……… Remote garden plots were not sprayed |
Mixed-methods study integrating qualitative data from focused ethnography and quantitative data during malariometric cross-sectional survey ……………… ND entomological and mass blood surveys |
Indoor and outdoor HLC, 1800–0600 h: locations of collections: in villages (2 houses), forest (2 sites), and “on the way” (in between) …………………... Phuoc Chien commune: outdoor HLC and indoor CDC light traps from 1800 to 0600 h |
1st survey: November 2004; 2nd survey: October and November 2005; 3rd survey: October–November 2006 …………………….. Parasitological and entomological surveys in Phuoc commune: September–October 2006 |
Highest biting activity of Anopheles vectors occur in the evening, with 6% of bites by 1900 h, 25% by 2000 h, and 50% before 2200 h; correlating human/mosquito activity patterns with the proportion of people protected by either LLIHNs and/or ITNs, local farmers at the forest fields are exposed to mosquito bites mainly owing to low ITN use; while half (52%) of Ra-glai respondents were asleep by 1900 h, only 58% would regularly be protected by ITNs; among the fraction of people staying out later in forest fields only about 20% were using LLIHNs; comparatively, at villages, both people staying out late and those sleeping were more likely to be protected, respectively by LLIHNs (56%) and ITNs (92%); Phuoc Chien: probable malaria transmission in the garden plots due to presence of A. dirus, a species absent in the village 2 km away |
| Dabhine and Myothugyi areas, Rakhine State, Myanmar: Smithuis et al (2013) [46, 75] | Coastal plain area (without hills or forest, where rice and other crops are cultivated); rice fields and partly forested hills | Complete coverage; approx. 1.6 ITN per child (5000 ITNs distributed in April 1998) | 84% in ITN group; 7% slept in untreated nets in control group | ND | Interview all ITN recipients, during cross-sectional surveys on ITN usage and ITN washing habits | Indoor and outdoor HLC (“HBC”), 1800–0600 h and 1700– 0700 h (3rd survey); cow-baited net trap (night and morning); exit traps; indoor knockdown collections | 1st survey: November 1995 to April 1996; 2nd survey: July 1996 to April 1999; 3rd survey: December 1999 to January 2000 | Biting-risk of 0–4- y-old children in no-net villages was about 61% and 91% compared with average (all age groups combined); compared with an average person in a village without ITN, the risk of mosquito bites per infant was 19% and 89%, respectively; proportion of human exposure to mosquitoes indoors for unprotected residents (πh,i): 0.41 (A. epiroticus), 0.48 (A. subpictus), and 0.54 (A. annularis); proportion of human exposure to mosquito that occurs indoors for LLIN users (πh,i,n): 0.06 (A. epiroticus), 0.06 (A. subpictus), 0.07 (A. annularis) (Killeen et al [2014] [8]) |
| Sabah State, Kudat District, Malaysia: Grigg et al (2017) [30]; Chua et al (2019) [48]; William et al (2013 [26] and 2014 [27]); Manin et al (2016) [76] | Paradason, Kudat District, Sabah, East Malaysia API (2011): 14.3 per 1000 ecological; habitats: forest edge, playground: long house, oil palm plantation, and bush shrubs (Chua et al [48]) | Study sites in Timbang Dayang, Limbuak Laut (Banggi), and Paradason (Kudat): 1.65 people per ITN; population access to ITNs in HH: 121% | NA | 100% (128 Houses in 2013; 144 houses in 2014) | Questionnaires and household surveys for case-control study using demographic, social, behavioral, household, and environmental variables associated with malaria risk | Outdoor HLC: 1800–0600 h | Mosquito collections: 14 mo. from October 2013 to December 2014 | Sleeping outside was an independent acquisition risk factor (aOR, 3.61; 95% CI, 1.48–8·85; P = .005), as was a history of recent travel (2.48; 1.45–4.23; P = .001); sleeping outside in the forest or plantation during a trip was not significant; use of a bed net remained unassociated with protection; a history of activities in the forest were not significantly associated with increased Plasmodium knowlesi malaria risk, or any other specific recreational activities such as hunting; outdoor residual spraying of houses reduced the simian vector population and simian malaria transmission (Rohani et al [2020] [49]) |
| Papua New Guinea: Rodriguez‑Rodriguez et al (2019) [50]; Kattenberg et al (2020) [52]; Hetzel et al (2016) [77]; Reimer et al (2016 [78] and 2013 [79]) | Coastal villages with coconut plantations, swamps inland foothills with thick vegetation; incidence: 20–115 per 1000 (in 2010) to 1–47 per 1000 (in 2014) |
Momase: 39.4 (2008–2009), 75.4 (2010–2011), and 79.0 (2016–2017); Islands: 44.0(2008–2009), 98.3 (2010–2011), 77.1 (2016–2017); access to an LLIN (2016); Madang: 79.8; East Sepik Province: 71.9%; New Ireland: 78.7% |
Momase: 47.0 (2008–2009), 48.4 (2010–2011), 70.2 (2016–2017); Islands: 25.4 (2008–2009), 40.0 (2010–2011), 38.5 (2016–2017); Sausi: 90%–100%; Dreikikir: 77%–86% and 79% (3-mo interval); Madang: 54% and 79% (3-y interval) (Reimer et al [78]) |
Nil | Hourly observations on number of animals and additional people present in hamlet (Reimer et al [78]) |
Outdoor HLC 1700–0600 h | Mosquito collections for 1 y before and 1 y after nationwide LLIN distribution; Madang: August 2008 to November 2011; Dreikikir: September 2008 to July 2011 |
Significant decrease in human landing rates in the year after LLIN distribution and remained low through y 3; LLINs may still have a large communal impact if LLIN coverage and usage is high, including individual use and high community LLIN coverage (Hetzel et al [2015] [86]; Reimer et al [78]) Aging of nets, early and outdoor mosquito biting may fuel ongoing transmission [Rodriguez-Rodriguez et al [50] |
| Solomon Islands: Pollard et al (2020) [53]; Russell et al (2016) [80–82] DHS (2015) [83] |
Coastal islands; API: 280 | ≈79.3% approximately | 84% | ≈26.2% | Daily movement diaries, interviews, and direct observations | Indoor and outdoor HLC, 1800–0600 h | Mosquito collections: July 2012 | Almost universal access to and use of LLIN with, only 7% of people were under an LLIN during the 1800–2100-h peak biting period when 76% of Anopheles farauti bites occur; proportion of exposure to mosquito bites on humans occurring indoors (πi): 0.130 ± 0.129. |
| Thailand: Somboon et al (1995) [84] and 1998 [85]) | Forest and forest fringe areas in Mae Sarianp District; Mae Hong Son Province; API (1989): 80.7–279.7 per 1000 (1989) |
ITN coverage: >80%; 2.2–2.7 person s per net |
>90% | IRS suspended from October 1989 until the end of the study | Fortnightly household interviews and observations of human behavior during transmission season | Indoor and outdoor HLC, 1800–0600 h; CDC light traps, cow- or buffalo-baited net trap |
Mosquito collections: monthly May–December 1990 and May–December 1991 | Residential villages, farm huts and forests are sites of transmission; malaria risk for forest activities is 4–6 times higher than other activities and 13 times higher than staying in villages; higher biting density of vectors at the farm huts but similar inoculation rates between villages and farm huts; community-wide use of ITNs did not generally reduce the vectorial capacity of vectors in this area, probably because of the biting behavior of the mosquitoes |
Abbreviations: aOR, adjusted OR; API, Annual parasite incidence; ASL, above sea level; CDC, Centers for Disease Control and Prevention; CI, confidence interval; CMS, Cambodia malaria survey; DHS, Demographic and Health Survey; EIR, entomological inoculation rate; GPS, Global Positioning System; HBC, human biting collections; HDN, Human double net; HH, Household; HLC: human landing collection; IRS, indoor residual spray; ITN, insecticide-treated bed net; LLIHN, long-lasting insecticidal hammock net; LLIN, long-lasting insecticidal net; NA, Not available; ND, not done; NIMPE, Vietnam National Institute of Malariology, Parasitology and Entomology; OR, odds ratio; PDR, People’s Democratic Republic; RMT, residual malaria transmission; PF, Plasmodium falicparium; s.l., sensu lato.
aOwnership is defined as having possession of ≥1 ITN
bThe ownership of nets was reported without indication of age, condition or whether they were insecticide treated or not