**4. Residual and outdoor transmission: how much and where?**

In 2012, global malaria transmission was reported as mainly attributable to 51 *Anopheles* species, with an average of about 3 major species per country [68]. Biological factors that determine whether a species becomes a major local threat are its competence for transmitting human malaria parasites, its anthropophilic *versus* zoophilic preference, and its abundance in relation to its ability to multiply, survive, and compete for resources with other *Anopheles* species. The third of these factors is regulated by the ecosystem's carrying capacity for potent vectors depending on their ecological niches [69]. Species of several *Anopheles* complexes are either major or secondary malaria vectors depending on their geographical range of distribution [70]. The peculiarity of these sibling species within a complex is that they cannot be distinguished using morphological criteria. However, several Asian malaria vectors within the Dirus, Leucosphyrus, Minimus, Maculatus, Culicifacies, Sundaicus, Subpictus complexes or groups show similar morphological characteristics, different ecological traits and vector competencies and overlapping geographical distribution with other vectors and non-vectors [70, 85, 92]. As some of these sibling species occur sympatrically and differ in their ability to transmit malaria and in their behaviour, the use of molecular tools to differentiate the vectors from the non-vectors is essential to target the correct species in vector control programs.

Malaria vector control relies largely on Long-Lasting Insecticidal Nets (LLINs) and Indoor Residual Spraying (IRS), along with Larval Source Management (LSM) as a supplementary measure appropriate in certain settings. These core interventions are highly efficacious for control of susceptible malaria vectors when implemented at universal coverage; LLINs and IRS contributed to a 48% reduction in malaria infection prevalence and 47% reduction in mortality worldwide between 2000 and 2013 [71]. However, malaria transmission can persist even when LLINs and/or IRS are effectively implemented and malaria vectors are susceptible to the insecticides used. This may be due to a combination of vector and human behaviour and bionomical characteristics, which compromise inadequate control measures against early and/or outdoor biting mosquitoes, and human activity away from protected houses or places at peak biting times. With current efforts focusing on malaria elimination [72], there is considerable interest in vector behaviour that is not influenced by application of core interventions (i.e., conventional IRS and Insecticide Treated Nets (ITNs)), such as feeding earlier and resting outdoors when humans are not protected. For example, an unprecedented malaria outbreak, related to illegal rosewood logging, occurred in 2014 with a seven-fold increase of cases in 1 year in Ubon Ratchathani Province, Northeastern Thailand [73]. Insecticide-susceptible and exophilic *An. dirus s.l.* were collected from a forested area in Ban Pakla and Chong Ta Ou Thai border control station, including *An. maculatus s.l*. collected remote villages with potentially low insecticide pressure [73]. These susceptible vector species are less amenable to control interventions due to their behaviour and their interactions with humans contribute to persistent residual transmission and represent barrier to success [74, 75].

minorities, or in conflict areas, all of which can hinder access to the public health system. Another key concern is to restrict or mitigate the widespread dispersal of parasites by these

Human and Simian Malaria in the Greater Mekong Subregion and Challenges for Elimination

Just as forest workers often stay in the forests for several days and sleep exposed to vectors [84], rubber tappers also work in plantations at night with higher likelihoods of being bitten by *Anopheles* mosquitoes, in particular vector species of the Dirus Complex [3, 85]; they all have poor access to healthcare services [86]. Plantation work is seasonal, and manpower is often composed of highly mobile seasonal migrants, but little is known about their patterns of movement. More malaria infections were observed in people with temporary labour positions and plantation workers at the Thailand-Myanmar border [87], but this was not confirmed due to a very high proportion of the study participants opting to perform forest or field activities, and a very low number opting to work in rubber plantation [59]. Many migrants that arrive for rubber tapping settle beyond the harvest season [87] and go on to work on other cash crops (e.g., rice,

**Ecotype % Access to LLIN % Use of** 

81.8% (Pursat)

Hamletsb 100% 75–95% Farm huts NA NA

Farm huts NA 62.7%c Forest NA 25%c

Forest plots & villages

Way to the forest

Forest plots 69.2% (Pailin);

**LLIN**

workers)

66.3% (forest workers)

NA NA Before 19:00 h 13%

68.4% (Ratanakiri) 70.7% (forest

Village NA 85% Before 22:00 h 45%

Forest plots NA 53% Before 21:00 h 64%

Village<sup>a</sup> 78% 80% Before 21:00 h and

Village 78% 95% Before 20:00 and 05:00 h

**Table 1.** Overview of residual malaria parasite transmission (RMT) in various ecological settings in Greater Mekong

**Proportion of**  *Anopheles* **bites or infective bites in relation to sleeping** 

Before 22:00 h 29%

(bites of *An maculatus)*

(bites only)

(bites only)

26% farm huts 37% forest

05:00 h 20.0% Suan Oi 33.7% Pha Man 37.6% farm huts

After 22:00 h 71% [53, 102]

http://dx.doi.org/10.5772/intechopen.76901

**Reference**

103

[83]

[82]

**time**

elusive population groups.

**District, province,** 

Eastern region: Borkeo & O'Chum districts, Rattanakiri Province; Western region: Pailin & Pursat Provinces; Cambodia

Ma Noi and Phuoc Binh communes, Ninh Thuan Province, south-central

Tha Song Yang, Tak Province, Thailand

Son Thai commune, Khan Hoa Province, central

Pha Man & Komonae hamlets, Thailand [82].

**country**

Vietnam

Vietnam

a

b

c

NA: not available.

Suan Oi village.

Subregion.

Regular use of LLIN.

From a geographical perspective, residual malaria parasite transmission has been reported across numerous transmission settings, even with good access and usage of LLINs or wellimplemented IRS [76–80]. From the programmatic perspective, residual malaria transmission (RMT) is defined as the persistent malaria transmission that occurs once universal coverage of LLINs and maximal coverage of IRS have been achieved. Identification and elucidation of RMT requires the following pre-conditions: (a) comprehensive and up-to-date LLIN and IRS coverage data, where coverage is defined as 100% access and usage of ITN/LLIN or IRS [81]; (b) outdoor human activity or behaviour to allow identification of outdoor sites and "gaps" in protection, not only before sleeping time, but also for people that remain outdoors during the night. In many countries of the GMS, LLIN and IRS distribution data are sparse or not readily available. Where these data are available, it is often compiled at a relatively high administrative level, such as district or province. Malaria transmission at the community level can vary considerably within a small area and thus to investigate RMT at this level, LLIN and IRS coverage data by village are necessary. Furthermore, LLIN coverage figures quoted at the province or district level often do not match the actual situation at the community level, perhaps due to inequities in distribution, inaccurate population estimates, and calculation of procurement need, limited replacement of outdated and damaged LLIN; the outcome of which could lead to an underestimation of the magnitude of RMT.

As malaria is becoming more and more restricted to hard-to-reach population groups, alternative or adapted control strategies are required who are somehow marginalised, poor, on the fringes of the public health system, living in dwellings that are either very close to the forest or harbour people who are exposed to the forest through their occupation (e.g., development sites and seasonal labour areas) or mobility behaviour. As shown in **Table 1**, the risk of RMT in the malaria foci is spread over the entire night, from dusk-to-dawn, requiring a combination of complementary vector control measures, such as long-lasting insecticide hammock nets (LLIHN) that can be used during different periods of the night. However, the use of LLIHN, single LLIN/ITN or topical repellents in the field may not be acceptable due to cultural and linguistic barriers of ethnic minorities and MMPs for which specific acceptability studies should be conducted to guide the feasibility of these vector control tools.

Another driver of RMT is mega and micro-development projects impacting the forest or creating new conditions suitable for vector species, and often attracting a substantial workforce from various horizons across borders and cultural boundaries [6]. Their sleeping or residential places can have additional vulnerabilities if they are remote, comprising mainly ethnic minorities, or in conflict areas, all of which can hinder access to the public health system. Another key concern is to restrict or mitigate the widespread dispersal of parasites by these elusive population groups.

Just as forest workers often stay in the forests for several days and sleep exposed to vectors [84], rubber tappers also work in plantations at night with higher likelihoods of being bitten by *Anopheles* mosquitoes, in particular vector species of the Dirus Complex [3, 85]; they all have poor access to healthcare services [86]. Plantation work is seasonal, and manpower is often composed of highly mobile seasonal migrants, but little is known about their patterns of movement. More malaria infections were observed in people with temporary labour positions and plantation workers at the Thailand-Myanmar border [87], but this was not confirmed due to a very high proportion of the study participants opting to perform forest or field activities, and a very low number opting to work in rubber plantation [59]. Many migrants that arrive for rubber tapping settle beyond the harvest season [87] and go on to work on other cash crops (e.g., rice,


a

at peak biting times. With current efforts focusing on malaria elimination [72], there is considerable interest in vector behaviour that is not influenced by application of core interventions (i.e., conventional IRS and Insecticide Treated Nets (ITNs)), such as feeding earlier and resting outdoors when humans are not protected. For example, an unprecedented malaria outbreak, related to illegal rosewood logging, occurred in 2014 with a seven-fold increase of cases in 1 year in Ubon Ratchathani Province, Northeastern Thailand [73]. Insecticide-susceptible and exophilic *An. dirus s.l.* were collected from a forested area in Ban Pakla and Chong Ta Ou Thai border control station, including *An. maculatus s.l*. collected remote villages with potentially low insecticide pressure [73]. These susceptible vector species are less amenable to control interventions due to their behaviour and their interactions with humans contribute to persis-

From a geographical perspective, residual malaria parasite transmission has been reported across numerous transmission settings, even with good access and usage of LLINs or wellimplemented IRS [76–80]. From the programmatic perspective, residual malaria transmission (RMT) is defined as the persistent malaria transmission that occurs once universal coverage of LLINs and maximal coverage of IRS have been achieved. Identification and elucidation of RMT requires the following pre-conditions: (a) comprehensive and up-to-date LLIN and IRS coverage data, where coverage is defined as 100% access and usage of ITN/LLIN or IRS [81]; (b) outdoor human activity or behaviour to allow identification of outdoor sites and "gaps" in protection, not only before sleeping time, but also for people that remain outdoors during the night. In many countries of the GMS, LLIN and IRS distribution data are sparse or not readily available. Where these data are available, it is often compiled at a relatively high administrative level, such as district or province. Malaria transmission at the community level can vary considerably within a small area and thus to investigate RMT at this level, LLIN and IRS coverage data by village are necessary. Furthermore, LLIN coverage figures quoted at the province or district level often do not match the actual situation at the community level, perhaps due to inequities in distribution, inaccurate population estimates, and calculation of procurement need, limited replacement of outdated and damaged LLIN; the outcome of

As malaria is becoming more and more restricted to hard-to-reach population groups, alternative or adapted control strategies are required who are somehow marginalised, poor, on the fringes of the public health system, living in dwellings that are either very close to the forest or harbour people who are exposed to the forest through their occupation (e.g., development sites and seasonal labour areas) or mobility behaviour. As shown in **Table 1**, the risk of RMT in the malaria foci is spread over the entire night, from dusk-to-dawn, requiring a combination of complementary vector control measures, such as long-lasting insecticide hammock nets (LLIHN) that can be used during different periods of the night. However, the use of LLIHN, single LLIN/ITN or topical repellents in the field may not be acceptable due to cultural and linguistic barriers of ethnic minorities and MMPs for which specific acceptability

Another driver of RMT is mega and micro-development projects impacting the forest or creating new conditions suitable for vector species, and often attracting a substantial workforce from various horizons across borders and cultural boundaries [6]. Their sleeping or residential places can have additional vulnerabilities if they are remote, comprising mainly ethnic

studies should be conducted to guide the feasibility of these vector control tools.

tent residual transmission and represent barrier to success [74, 75].

102 Towards Malaria Elimination - A Leap Forward

which could lead to an underestimation of the magnitude of RMT.

Suan Oi village. b

Pha Man & Komonae hamlets, Thailand [82].

c Regular use of LLIN.

**Table 1.** Overview of residual malaria parasite transmission (RMT) in various ecological settings in Greater Mekong Subregion.

cassava, fruit orchards). On return to their usual settlements, they contribute to the spread of malaria within and across international borders [41, 43]. By creating hot-spots of malaria and disproportionately affecting people with certain high-risk occupations [86, 89], residual transmission under these circumstances has so far hindered progress towards elimination.
