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Piperonyl butoxide (PBO) combined with pyrethroids in long‐lasting insecticidal nets (LLINs) to prevent malaria in Africa

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References

Additional references

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Table 1. WHOPES classification

WHOPES Phase

Definition

WHOPES Phase I. Laboratory bioassays

Cone bioassays: these are studies that are conducted in the laboratory setting and use standard WHO protocols (WHOPES 2013, Section 2.2.1), where mosquitoes are exposed to a suitable LLIN (treated intervention or untreated control) for three minutes using a standard plastic WHO cone. Following net exposure, mosquitoes are transferred to a holding container and maintained on a sugar solution diet while entomological outcomes (mosquitoes knocked down one hour post‐exposure, and mosquito mortality 24 hours post‐exposure) are measured.

Tunnel tests: these are studies conducted in the laboratory setting that use standard WHO protocols (WHOPES 2013, Section 2.2.2). Mosquitoes are released into a glass tunnel covered at each end with untreated netting. The intervention or control LLIN net sample is placed one‐third down the length of the tunnel and the net contains nine holes that enable mosquitoes to pass through. A suitable bait is immobilized in the shorter section of the tunnel where it is available for mosquito biting. Mosquitoes are released into the opposite end of the tunnel and must make contact with the net and locate holes before being able to feed on the bait. After 12 to 15 hours, mosquitoes are removed from both sections of the tunnel and entomological outcomes (the number of mosquitoes in each section, mortality, and blood‐feeding inhibition at the end of the assay and 24 hours post‐exposure) are recorded.

Wire‐ball bioassays: these are studies conducted in the laboratory setting where mosquitoes are introduced into a wire‐ball frame that has been covered with either the intervention or control LLIN. Mosquitoes are exposed for three minutes, after which they are transferred to a holding container and entomological outcomes (mosquitoes knocked down one hour post‐exposure, and mosquito mortality 24 hours post‐exposure) are measured.

WHOPES Phase II. Experimental hut trials

WHOPES Phase II experimental hut trials are field trial studies conducted in Africa where wild mosquito populations or local colonized populations are evaluated. Volunteers or livestock sleep in experimental huts under a purposefully holed LLIN, with one person or animal per hut. Huts are designed to resemble local housing based on a West or East African design (WHOPES 2013; Section 3.3.1‐2). However they have identical design features, such as eave gaps or entry slits to allow mosquitoes to enter, and exit traps to capture exiting mosquitoes. LLINs and volunteers are randomly allocated to huts and rotated in a Latin square to avoid bias, with huts cleaned between rotations to avoid contamination. Several nets, including an untreated control net, can be tested at the same time. Dead and alive mosquitoes are collected each morning from inside the net, inside the hut, and inside the exit traps. They are then scored as either blood‐fed or non‐blood‐fed, and either alive or dead, and live mosquitoes are maintained for a further 24 hours to assess delayed mosquito mortality.

WHOPES Phase III. Village trials

WHOPES Phase III village trials are village trials conducted in Africa where wild mosquito populations are evaluated. Villages chosen to be included in the study are similar in terms of size, housing structure, location, and the data available on the insecticide resistance status of the local malaria vectors. Households are assigned either conventional LLINs or PBO‐LLINs. Randomization can be at the household or village level. Adult mosquitoes are collected from the study houses and mosquito density is measured. An indication of malaria transmission is measured in the study sites either by recording infections in mosquitoes, malaria prevalence, or malaria incidence.

Figures and Tables -
Table 1. WHOPES classification
Table 2. WHO‐recommended LLINs

Product name

Product type

Status of WHO recommendation

DawaPlus 2.0

Deltamethrin coated on polyester

Interim

DawaPlus 3.0

Combination of deltamethrin coated onto polyester (side panels), and deltamethrin and PBO incorporated into polyester (roof)

Interim

DawaPlus 4.0

Deltamethrin and PBO incorporated into polyester

Interim

Duranet

Alpha‐cypermethrin incorporated into polyethylene

Full

Interceptor

Alpha‐cypermethrin coated on polyester

Full

LifeNet

Deltamethrin incorporated into polypropylene

Interim

MAGNet

Alpha‐cypermethrin incorporated into polyethylene

Full

MiraNet

Alpha‐cypermethrin incorporated into polyethylene

Interim

Olyset Net

Permethrin incorporated into polyethylene

Full

Olyset Plus

Permethrin and PBO incorporated into polyethylene

Interim

Panda Net 2.0

Deltamethrin incorporated into polyethylene

Interim

PermaNet 2.0

Deltamethrin coated on polyester

Full

PermaNet 3.0

Combination of deltamethrin coated on polyester with strengthened border (side panels), and deltamethrin and PBO incorporated into polyethylene (roof)

Interim

Royal Sentry

Alpha‐cypermethrin incorporated into polyethylene

Full

SafeNet

Alpha‐cypermethrin coated on polyester

Full

Veeralin

Alpha‐cypermethrin and PBO incorporated into polyethylene

Interim

Yahe

Deltamethrin coated on polyester

Interim

Yorkool

Deltamethrin coated on polyester

Full

Abbreviations: LLIN: long‐lasting insecticidal net; WHO: World Health Organization.

Figures and Tables -
Table 2. WHO‐recommended LLINs
Table 3. WHO‐recommended insecticide products for treatment of mosquito nets for malaria vector control

Insecticide

Formulation1

Dosage2

Alpha‐cypermethrin

SC 10%

20 to 40

Cyfluthrin

EW 5%

50

Deltamethrin

SC 1%
WT 25%
WT 25% + binder3

15 to 25

Etofenprox

EW 10%

200

Lambda‐cyhalothrin

CS 2.5%

10 to 15

Permethrin

EC 10%

200 to 500

1Abbreviations: EC: emulsifiable concentrate; EW: emulsion, oil in water; CS: capsule suspension; SC: suspension concentrate; WT: water dispersible tablet.
2Active ingredient/netting (mg/m²).
3K‐O TAB 1‐2‐3.

Figures and Tables -
Table 3. WHO‐recommended insecticide products for treatment of mosquito nets for malaria vector control
Table 4. Definition of resistance level

Outcome

Confirmed resistance

Suspected resistance

Susceptible

Unclassified

WHO mosquito mortality

< 90%

90% to 97 %

98% to 100%

Unknown

CDC knock‐down

< 90%

80% to 97%

98% to 100%

Unknown

Abbreviations: CDC: Centers for Disease Control and Prevention; WHO: World Health Organization.

Definition of resistance level based on mosquito mortality (%) after exposure to insecticide in a WHO diagnostic dose assay (WHO mosquito mortality), or a CDC bottle bioassay (CDC knock‐down) using the methodology, diagnostic doses, and diagnostic times recommended by each test respectively.

Figures and Tables -
Table 4. Definition of resistance level
Table 5. Stratification of resistance level

Outcome

Low

Moderate

High

Unclassified

Mosquito mortality1

61% to 90%

31% to 60%

< 30%

Unknown

124‐hour post‐exposure mortality (%).

Figures and Tables -
Table 5. Stratification of resistance level
Table 6. Study inclusion screening form

Criteria

Assessment

Comments

Yes

No

Unclear

Mosquito population

Did the study test Anopheles gambiae complex or Anopheles funestus group mosquitoes?

State mosquito species

Were a minimum of 50 mosquitoes tested per study arm?

Intervention

Did the study include an long‐lasting insecticidal net (LLIN) or insecticide treated net (ITN)?

State net LLIN or ITN

Was the intervention net either of the following?

  • A piperonyl butoxide (PBO) LLIN which received a minimum of interim World Health Organization (WHO) approval.

  • An ITN impregnated with WHO‐recommended dose of pyrethroid + PBO.

State net type

Was the control net either of the following?

  • A pyrethroid LLIN of the same fabric impregnated with the same insecticide and dose as intervention net (objective 1).

  • A pyrethroid LLIN impregnated with the same insecticide at any dose (objective 2 (a and b)).

State which objective study meets

Study design

Was the study one of the following?

  • Laboratory bioassay (cone, tunnel, ball)

  • Experimental hut study

  • Village trial

State study type

For laboratory bioassay. Did the study use standard‐WHO protocol?

For experimental hut study and village trial. Was the study conducted in Africa?

State country

Outcome

Did the study include at least one of the following outcome measures?

  • Mortality.

  • Blood feeding.

  • Sporozoite rate.

  • Not passed through net.

  • Deterrence.

  • Exophily.

  • Mosquito density.

  • Parity rate.

Decision

Is the study eligible for inclusion?

State reason(s) for exclusion

Discuss with authors

Figures and Tables -
Table 6. Study inclusion screening form