Highlights
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The use of, and population adherence to, control measures impact malaria transmission.
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Good knowledge of malaria and control measures was observed.
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The majority of heads of households visited health centres in cases of suspected malaria.
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Malaria prevalence was high and varied with age, house type, and sleeping time.
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Malaria transmission persists, despite the use of control tools by the population.
Keywords: KAP, malaria prevalence, malaria determinants, forested area, Cameroon
Abbreviations: HoH, head of household; LLIN, long-lasting insecticidal net; IRS, indoor residual spraying; WHO, World Health Organization; MoH, Ministry of Health. PBO, piperonyl butoxide; mRDT, malaria rapid diagnostic test; KAP, knowledge, attitude, and practice; NMCP, National Malaria Control Program
Abstract
Objective
This study assessed knowledge, attitudes, and practices (KAP) regarding malaria among communities living in the equatorial forest region of south Cameroon.
Methods
The study was conducted in Olama and Nyabessan. Interviews were undertaken using a semi-structured questionnaire for data collection on KAP, while malaria rapid diagnostic testing, using SD BIOLINE kits, was employed for malaria parasite detection.
Results
In total, 186 heads of households (HoH), comprising 105 (56.45%) males and 81 (43.45%) females, were interviewed. The majority of HoH demonstrated good knowledge of malaria (86.56%; n = 161) and control measures, with a high proportion of long-lasting insecticidal net (LLIN) ownership (96.8%; n = 180). More than two-thirds (81.1%; n = 151) of households owned at least one LLIN for two people. The majority of HoH (85.40%) declared visiting hospitals or clinics in cases of suspected malaria. Malaria parasite prevalence was high in the two study sites (63.9% in Nyabessan and 48.65% in Olama), and varied according to age, house type, and sleeping time.
Conclusion
The study indicated that despite good knowledge of malaria, high possession and utilization of control measures by population, transmission of malaria still persist in the area. The study stress the need for implementing additional control measures to improve the fight against malaria in the area.
Introduction
Malaria remains the most dangerous vector-borne disease in the world, causing high mortality among young children and pregnant women. It is estimated that 229 million new malaria cases were recorded across the world in 2019, leading to 409,000 deaths. Sub-Saharan African countries are the most affected, with 93% of cases and 67% of associated deaths (WHO, 2020). In Cameroon, malaria accounts for over 30% of outpatient visits and is classified as the third-highest cause of mortality in healthcare centres after HIV/AIDS and neonatal infections (PNLP, 2019).
Malaria prevention relies on chemoprevention and vector control, with the mass distribution of bed nets and indoor residual spraying as the primary control measures (Bhatt et al., 2015; Keiser et al., 2005). The deployment of these tools during the last decade has led to a significant reduction in malaria morbidity and mortality across the world (Bayoh et al., 2010; Bhatt et al., 2015; Cook et al., 2018; Finda et al., 2018; Meyers et al., 2016; Meyrowitsch et al., 2011; Mwangangi et al., 2013).
Between 2000 and 2016, Cameroon recorded reductions in the prevalence and mortality of malaria of around 29% and 57%, respectively (WHO, 2015). The regular scaling up of LLINs was the mainstay of this reduction. Between 2014 and 2017, around 20 million nets were distributed in Cameroon (WHO, 2017), increasing the ownership and usership rate in the population. The latest LLIN mass distribution campaign in the country took place in 2019, leading to the distribution of over 15 million pyrethroid-only and pyrethroid + PBO (piperonyl butoxide) bed nets (PNLP, 2021).
Despite progress in the scaling up of LLINs in the country, no significant reduction of malaria mortality and morbidity has been recorded since 2015 (WHO, 2017; WHO, 2018). Several factors, including the rapid expansion of insecticide resistance (Antonio-Nkondjio et al., 2019; Piameu et al., 2021) and changes in vector composition and in the feeding and resting behaviour of Anopheles mosquitoes (Bamou et al., 2018; Moiroux et al., 2012; Mwangangi et al., 2013; Sherrard-Smith et al., 2018) are considered to affect the efficacy of control measures. In addition to human-related factors, such as sleeping time, night-time activities, and time spent outdoors at night, factors such as the state or integrity of LLINs, socioeconomic status, and house type could also influence transmission risk, but the effects of these factors have not been fully assessed (Durnez et al., 2013; Finda et al., 2018; Gryseels et al., 2015; Rodríguez-Rodríguez et al., 2021).
Data on household characteristics and human behaviour could be useful for mapping malaria transmission risk and for improving vector control interventions and malaria control programmes. In the south Cameroon forest region, previous studies have indicated a high diversity of anopheline species, along with high levels of insecticide resistance and different behavioural patterns among mosquito species (Antonio-Nkondjio et al., 2005; Awono-Ambene et al., 2004; Bamou et al., 2021, 2018; Mbakop et al., 2019). However, there is not enough information on the influence of human, household, or house-related factors on exposure to malaria transmission risk. Our study assessed the influence of house characteristics and human-related factors on malaria transmission risk.
Methodology
Ethical considerations
This study received approval from the WHO Ethics Review Committee (WHO ERC), protocol ID ERC.0002666, and from the Cameroon National Ethics Committee for Research on Human Health (CNERSH), under ethical clearance number 2016/01/685/CE/CNERSH/SP. Written informed consent was obtained from the parents/guardians of children during the malaria prevalence surveys, while assent was obtained for participants under 18 years. The Helsinki Declaration's guidance on ethical principles regarding human subjects was followed in this study.
Study sites
The study was conducted in two villages, Olama and Nyabessan, in the equatorial forest region of south Cameroon. Olama (3°24′ N; 11°18’ E) and Nyabessan (2°80′ N; 10°25′ E) are located 65 km and 220 km from Yaoundé, respectively (Figure 1). Olama village is surrounded by the Nyong river and is characterized by high forest cover. It consists of a cluster of traditional houses built with mud. Nyabessan is bordered by the Ntem river and is located near the recently constructed Menve'ele dam. Houses in Nyabessan are constructed in wood and mud. The main activities in both villages are farming and fishing. Malaria is endemic in both localities, with an entomological inoculation rate of about 252 and 48 infective bites per person per year in Nyabessan and Olama, respectively (Bamou et al., 2021, 2018).
Figure 1.
Map of the southern part of Cameroon, showing both study sites.
Sample size
The required sample size was estimated using the Lorentz formula:
considering the proportion of people infected with malaria (p) in the country (30–45%), with 5% error. The minimum sample size was estimated to be about 276 participants, while around 400 were included in the study. The number of HoH included for questionnaire interviews was 186 (93 in each site), representing more than 80% of households.
Study design and data collection
This was a household-based cross-sectional survey. After obtaining administrative authorization and ethical clearance, sampling was carried out randomly in both study sites, with almost all houses visited. Houses where people were absent were revisited. In the presence of the head of household (HoH) or their spouse, or an inhabitant over 18 years of age, the purpose of the study was explained and their willingness to participate in the study requested. People included in this study thus comprised households with informed consent approval. Only the HoH or their spouse, or inhabitants aged over 18 years, were interviewed. For the purpose of malaria diagnostics, in addition to the questionnaire participants, children were included after obtaining consent from their parents.
The door-to-door survey was conducted by well-trained field staff. A well-designed, pre-tested questionnaire was submitted to the HoH in both villages after obtaining their free and informed consent. In cases where the HoH was absent, the spouse or another family member over the age of 18 was interviewed. The questionnaire comprised 30 questions, and was divided into three sections. The first section collected information on sociodemographic characteristics (age, gender, number of family members, and levels of education). The second section addressed the economic status of residents/households (type of cooking fuel, source of income, source of water for domestic use, assets in possession, types of walls and roofs). The last section concerned malaria knowledge (vectors, signs, and symptoms) and control measures, evening activities of residents, and sleeping behaviour (time of sleeping and waking up). Those going to bed before 9 pm were classed as ‘sleep early’, and those going to bed after 9 pm as ‘sleep late’. Those waking up before 6 am were classed as ‘wake up early’ and those waking up after 6 am as ‘wake up late.
Parasitological analysis
In addition to the household survey, malaria rapid diagnostic tests (mRDTs) were performed in households that consented to participate in the study to determine malaria prevalence in the population within the two villages during the dry season (December 2016) and rainy season (November 2017). Parasite screening in blood samples was performed using the SD BIOLINE Malaria Ag. Plasmodium falciparum/Pan rapid diagnostic test kit (Standard Diagnostics, Inc., Republic of Korea), according to the manufacturer's instructions. This targets histidine-rich protein 2 (HRP2) and lactate dehydrogenase (pLDH), and has 98% specificity and 99.5% sensitivity (Tadesse et al., 2016).
Data analysis
The collected data were analysed using SPSS version 20.0. Ages of participants, times of going to bed and times of waking up were categorized. For categorical or qualitative variables, data were presented as frequencies or percentages, while for continuous variables (age) they were presented as means. The chi-squared test was used for comparisons of proportions at the 0.05 significant level. A univariate analysis was also carried out to determine whether any of the prospectively defined independent factors (age, sex, net usage and sleeping behaviour) were significantly associated with malaria prevalence. To assess risk factors, odds ratios as well as their 95% confidence intervals were computed using Medcalc version 20.015 software.
Level of knowledge was assessed by considering answers to two questions regarding (1) the mode of transmission (vector) and (2) malaria symptoms. Participants with correct answers to these two questions (knowledge of the vector and capable of citing at least two symptoms of malaria) were considered to have correct knowledge, while others were considered to have incorrect knowledge.
Results
Background characteristics of the studied population
Interviews were performed in 93 houses in each locality during the study period. The majority of respondents (HoH) were males (56.45%) — 62.40% in Olama and 50.50% in Nyabessan (Table 1). More than half of the respondents/HoH (n = 134; 72.04%) had been educated to at least secondary school level (Figure 1) and were working for the SinoHydro Company constructing roads and finalising the dam project. Livestock ownership was higher in Olama compared with Nyabessan (62% vs 34%) (Table 1). Bedtimes and waking-up times in both villages varied according to age and gender. The majority of the people (HoH and their house members) were found to go to bed after 9 pm (sleeping late behaviour) — 73.5% and 83.5% for Olama and Nyabessan, respectively. Women were more likely to wake up early — before 6 am. Activities keeping people outdoors during the night were cooking for women, selling or drinking with friends for men, and studying for young boys and girls. In Olama, playing or talking with friends in the evening was also recorded.
Table 1.
Data obtained from the heads of households surveyed in Olama and Nyabessan.
| Olama |
Nyabessan |
Total |
||||
|---|---|---|---|---|---|---|
| N | % | N | % | N | % | |
| Gender | ||||||
| Male | 58 | 62.4 | 47 | 50.50 | 105 | 56.45 |
| Female | 35 | 37.6 | 46 | 49.50 | 81 | 43.55 |
| Age (years)# | ||||||
| 18–34 | 30 | 33.71 | 48 | 59.26 | 78 | 45.88 |
| 35–54 | 37 | 41.57 | 27 | 33.33 | 64 | 37.64 |
| > 54 | 22 | 24.72 | 6 | 7.41 | 28 | 16.47 |
| Educational level of household heads | ||||||
| University | 15 | 16.13 | 7 | 7.52 | 22 | 11.83 |
| Secondary | 51 | 54.84 | 61 | 65.60 | 112 | 60.21 |
| Primary | 27 | 29.03 | 20 | 20.51 | 47 | 25.27 |
| None | 0 | 0.00 | 5 | 5.37 | 5 | 2.69 |
| Occupation/source of revenues | ||||||
| Small-scale farming | 66 | 70.96 | 8 | 8.60 | 74 | 39.78 |
| Employment | 11 | 11.82 | 43 | 46.23 | 54 | 29.03 |
| Small-scale business | 16 | 17.20 | 36 | 38.78 | 52 | 27.96 |
| Others | 0 | 0.00 | 6 | 6.45 | 6 | 3.27 |
| Household asset ownership* | ||||||
| Radio | 58 | 65.20 | 36 | 16.90 | 94 | 52.80 |
| Television | 59 | 66.30 | 25 | 28.10 | 84 | 47.20 |
| Phone | 86 | 96.60 | 77 | 86.50 | 163 | 91.60 |
| Gas cooker | 27 | 30.30 | 17 | 19.10 | 44 | 24.70 |
| Motocycle/car | 29 | 31.18 | 16 | 17.02 | 45 | 24.19 |
| Source of drinking water* Borehole/well | 73 | 78.10 | 62 | 66.31 | 135 | 72.58 |
| Source of energy for cooking: firewood | 86 | 92.50 | 74 | 79.60 | 160 | 86.02 |
| Possession of livestock | 58 | 62.00 | 32 | 34.00 | 90 | 48.40 |
| Number of household members | ||||||
| 1–5 | 23 | 24.70 | 55 | 59.10 | 78 | 41.90 |
| 6–10 | 41 | 44.10 | 33 | 35.50 | 74 | 39.80 |
| ≥ 10 | 29 | 31.20 | 5 | 5.40 | 34 | 18.30 |
| Number of households with members < 5 years | ||||||
| 1–5 | 60 | 64.51 | 50 | 53.76 | 110 | 59.14 |
| 6–10 | 6 | 6.45 | 1 | 1.07 | 7 | 3.8 |
| ≥ 10 | 1 | 1.07 | 1 | 1.07 | 2 | 1.07 |
| Number of rooms per house | ||||||
| 1–5 | 45 | 48.40 | 80 | 86.02 | 128 | 68.82 |
| 6–10 | 45 | 48.40 | 13 | 13.97 | 58 | 31.18 |
| ≥ 10 | 3 | 3.20 | 0 | 0.00 | 3 | 1.61 |
N: number of participants; %: percentage.
The percentages do not add up to 100 because these results are from multiple-response questions.
The number of respondents who declared their age is below the sample size.
House characteristics
House characteristics varied significantly between sites (p < 0.001); they were predominantly constructed with mud and iron/zinc sheet roofing (54.8%) in Olama and with wooden planks and iron/zinc sheet roofing (75.3%) in Nyabessan (Figure S1). More than 90% of the houses in both villages had open eaves. Household composition varied significantly from one locality to the other (p < 0.001). In Olama, the total number of people per house ranged from 1 to 25 individuals, with a mean of 9.16. The average number of people per house in Nyabessan was 5.14. Children under 5 years old were found in the majority of houses.
General knowledge about malaria
All respondents (HoH) of both study sites declared to have heard about malaria before, and almost all of them (88.17%) attributed the cause of malaria to mosquito bites (Table 2). Fever and headache were the most cited symptoms of malaria. In general, more than 80% of HoH were able to give at least two correct symptoms of malaria (n = 82; 88.17% and n = 79; 84.95% in Olama and Nyabessan, respectively).
Table 2.
Population knowledge and attitude concerning malaria prevention and the use of LLINs in Olama and Nyabessan.
| Olama | Nyabessan | Total | |
|---|---|---|---|
| Heard about malaria | |||
| Yes | (93) 100.0# | (93) 100.0 | (186) 100.0 |
| No | (0) 0.0 | (0) 0.0 | (0) 0.0 |
| Mode of transmission of malaria | |||
| Mosquito bites | (85) 91.4 | (79) 84.9 | (164) 88.2 |
| Dirt | (2) 2.2 | (3) 3.2 | (5) 2.7 |
| Other | (6) 6.5 | (7) 7.5 | (13) 6.9 |
| No idea | (0) 0.0 | (4) 4.3 | (4) 2.15 |
| Purpose of using net (%)* | |||
| Stop mosquitoes biting | (42) 46.7 | (54) 60.0 | (96) 53.3 |
| Stop buzzing | (1) 1.0 | (4) 4.4 | (5) 2.8 |
| Be able to sleep | (5) 5.6 | (7) 7.8 | (12) 6.7 |
| Fear of malaria | (42) 46.7 | (26) 29.0 | (68) 37.8 |
| Other malaria control tools in use (%) | |||
| Coils | (10) 10.8 | (5) 5.4 | (15) 8.1 |
| Insecticide sprays | (15) 16.1 | (15) 15.1 | (30) 15.6 |
| Burning of organic materials | (2) 2.2 | (2) 2.2 | (4) 2.2 |
| Opening drain | (2) 2.2 | (7) 7.5 | (9) 4.8 |
| Door and window screening | (0) 0.0 | (3) 3.2 | (3) 1.6 |
| Repellents | (8) 8.6 | (9) 9.7 | (17) 9.2 |
| Others | (1) 1.1 | (4) 4.3 | (5) 2.7 |
| Household members having fever in past 2 weeks (%) | (42) 45.2 | (59) 63.4 | (101) 54.3 |
| Action undertaken by household member in case of fever (%)⁎⁎ | |||
| Self-medication | (7) 16.7 | (11) 18.6 | (18) 17.8 |
| Visiting a traditional healer | (4) 9.5 | (8) 13.6 | (12) 11.9 |
| Visiting hospital | (19) 45.2 | (34) 56.6 | (53) 52.5 |
| Visiting local clinic | (24) 57.1 | (7) 11.9 | (31) 30.7 |
n (%): sample size (percentage).
Frequencies were calculated using only the number of households with access to LLINs, ie 90 in each study site.
Frequencies were calculated using only the number of households where fever was observed in the 2 weeks prior the questionnaire.
Mosquito control practices and prevention of malaria in Olama and Nyabessan
Mosquito net ownership rate (number of households possessing at least one bed net) was high – 96.8% of households in both sites (Tables 2 and 3). Other control measures used to protect residents from mosquito bites included insecticide coils (8.1%), insecticide sprays (15.6%), repellents (9.1%), and screens on windows (1.6%).
Table 3.
Ownership, access to, and usage of LLINs in Olama and Nyabessan.
| Olama | Nyabessan | Total | |
|---|---|---|---|
| Households with access to LLINs (%)* | 90 (96.8)⁎⁎⁎ | 90 (96.8) | 180 (96.8) |
| Household members who slept under LLINs (%)* | 89 (95.7) | 87 (93.3) | 176 (94.4) |
| Households with children under 5 years old who slept under LLINs (%)⁎⁎ | 55 (82.1) | 52 (72.2) | 107 (77.0) |
| Households with at least one LLIN for every two people (%)* | 54 (58.1) | 70 (74.79) | 124 (64.43) |
| Household usage of ITNs 5–7 times per week (%)* | 96.50 | 100.00 | 98.25 |
Sample size is the number of HoH who participated in the study, i.e. 93 per study site.
Sample size is the number of HoH who declared having children under 5 years old, ie 67 in Olama and 72 in Nyabessan (see Table 1).
n (%): number (percentage).
The mosquito net brands used in both localities were mostly Olyset® and Permanet®. In Olama, about 94% of LLINs were acquired from free distribution campaigns conducted by the Ministry of Health (MoH), while in Nyabessan, in addition to free distribution campaigns, some residents declared that their bed nets were bought from a local shop or clinic (43.8%). Net usage rate was high in both sites, with 93.3% and 95.6% of people in Nyabessan and Olama, respectively, claiming regular net use. All house members reported sleeping under mosquito nets at least 5 days per week in both localities, with net usage particularly high for children under 5 years of age.
Despite this high rate of net possession, only 64.43% of households reported access to one LLIN for every two inhabitants, as recommended by WHO. This observation was locality dependent, with Nyabessan having the highest proportion of households with one LLIN for two inhabitants (74.79%). LLIN usage rate (the proportion of people who slept under LLINs the night before the day of the survey) was 94.45% (Table 3).
Most of the nets were acquired in 2016 (59.7%), 2 years before the survey. In Olama the majority of LLINs were in good condition, without holes (86.5%), whereas in Nyabessan the figure was only 22.7%.
The interviews revealed that family members regularly complained of fever. The proportions of people complaining of fever 2 weeks before the interview were 62.9% and 45.7% in Nyabessan and Olama, respectively (Table 2). The majority of people interviewed reported going to the hospital or clinic in cases of fever (85.4%). Some reported self-medication (17.15%) or boiling and drinking plant extracts macerated in water (11.6%).
Malaria detection in human populations
Characteristics of participants screened for malaria
In total, 836 individuals (household members), belonging to 258 houses (147 in Nyabessan vs 111 in Olama), were screened for malaria during the study, using mRDT. Most of those screened were children under 11 years old. The majority of these participants used LLINs (69.74% in Nyabessan vs 88.31% in Olama).
Age and exposure to Plasmodium infection
Of the 836 participants tested for malaria (430 in Olama and 406 in Nyabessan), 351 were found to be infected with Plasmodium sp., representing a prevalence of 42%. Malaria prevalence was significantly different between the two villages (χ² = 41.3; df = 1; p < 0.0001). Prevalence of infections in both sites was significantly higher in the 5–16 years age group compared with the other age groups (p < 0.0001). In Olama, 200 people participated in the dry season and 230 in the rainy season, resulting in prevalences of 18% (n = 36) and 32% (n = 74), respectively, showing a significant difference between the seasons (χ² = 11.011; df = 1; p < 0.001). In Nyabessan, 208 people were screened in the dry season and 198 in the rainy season, revealing prevalences of 65.38% (n = 136) and 55.03% (n = 105), respectively (Table 4), also showing a significant difference between the seasons (χ ² = 4.52; df = 1; p = 0.03).
Table 4.
Factors associated with malaria prevalence in Olama and Nyabessan.
|
Nyabessan |
Olama |
|||||||
|---|---|---|---|---|---|---|---|---|
| Prevalence (%) n/N | OR (95% CI) | p-value | Prevalence (%) n/N | OR (95% CI) | p-value | |||
| House type | ||||||||
| Cement | (60.0) 30/50 | 1 | NA | (23.0) 31//135 | 1 | NA | ||
| Wood | (54.1) 178/329 | 0.76 (0.43–1.44) | 0.43 | (38.5) 10/26 | 2.1 (0.84–5.08 | 0.1 | ||
| Mud | (58.3) 7/12 | 0.93 (0.26–3.55) | 0.92 | (25.5) 66/259 | 1.15 (0.7–1.87) | 0.58 | ||
| Sleeping behavior | ||||||||
| Sleep early | (59.0) 162/274 | 1 | NA | (29.0) 92/321 | 1 | 0.007 | ||
| Sleep late | (42.0) 53/125 | 0.51 (0.33–0.78 | 0.002 | (16.0) 17/108* | 0.46 (0.26–0.82)⁎⁎ | |||
| Wake up late | (54.0) 106/295 | 1 | NA | (24.0) 82/345 | 1 | NA | ||
| Wake up early | (54.0) 110/205 | 0.97 (0.65–1.44) | 0.88 | (33.0) 26/80 | 1.54 (0.91–2.62) | 0.11 | ||
| Age | ||||||||
| 0–5 | (59.0) 94/160 | 1a | NA | (23.0) 32/140* | 1a | NA⁎⁎ | ||
| 6–11 | (74.0) 73/99 | 1.97 (1.14–3.40) | 0.015 | (39.0) 55/141 | 2.16 (1.28–3.63) | 0.003 | ||
| 12–16 | (67.0) 42/63 | 1.40 (0.76–2.59) | 0.270 | (24.0) 21/88 | 1.06 (0.56–1.98) | 0.86 | ||
| > 16 | (20.0) 17/84 | 0.18 (0.09–0.33 | 0.001 | (2.0) 1/61 | 0.06 (0–0.42) | 0.005 | ||
| Season | ||||||||
| Dry | (55.0) 105/208 | 1a | NA | (32.0) 74/200 | 1a | |||
| Rainy | (65.4) 136/198 | 2.15 (1.43–3.22) | 0.001 | (18.0) 36/230 | 0.03 (0.20–0.49) | 0.001 | ||
(%) n/N: (Percentage) number of positive RDT/tested RDT; OR (95% CI): odds ratio (95% confidence interval).
NA: Not applicable.
Reference.
House type and malaria prevalence
In total, 258 houses (147 in Nyabessan vs 111 in Olama) were visited for malaria detection during the study. Taking all house types, malaria parasite prevalence was high in Nyabessan (63.9%, CI: 51.67–78.25) compared with Olama (48.65%, CI: 36.55–63.48) (χ² = 19.69; df = 1; p < 0.0001). A significant association was observed between malaria parasite prevalence and house characteristics (χ² = 4.58; p = 0.032). In Olama, people living in cement houses were found to be less infected by malaria parasites (Table 4).
Impact of sleeping behaviour on exposure to Plasmodium infection
People sleeping early were found to be more infected than those going to sleep late, in both Olama (χ ² = 7.1; df = 1; p = 0.007) and Nyabessan (χ² = 9.64; df = 1; p = 0.002). No significant differences were recorded between people waking up early or late in Olama (χ² = 2.61; df = 1; p = 0.07) and Nyabessan (χ² = 0.02; df = 1; p = 0.088) (Table 4).
Discussion
The study objective was to assess the influence of human behavioural factors and housing characteristics on exposure to malaria transmission risk in the equatorial forest region of Cameroon. According to the results, poor house construction, human activities during the night, and the poor physical integrity of LLINs were exposing the population to higher risks of malaria transmission. The majority of people interviewed had good knowledge of the vector and prevention measures (86.50%). This was consistent with previous studies in the country (Kimbi et al., 2014; Ndo et al., 2011; Nkuo Akenji et al., 2005).
Sound knowledge of the vector and prevention measures could reduce malaria transmission, especially if the population applied this knowledge through the use of effective control tools, such as LLINs. In Mwa, Kenya such knowledge was observed to contribute to the reduction of malaria in the locality (Oketch et al., 2008). Most people interviewed had been educated to at least secondary level, which might have increased their knowledge about the disease, since malaria and its control measures are part of the education program (Talipouo et al., 2019; Tassew et al., 2017; Woyessa et al., 2014). The presence of secondary schools and basic infrastructure such as health centres would have increased the prevalence of well-educated people in the study areas.
The fear of contracting malaria and desire to avoid mosquito bites were the main reasons pushing people to use LLINs. Frequent and correct use of LLINs could help reduce malaria morbidity and the related costs of treatment for poor communities. As the study was conducted a few months after a mass distribution campaign of nets, net ownership was high (95%) in the region, with more than 58% of households possessing at least one net for two people. Most of the people (HoH) interviewed declared sleeping regularly under a mosquito net, thus increasing community protection (Koenker et al., 2018; Koenker and Kilian, 2014). The ownership and usage of LLINs recorded during our study were similar to those recorded in the city of Yaoundé (Talipouo et al., 2019). However one should keep in mind that these data were recorded through self-reporting, which has been demonstrated to overestimate the real use of LLINs by the population (Talipouo et al., 2019).
Despite the recent distribution of bed nets, many were found with holes. This rapid degradation of mosquito nets just a few years after their acquisition may be due to their frequent use by residents, the low quality of material used, poor handling of the nets by the population (particularly children), and the means of hanging them. Similar physical deterioration of nets after only a year of use has been reported elsewhere (Githinji et al., 2010; Protopopoff et al., 2007). With the spread of insecticide resistance in vector populations, deteriorated bed nets become neither chemical nor physical barriers to mosquito bites. Permanet® 2.0 and Olyset® bed nets were the two brands found in use in the two localities. Despite the rapid expansion of insecticide resistance across the country (Antonio-Nkondjio et al., 2017; Piameu et al., 2021), pyrethroid-only nets are still widely distributed to the population for malaria prevention. Since insecticide resistance in vector populations is mainly conferred by monoxygenase-based mechanisms, the use of new-generation nets that combine pyrethroid and piperonyl butoxide (PBO) should be prioritized for combating malaria in the country (Martin et al., 2021; Gleave et al., 2021; Martin et al., 2021).
In most households, the use of LLINs was associated with other prevention methods against mosquito bites, such as insecticide sprays, insecticide coils, insect repellents, or the use of screens on windows. The use of different insecticide-based control measures, such as insecticide sprays and coils, alongside pesticides in agriculture could increase selection for insecticide resistance in mosquito populations (Antonio-Nkondjio et al., 2019; Bamou et al., 2019; Chouaïbou et al., 2008; Mouhamadou et al., 2019). Despite the importance of LLINs for controlling malaria, the fact that this tool is mostly efficient against indoor biting mosquitoes stresses the need for additional control measures to also target outdoor biting mosquitoes and to increase protection against malaria transmission.
The vast majority of those interviewed reported visiting a hospital or clinic for consultation when suspecting a case of fever. Some people admitted visiting traditional healers or treating themselves with local plants. These findings are in contrast with the results of studies conducted in urban settings, which suggest a higher rate of self-medication (Talipouo et al., 2019). The widespread use of hospitals and clinics by the study population could be a result of the Government of Cameroon subsidizing the treatment of malaria in public healthcare facilities (PNLP 2019). In addition, both study sites have community health workers, providing primary care services to people suffering from uncomplicated malaria or other common diseases. The frequent hospital visits in cases of sickness could also reflect a high level of confidence in, and close relationship with, healthcare workers.
Except for children under 5 years old, fewer than 50% of the population went to bed before 8 pm. They stayed outdoors during the first part of the night for social, educational and economic activities, such as playing, selling, discussing or watching television. These types of outdoor activity may lead to increased exposure to mosquito bites and malaria transmission. Outdoor malaria transmission has been identified as a major gap in malaria control (Finda et al., 2019; Monroe et al., 2019a, 2019b, 2015). Drivers for residual malaria transmission or factors promoting persistent malaria transmission have been explored in a range of studies (Monroe et al., 2015; Msellemu et al., 2017; Thomas et al., 2018).
A high prevalence of asymptomatic malaria was observed in both localities, despite extensive bed net coverage, which could be associated with household- or individual-related factors. Children aged 5–16 years were more infected than other age groups. It also appeared that sleeping time and the number of people under a net could also affect the level of exposure to mosquito bites, as reported elsewhere (Msellemu et al., 2017). All these findings highlight the need to improve malaria control strategies through the early detection of cases, prompt treatment, and sensitization campaigns.
Previous studies in the same region indicated that P. falciparum infection rates among non-users of treated nets were twice those found among users (Bamou et al., 2021, 2018), highlighting the importance of treated net use despite the increased prevalence of insecticide resistance in vector populations. House characteristics were also found to affect to malaria transmission risk, with people living in wooden houses exposed to a higher risk than those living in well-constructed, cemented houses. Previous studies have also reported a close association between the prevalence of malaria or mosquito abundance and house characteristics (Githinji et al., 2010; Liu et al., 2019; Ngadjeu et al., 2020; Nguela et al., 2020).
Limitations
Despite the strength of this study in showing the prevalence of malaria in a forested area of Cameroon, and the associated risk factors, there were some limitations. First, the questionnaire used only two questions — regarding the mode of transmission (vector) and malaria symptoms — to assess knowledge on malaria. Second, the study used only malaria diagnostic testing (mRDT) to estimate disease prevalence, without the support of microscopy and/or molecular biology to confirm cases.
Conclusion
This study highlights the need for additional control measures specifically addressing existing gaps, such as outdoor transmission of malaria, resistance of mosquitoes to insecticides, poor use of LLINs, or poor house construction. Despite the high coverage of the population with LLINs, the prevalence of malaria in the Cameroon equatorial forest region remains high, and requires further attention with regard to eliminating malaria in the country.
Authors’ contributions
RB, JM, and CAN conceived and designed the study protocol. RB, TT, EK, PAA, and CAN participated in field activities and data acquisition. EK, TT, PAA, FN, and JM critically revised the manuscript. BR and CAN interpreted and analysed data, and wrote the paper with the contribution of other authors. FN, JM, and BR supervised the work. All the authors read and approved the final version.
Availability of data and material
The datasets supporting the findings of this paper are included in this paper.
Funding
This work received financial support from a WHO TDR grant (2016/602099-0) and a Wellcome Trust Senior Fellowship in Public Health and Tropical Medicine (202687/Z/16/Z) to CAN. The funding bodies had no role in the study design, collection of data, analysis and interpretation of data, or in writing the manuscript.
Ethical approval
The study was conducted under ethical clearance delivered by the Cameroon National Ethics Committee for Research on Human Health (no. 2016/01/685/CE/CNERSH/SP) and the World Health Organization Ethics Review Committee (protocol ID ERC.0002666).
Consent to participate
Informed consent was obtained from all individual participants included in the study.
Consent for Publication
Not applicable
Competing interests
The authors declare that they have no competing interests.
Acknowledgements
The authors give special thanks to all the study participants from the villages of Olama and Nyabessan, and to the research team from the OCEAC Malaria Research Laboratory, without whom this study would have not been possible. The authors are also grateful to the medical authorities of the region and their agents for their help in malaria detection.
Footnotes
Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.ijregi.2022.11.003.
Contributor Information
Roland Bamou, Email: bamou2011@gmail.com, roland.bamou@nih.gov.
Timoléon Tchuinkam, Email: timotchuinkam@yahoo.fr.
Parfait Awono-Ambene, Email: hpaawono@yahoo.fr.
Flobert Njiokou, Email: njiokou@yahoo.fr.
Joseph Mwangangi, Email: jmwangangi@kemri-wellcome.org.
Christophe Antonio-Nkondjio, Email: antonio_nk@yahoo.fr.
Appendix. Supplementary materials
Supplementary files
Figure S1: Types of houses with iron/zinc roofing found in both study sites (Olama and Nyabessan): (A) house with wooden construction; (B) house with mud construction
References
- Antonio-Nkondjio C., Ndo C., Njiokou F., Bigoga J.D., Awono-Ambene P., Etang J., Ekobo A.S., Wondji C.S. Review of malaria situation in Cameroon: technical viewpoint on challenges and prospects for disease elimination. Parasites and Vectors. 2019;12:501. doi: 10.1186/s13071-019-3753-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Antonio-Nkondjio C., Simard F., Awono-Ambene P., Ngassam P., Toto J.-C., Tchuinkam T., Fontenille D. Malaria vectors and urbanization in the equatorial forest region of south Cameroon. Trans Roy Soc Trop Med Hyg. 2005;99:347–354. doi: 10.1016/j.trstmh.2004.07.003. [DOI] [PubMed] [Google Scholar]
- Antonio-Nkondjio C., Sonhafouo-Chiana N., Ngadjeu C.S., Doumbe-Belisse P., Talipouo A., Djamouko-Djonkam L., Kopya E., Bamou R., Awono-Ambene P., Wondji C.S. Review of the evolution of insecticide resistance in main malaria vectors in Cameroon from 1990 to 2017. Parasit Vectors. 2017;10:1–14. doi: 10.1186/s13071-017-2417-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Awono-Ambene H.P., Kengne P., Simard F., Antonio-Nkondjio C., Fontenille D. Description and bionomics of Anopheles (Cellia) ovengensis (Diptera: Culicidae), a new malaria vector species of the Anopheles nili group from south Cameroon. Journal of Medical Entomology. 2004;41:561–568. doi: 10.1603/0022-2585-41.4.561. [DOI] [PubMed] [Google Scholar]
- Bamou R., Mbakop L.R., Kopya E., Ndo C., Awono-Ambene P., Tchuinkam T., Rono M.K., Mwangangi J., Antonio-Nkondjio C. Changes in malaria vector bionomics and transmission patterns in the equatorial forest region of Cameroon between 2000 and 2017. Parasit Vectors. 2018;11:1–13. doi: 10.1186/s13071-018-3049-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bamou R., Rono M., Degefa T., Midega J., Mbogo C., Ingosi P., Kamau A., Ambelu A., Birhanu Z., Tushune K., Kopya E., Awono-Ambene P., Tchuinkam T., Njiokou F., Yewhalaw D., Antonio Nkondjio C., Mwangangi J. Entomological and anthropological factors contributing to persistent malaria transmission in Kenya, Ethiopia, and Cameroon. J Infect Dis. 2021;223:S155–S170. doi: 10.1093/infdis/jiaa774. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bamou R., Sonhafouo-Chiana N., Mavridis K., Tchuinkam T., Wondji C.S., Vontas J., Antonio-Nkondjio C. Status of insecticide resistance and its mechanisms in Anopheles gambiae and Anopheles coluzzii populations from forest settings in south Cameroon. Genes. 2019;10:741. doi: 10.3390/genes10100741. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bayoh M.N., Mathias D.K., Odiere M.R., Mutuku F.M., Kamau L., Gimnig J.E., Vulule J.M., Hawley W.A., Hamel M.J., Walker E.D. Anopheles gambiae: historical population decline associated with regional distribution of insecticide-treated bed nets in western Nyanza Province. Kenya. Malar J. 2010;9:62. doi: 10.1186/1475-2875-9-62. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bhatt S., Weiss D.J., Cameron E., Bisanzio D., Mappin B., Dalrymple U., Battle K.E., Moyes C.L., Henry A., Eckhoff P.A., Wenger E.A., Briët O., Penny M.A., Smith T.A., Bennett A., Yukich J., Eisele T.P., Griffin J.T., Fergus C.A., Lynch M., Lindgren F., Cohen J.M., Murray C.L.J., Smith D.L., Hay S.I., Cibulskis R.E., Gething P.W. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–211. doi: 10.1038/nature15535. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chouaïbou M., Etang J., Brévault T., Nwane P., Hinzoumbé C.K., Mimpfoundi R., Simard F. Dynamics of insecticide resistance in the malaria vector Anopheles gambiae s.l. from an area of extensive cotton cultivation in northern Cameroon: dynamics of insecticide resistance. Tropical Med Inter Health. 2008;13:476–486. doi: 10.1111/j.1365-3156.2008.02025.x. [DOI] [PubMed] [Google Scholar]
- Cook J., Hergott D., Phiri W., Rivas M.R., Bradley J., Segura L., Garcia G., Schwabe C., Kleinschmidt I. Trends in parasite prevalence following 13 years of malaria interventions on Bioko island, Equatorial Guinea: 2004–2016. Malar J. 2018;17:62. doi: 10.1186/s12936-018-2213-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Durnez L., Mao S., Denis L., Roelants P., Sochantha T., Coosemans M. Outdoor malaria transmission in forested villages of Cambodia. Malaria Journal. 2013;12:1–14. doi: 10.1186/1475-2875-12-329. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finda M.F., Limwagu A.J., Ngowo H.S., Matowo N.S., Swai J.K., Kaindoa E., Okumu F.O. Dramatic decreases of malaria transmission intensities in Ifakara, south-eastern Tanzania since early 2000s. Malar J. 2018;17:362. doi: 10.1186/s12936-018-2511-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finda M.F., Moshi I.R., Monroe A., Limwagu A.J., Nyoni A.P., Swai J.K., Ngowo H.S., Minja E.G., Toe L.P., Kaindoa E.W., Coetzee M., Manderson L., Okumu F.O. Linking human behaviours and malaria vector biting risk in south-eastern Tanzania. PLoS One. 2019;14 doi: 10.1371/journal.pone.0217414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ghebreyesus, T.A., 2017. World malaria report 2017: foreword. World Health Organization.
- Githinji S., Herbst S., Kistemann T., Noor A.M. Mosquito nets in a rural area of western Kenya: ownership, use and quality. Malar J. 2010;9:250. doi: 10.1186/1475-2875-9-250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gleave K., Lissenden N., Chaplin M., Choi L., Ranson H. Piperonyl butoxide (PBO) combined with pyrethroids in insecticide-treated nets to prevent malaria in Africa. Cochrane Database of Systematic Reviews. 2021:2021. doi: 10.1002/14651858.CD012776.pub3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gryseels C., Durnez L., Gerrets R., Uk S., Suon S., Set S., Phoeuk P., Sluydts V., Heng S., Sochantha T. Re-imagining malaria: heterogeneity of human and mosquito behaviour in relation to residual malaria transmission in Cambodia. Malar J. 2015;14:1–12. doi: 10.1186/s12936-015-0689-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keiser J., Singer B.H., Utzinger J. Reducing the burden of malaria in different eco-epidemiological settings with environmental management: a systematic review. The Lancet Infect Dis. 2005;5:695–708. doi: 10.1016/S1473-3099(05)70268-1. [DOI] [PubMed] [Google Scholar]
- Kimbi H.K., Nkesa S.B., Ndamukong-Nyanga J.L., Sumbele I.U.N., Atashili J., Atanga M.B.S. Socio-demographic factors influencing the ownership and utilization of insecticide-treated bed nets among malaria vulnerable groups in the Buea Health District, Cameroon. BMC Res Notes. 2014;7:624. doi: 10.1186/1756-0500-7-624. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koenker H., Arnold F., Ba F., Cisse M., Diouf L., Eckert E., Erskine M., Florey L., Fotheringham M., Gerberg L., Lengeler C., Lynch M., Mnzava A., Nasr S., Ndiop M., Poyer S., Renshaw M., Shargie E., Taylor C., Thwing J., Van Hulle S., Ye Y., Yukich J., Kilian A. Assessing whether universal coverage with insecticide-treated nets has been achieved: is the right indicator being used? Malar J. 2018;17:355. doi: 10.1186/s12936-018-2505-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koenker H., Kilian A. Recalculating the net use gap: a multi-country comparison of ITN use versus ITN access. PLoS One. 2014;9:e97496. doi: 10.1371/journal.pone.0097496. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu H., Dixon D., Bibbs C.S., Xue R.-D. Autocidal gravid ovitrap incorporation with attractants for control of gravid and host-seeking Aedes aegypti (Diptera: Culicidae) J Med Entomol. 2019;56:576–578. doi: 10.1093/jme/tjy207. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Martin J.L., Mosha F.W., Lukole E., Rowland M., Todd J., Charlwood J.D., Mosha J.F., Protopopoff N. Personal protection with PBO-pyrethroid synergist-treated nets after 2 years of household use against pyrethroid-resistant Anopheles in Tanzania. Parasites and Vectors. 2021;14:150. doi: 10.1186/s13071-021-04641-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mbakop L.R., Awono-Ambene P.H., Mandeng S.E., Ekoko W.E., Fesuh B.N., Antonio-Nkondjio C., Toto J.-C., Nwane P., Fomena A., Etang J. Malaria transmission around the Memve'ele hydroelectric dam in South Cameroon: a combined retrospective and prospective study, 2000–2016. International Journal of Environmental Research and Public Health. 2019;16 doi: 10.3390/ijerph16091618. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyers J.I., Pathikonda S., Popkin-Hall Z.R., Medeiros M.C., Fuseini G., Matias A., Garcia G., Overgaard H.J., Kulkarni V., Reddy V.P., Schwabe C., Lines J., Kleinschmidt I., Slotman M.A. Increasing outdoor host-seeking in Anopheles gambiae over 6 years of vector control on Bioko Island. Malar J. 2016;15:239. doi: 10.1186/s12936-016-1286-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyrowitsch D.W., Pedersen E.M., Alifrangis M., Scheike T.H., Malecela M.N., Magesa S.M., Derua Y.A., Rwegoshora R.T., Michael E., Simonsen P.E. Is the current decline in malaria burden in sub-Saharan Africa due to a decrease in vector population? Malar J. 2011;10 doi: 10.1186/1475-2875-10-188. 188–188. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moiroux N., Gomez M.B., Pennetier C., Elanga E., Djènontin A., Chandre F., Djègbé I., Guis H., Corbel V. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Inf Dis. 2012;206:1622–1629. doi: 10.1093/infdis/jis565. [DOI] [PubMed] [Google Scholar]
- Monroe A., Asamoah O., Lam Y., Koenker H., Psychas P., Lynch M., Ricotta E., Hornston S., Berman A., Harvey S.A. Outdoor-sleeping and other night-time activities in northern Ghana: implications for residual transmission and malaria prevention. Malar J. 2015;14:35. doi: 10.1186/s12936-015-0543-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Monroe A., Mihayo K., Okumu F., Finda M., Moore S., Koenker H., Lynch M., Haji K., Abbas F., Ali A., Greer G., Harvey S. Human behaviour and residual malaria transmission in Zanzibar: findings from in-depth interviews and direct observation of community events. Malar J. 2019;18:220. doi: 10.1186/s12936-019-2855-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Monroe A., Moore S., Koenker H., Lynch M., Ricotta E. Measuring and characterizing night time human behaviour as it relates to residual malaria transmission in sub-Saharan Africa: a review of the published literature. Malar J. 2019;18:6. doi: 10.1186/s12936-019-2638-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mouhamadou C.S., de Souza S.S., Fodjo B.K., Zoh M.G., Bli N.K., Koudou B.G. Evidence of insecticide resistance selection in wild Anopheles coluzzii mosquitoes due to agricultural pesticide use. Infect Dis Poverty. 2019;8:64. doi: 10.1186/s40249-019-0572-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Msellemu D., Shemdoe A., Makungu C., Mlacha Y., Kannady K., Dongus S., Killeen G.F., Dillip A. The underlying reasons for very high levels of bed net use, and higher malaria infection prevalence among bed net users than non-users in the Tanzanian city of Dar es Salaam: a qualitative study. Malar J. 2017;16:423. doi: 10.1186/s12936-017-2067-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mwangangi J.M., Mbogo C.M., Orindi B.O., Muturi E.J., Midega J.T., Nzovu J., Gatakaa H., Githure J., Borgemeister C., Keating J., Beier J.C. Shifts in malaria vector species composition and transmission dynamics along the Kenyan coast over the past 20 years. Malar J. 2013;12:13. doi: 10.1186/1475-2875-12-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ndo C., Menze-Djantio B., Antonio-Nkondjio C. Awareness, attitudes and prevention of malaria in the cities of Douala and Yaoundé (Cameroon) Parasites and Vectors. 2011;4:1–6. doi: 10.1186/1756-3305-4-181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ngadjeu C.S., Doumbe-Belisse P., Talipouo A., Djamouko-Djonkam L., Awono-Ambene P., Kekeunou S., Toussile W., Wondji C.S., Antonio-Nkondjio C. Influence of house characteristics on mosquito distribution and malaria transmission in the city of Yaoundé, Cameroon. Malar J. 2020;19:53. doi: 10.1186/s12936-020-3133-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nguela R.L., Bigoga J.D., Armel T.N., Esther T., Line D., Boris N.A., Frederic T., Kazi R., Williams P., Mbacham W.F., Leke R.G.F. The effect of improved housing on indoor mosquito density and exposure to malaria in the rural community of Minkoameyos, Centre Region of Cameroon. Malar J. 2020;19:172. doi: 10.1186/s12936-020-03232-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nkuo Akenji T., Ntonifor N.N., Kimbi H.K., Abongwa E.L., Ching J.K., Ndukum M.B., Anong D.N., Nkwescheu A., Songmbe M., Boyo M.G. The epidemiology of malaria in Bolifamba, a rural community on the eastern slopes of Mount Cameroon: seasonal variation in the parasitological indices of transmission. Annals of Trop Med Parasitol. 2005;99:221–227. doi: 10.1179/136485905X29693. [DOI] [PubMed] [Google Scholar]
- Piameu M., Nwane P., Toussile W., Mavridis K., Wipf N.C., Kouadio P.F., Mbakop L.R., Mandeng S., Ekoko W.E., Toto J.C., Ngaffo K.L., Ngo Etounde P.K., Ngantchou A.T., Chouaibou M., Müller P., Awono-Ambene P., Vontas J., Etang J. Pyrethroid and etofenprox resistance in Anopheles gambiae and Anopheles coluzzii from vegetable farms in Yaoundé, Cameroon: dynamics, intensity and molecular basis. Molecules. 2021;26 doi: 10.3390/molecules26185543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- PNLP Plan Strategique National de Lutte Contre le Paludisme au Cameroun 2019. Minsanté. 2019:2019. [Google Scholar]
- PNLP Programme National de Lutte Contre le Paludisme au Cameroun. Minsanté. 2021 https://pnlp.cm/ Available from: [Google Scholar]
- Protopopoff N., Van Bortel W., Marcotty T., Van Herp M., Maes P., Baza D., D'Alessandro U., Coosemans M. Spatial targeted vector control in the highlands of Burundi and its impact on malaria transmission. Malar J. 2007;6:158. doi: 10.1186/1475-2875-6-158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rodríguez-Rodríguez D., Katusele M., Auwun A., Marem M., Robinson L.J., Laman M., Hetzel M.W., Pulford J. Human behaviour, livelihood, and malaria transmission in two sites of Papua New Guinea. J Inf Dis. 2021;223:S171–S186. doi: 10.1093/infdis/jiaa402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sherrard-Smith E., Griffin J.T., Winskill P., Corbel V., Pennetier C., Djénontin A., Moore S., Richardson J.H., Müller P., Edi C., Protopopoff N., Oxborough R., Agossa F., N'Guessan R., Rowland M., Churcher T.S. Systematic review of indoor residual spray efficacy and effectiveness against Plasmodium falciparum in Africa. Nat Commun. 2018;9:4982. doi: 10.1038/s41467-018-07357-w. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tadesse E., Workalemahu B., Shimelis T. Diagnostic performance evaluation of the SD BIOLINE malaria antigen ag pf/pan test (05FK60) in a malaria endemic area of southern Ethiopia. Rev Inst Med Trop S Paulo. 2016;58 doi: 10.1590/S1678-9946201658059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Talipouo A., Ngadjeu C.S., Doumbe-Belisse P., Djamouko-Djonkam L., Sonhafouo-Chiana N., Kopya E., Bamou R., Awono-Ambene P., Woromogo S., Kekeunou S. Malaria prevention in the city of Yaoundé: knowledge and practices of urban dwellers. Malar J. 2019;18:167. doi: 10.1186/s12936-019-2799-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tassew A., Hopkins R., Deressa W. Factors influencing the ownership and utilization of long-lasting insecticidal nets for malaria prevention in Ethiopia. Malar J. 2017;16:262. doi: 10.1186/s12936-017-1907-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas S., Ravishankaran S., Asokan A., Johnson Amala Justin N.A., Maria Jusler Kalsingh T., Mathai M.T., Valecha N., Eapen A. Socio-demographic and household attributes may not necessarily influence malaria: evidence from a cross sectional study of households in an urban slum setting of Chennai, India. Malar J. 2018;17:4. doi: 10.1186/s12936-017-2150-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WHO . World Health Organization; Geneva: 2018. World Malaria Report 2018.www.who.int/malaria [Google Scholar]
- WHO . World Health Organization; Geneva: 2015. World Malaria Report 2015.www.who.int/malaria [Google Scholar]
- WHO . World Health Organization; Geneva: 2020. World Malaria Report 2020.https://www.who.int/publications/i/item/9789240015791 [Google Scholar]
- Woyessa A., Deressa W., Ali A., Lindtjørn B. Ownership and use of long-lasting insecticidal nets for malaria prevention in Butajira area, south-central Ethiopia: complex samples data analysis. BMC Public Health. 2014;14:99. doi: 10.1186/1471-2458-14-99. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplementary files
Figure S1: Types of houses with iron/zinc roofing found in both study sites (Olama and Nyabessan): (A) house with wooden construction; (B) house with mud construction
Data Availability Statement
The datasets supporting the findings of this paper are included in this paper.

