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Journal of Entomology and Zoology Studies 2019; 7(3): 941-946
E-ISSN: 2320-7078
P-ISSN: 2349-6800
JEZS 2019; 7(3): 941-946
© 2019 JEZS
Received: 22-03-2019
Accepted: 25-04-2019
AA Amaechi
Tropical Disease Research Unit,
Department of Animal and
Environmental Biology, Imo
State University, P.M.B. 2000
Owerri, Nigeria
BEB Nwoke
Tropical Disease Research Unit,
Department of Animal and
Environmental Biology, Imo
State University, P.M.B. 2000
Owerri, Nigeria
JI Iwunze
Tropical Disease Research Unit,
Department of Animal and
Environmental Biology, Imo
State University, P.M.B. 2000
Owerri, Nigeria
CA Ikpeama
Tropical Disease Research Unit,
Department of Animal and
Environmental Biology, Imo
State University, P.M.B. 2000
Owerri, Nigeria
MN Ezike
Tropical Disease Research Unit,
Department of Animal and
Environmental Biology, Imo
State University, P.M.B. 2000
Owerri, Nigeria
MO Nwachukwu
Department of Biological
Sciences, Federal University of
Technology, P.M.B 1526 Owerri,
Nigeria
G Ugagu
Imo State Polythecnic Ohaji-
Egbema Imo State
J Egejuru
Out Patient Department (OPD)
Federal Medical Center Owerri,
Nigeria
Correspondence
AA Amaechi
Tropical Disease Research Unit,
Department of Animal and
Environmental Biology, Imo
State University, P.M.B. 2000
Owerri, Nigeria
Attractiveness of human subjects to the malaria
and lymphatic filariasis vectors in parts of Ebonyi
state, Nigeria
AA Amaechi, BEB Nwoke, JI Iwunze, CA Ikpeama, MN Ezike, MO
Nwachukwu, G Ugagu and J Egejuru
Abstract
Malaria and Lymphatic filariasis (LF) are African’s most important vector-borne diseases transmitted by
mosquitoes. Attractiveness of pregnant women and Alcohol drinkers was investigated in sentinel sites in
Ebonyi State, Nigeria from March to May, 2017. Two cohorts were used; pregnant women and non-
pregnant women households, Alcohol drinkers and non alcohol drinkers households. Mosquitoes were
caught indoors once a week by Mechanical Aspirator (MA) and Pyrethrum knock down (PKD)
techniques and identified using standard morphological keys. Attractiveness was determined by
estimating the number of mosquitoes caught and number of blood fed collected and assessed for parity
and physiological status. Of the 331 engorged mosquitoes, cohorts for pregnant women (70.78%) and
Alcohol drinkers (68.49%) had more mosquitoes than cohorts for non-pregnant women (29.22%) and
non alcohol drinkers (30.51%). Overall parity rates of the mosquitoes were 39.6% versus 20.13% for
cohorts of pregnant women and non-pregnant women and 51.98% versus 20.90% for cohorts of alcohol
drinkers and non alcohol drinkers respectively. Pregnant women and Alcohol drinkers attracted
significantly more Anopheles (the main malaria and LF vectors in the area) than non-pregnant women
and non alcohol drinkers (89.91% versus 22.02%, 83.74% versus 26.83%). However, the cohorts
attracted similar proportions of culicine mosquitoes (24.44% versus 46.67% and 47.62% versus 52.38%).
Pregnant women who consume alcohol could be at higher risk than non-pregnant women 79.09% versus
29.9%. This study supports the view that some individuals within a community are at risk from
mosquito-borne diseases than others and need to be integrated into public health policies for control.
Keywords: Vector attractiveness, human subjects, malaria and filariasis vectors
Introduction
Attractiveness of biting insects is important in medical contexts mostly in the dynamics of
transmission of pathogens by mosquitoes. It has been observed that when selecting a human
host, mosquitoes have a preference for certain individuals [1]. Anopheles species and Culex
quinquefasciatus, the primary malaria and lymphatic filariasis (LF) vectors have tremendous
vectorial capacity which is usually assessed by their strong preferences for feeding on humans
[2]. The rate of contact between host and mosquitoes has long been recognized as a crucial
determinant of transmission3 and successful controls depends on understanding the interaction
[4, 5]. Various factors are known to contribute to the differential attractiveness to biting insects.
For example, it has been reported that heat and moisture, olfactory cue [6], distinct body odor
[7], diet, general health condition, reproductive status [8, 9] are used by mosquito vectors to
locate and orientate towards human hosts.
Studies have shown that pregnant women due to physiological changes are significantly more
attracted to Anopheles mosquitoes than non-pregnant women [10, 11]. Beer consumption have
equally been found to increase human attractiveness to Anopheles [2]. While people infected
with malaria have been observed to be more attracted to Anopheles during transmissible stage
in what seem like host-parasite manipulation [13], no equivocal data exist on filarial parasite
manipulation. Predictions of transmission usually assume that all individual are at equal risk
from mosquito bites. However, there is evidence that humans vary in their attractiveness to
mosquitoes [14, 1]. Thus, host-vector contact is far from random [15].
Despite the co-endemicity of malaria and LF and sharing of exclusively night biting
endophagic vectors, human attractiveness to their vectors has been differential and limited to
either experimental studies or cross-sectional field surveys.
Journal of Entomology and Zoology Studies
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Thus, in scientific literature there is a conspicuous lack of
data on the attractiveness on human subjects to these vectors,
a fact which suggest rarity of the attractiveness.
Despite also potential consequences on exposure to malaria
and LF vectors, there is a serious lack of data on how diet and
pregnancy affect human attractiveness to malaria and LF
vectors from natural populations. This study was part of
arthropod-borne pathogen research tailored to evaluate the
threat that mosquito borne pathogens pose to human health.
Materials and Methods
Study Area
The study was conducted in two (2) sentinel villages;
Orijiriafor and Ndiagu Obu in Ohaukwu LGA of Ebonyi State
Nigeria (7031180181N and 5036160151E).
The areas are typical and represented the highest malaria and
LF endemic villages in Nigeria. The sites were chosen based
on preliminary immunochromatographic card text (ICT)
survey and malaria indicating the presence of both diseases in
the area. The ecology of the area has been described in details
[16, 17]. The inhabitants are Igbos who mainly live in mud walls
and thatched houses. Houses with block walls and or iron
sheets roofing are extremely rare. They are peasants growing
mainly maize, rice yam and cassava. Livestock kept include
cattle and goats with some animals tethered inside human
dwellings.
Ethical consideration/Study protocol
Ethical clearance and permission was approved by the Post
Graduate Research Board of the Zoology Department of Imo
State University, Owerri, Nigeria and Ebonyi State Ministry
of Health. All participarts were adult volunteers enrolled after
the nature of study was explained. Informed verbal concent
was obtained from residents of households on mosquito
collections. Purpose, procedure and benefits were made
known to them. Volunteers were given sufficient time to
consider their involvements.
Subject/Volunteers
Two cohorts were used for the study; the households for
pregnant women/non-pregnant women and households for
alcohol/water drinkers. The cohorts were carefully selected to
exclude those houses where animals were tethered inside. Ten
pairs of women in 10 different houses each pair consisting of
pregnant and non-pregnant women of roughly similar age,
weight and parity were chosen. After the study protocol, the
20 women were invited to participate an all gave their
informed consent.
The later cohort consisted of adults aged 20-45 years in good
health and not using any medication. Twenty eight (28)
participants were randomly selected and assigned to the palm
wine (n=18) and the water group (n=10). The participants
were excluded from smoke, drink or use of deodorants. The
beverage used in this study was Raffia species (Palm wine)
which had stayed till the following day (popularly called
overnights). This is the commonest consumed alcoholic drink
in the Eastern part of Nigeria including Ebonyi State.
They are predominantly consumed by males during the
evening at specific joints called “Bar Joints”. For the study,
we bought the kegs of palm wine from three different joints in
the villages and had a long night discussion with the
participants while the drink. Participants for the water group
drank portable sachet water from known source (Dachi
water).
Mosquito Sampling Techniques/Laboratory Processing
The density/abundance and parity status of the mosquitoes
were assessed in households. Houses were visited twice
monthly during the mornings and indoor resting mosquitoes
were collected by pyrethrum spray catch (PSC) and
mechanical aspirator [18]. The time and period of collection
were chosen to catch fully engorge vectors and reflected the
habit of vectors. Houses were of similar constructions to
avoid the effect of variability. Indoor resting mosquitoes
collected in these selected houses were taken to a temporary
dissection center as time allowed. Visual identification (for
morphology) was made using different keys and
characteristics [19] and sorted by abdominal status (fed, unfed,
gravid and half gravid). Blood fed mosquitoes were further
assessed for parity status by observing the degree of ovarian
trachioles [20]. Attractiveness was indicated by estimating the
proportions caught and blood fed from each cohort.
Statistical Analysis
Data were analysed by Chi square using Epi Info 6 computer
software statistical analysis programme (Version 2003) to
compare the indices. Vector density and rates were calculated
using percentages.
Results
Of 331 mosquitoes caught and assessed for density and parity,
46.53% (154/331) were from households for pregnant/non-
pregnant women while 53.47% (177/331) were from palm
wine/water drinkers households respectively. Cohorts for
pregnant women (70.78%) and alcohol drinkers (68.49%) had
significantly greater mosquitoes than cohorts for non-pregnant
women (29.22%) and water drinkers (30.51%).
Overall, parity rates of the mosquitoes were 39.61% versus
20.13% for cohorts of pregnant women and non-pregnant
women and 51.98% versus 20.90% for alcohol drinkers and
water drinkers respectively (Tables 1 & 3). Furthermore,
pregnant women (89.91%) and alcohol drinkers (83.74%)
attracted significantly more Anopheles species than non-
pregnant women (22.02%) and water drinkers (26.83%).
However, the cohorts attracted similar proportions of culicine
mosquitoes; (24.44% versus 46.67%) for pregnant and non-
pregnant women and (47.62% versus 52.38%) for alcohol and
water drinkers respectively (Tables 2&4).
Combination of mosquitoes collected from similar attraction
households showed significant difference (P<0.05). While
households for pregnant women and alcohol drinkers had
70.09%, households for non-pregnant women and water
dinkers had 29.91% (Table 5).
Journal of Entomology and Zoology Studies
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Table 1: Overall vector densities and physiological status.
Classification of data
Households (%)
Total
PW
NPW
1. Species
An. gambie sl
71(65.14)
13(28.89)
84(54.55)
An. funestus sl
27(24.77)
11(24.44)
38(24.68)
Cx. quinquefasciatus
11(0.09)
18(46.00)
29(18.83)
A. aegypti
0(0.00)
3(6.67)
3(1.95)
2. Abdominal condition
Overall parous
61(39.61)
31(20.13)
91(59.09)
Overall nulliparous
48(31.17)
18(8.97)
62(40.26)
3. Parity and Blood meal
Gravid
49(44.95)
26(57.78)
75(82.42)
Not gravid
12(11.01)
5(11.11)
17(18.68)
Blood fed
58(53.21)
26(57.78)
84(94.31)
Unfed
3(2.25)
0(0.00)
3(3.30)
4. Rate (%)
Parous
39.61
20.13
59.09
Legend: for table 1 and 2
PW = Pregnant women
NPW = Non-pregnant women
Table 2: Relative attraction of the study groups for mosquito vectors
Periods
Anopheles (%)
Culex (%)
PW
NPW
PW
NPW
Week 1
13(59.09)
9(40.91)
4(57.14)
3(42.86)
Week 2
16(69.57)
7(30.43)
3(37.50)
5(62.50)
Week 3
17(85.00)
3(15.00)
0(0.00)
5(1.00)
Week 4
21(100.00)
0(0.00)
1(100.00)
0(0.00)
Week 5
31(86.11)
5(13.89)
3(27.27)
8(72.72)
Total
98(89.91)
24(22.02)
11(24.44)
21(46.67)
Table 3: Overall vector densities and physiological status
Classification of data
Alcohol consumption (%)
Total
AD
NAD
1. Species
An. gambie sl
66(53.66)
15(27.27)
81(45.51)
An. funestus sl
37(30.08)
17(30.91)
54(30.34)
Cx. quinquefasciatus
18(14.63)
22(40.00)
40(22.47)
A. aegypti
1(0.81)
0(0.00)
1(0.56)
Mn. Africana
1(0.81)
0(0.00)
1(0.56)
2. Abdominal condition
Overall parous
92(51.98)
37(20.90)
129(72.88)
Overall nulliparous
31(17.51)
18(10.17)
49(27.53)
3. Parity and Blood meal:
Gravid
71(57.72)
30(54.55)
101(78.30)
Not gravid
21(17.07)
07( 12.73)
28(21.71)
Blood fed
75(60.98)
28(50.91)
103(79.84)
Unfed
17(13.82)
05(9.09)
22(17.05)
4. Rate (%)
Parous
51.98
20.90
72.88
Legend: for table 3 and 4
AD = Alcohol drinkers
NAD = Non-Alcohol drinkers/ water drinkers
Table 4: Relative attraction of the study group for mosquito
Periods
Anopheles (%)
Culex (%)
AD NAD
AD NAD
Week 1
7(70.00)
3(30.00)
5(62.50)
3(37.50)
Week 2
21(100.00)
0(0.00)
4(50.00)
4(50.00)
Week 3
17(70.83)
7(29.17)
2(25.00)
6(75.00)
Week 4
32(69.57)
14(30.43)
6(66.67)
3(33.33)
Week 5
26(74.29)
9(25.71)
3(33.33)
6(55.57)
Total
103(83.74)
33(26.83)
20(47.62)
22(53.38)
Journal of Entomology and Zoology Studies
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Table 5: Combination of mosquitoes collected from similar attraction households.
Species
No (%) collected
Total
PW/AD NPW/NAD
An. gambie sl
137(83.03)
28(16.67)
165(49.85)
An. funestus sl
64(69.57)
28(30.43)
92(27.97)
Cx. quinquefasciatus
29(42.03)
40(57.97)
69(20.85)
Others
2(40.00)
3(60.00)
3(1.51)
Total
232(70.09)
99(29.91)
331
Legend
PW/AD = household from pregnant women and Alcohol drinkers.
NPW/NAD = households from non-pregnant women and non alcohol/water drinkers.
Discussion
Host preferences has been studied in the laboratory and field
with a range of tools. The principle of these devices is that
mosquitoes are exposed to two or more host odours
simultaneously in a choice situation and then express a
positive response to a particular host by an upwind flight and
landing [12].
In the laboratory elimination of certain genetic traits by stress,
selective breeding and lack of exposure to natural
environmental condition including loss of feeding preference
are inherent limitations to this [21, 22]. However field survey is
conducted by examination of blood meal origin [23] and
observing mosquito behaviour in a choice situation [24].
Results of blood meal origin is often biased in favour of the
most abundant host species which may not be the preferred
host [25]. Observational could highlight the technical
difficulties of getting an accurate estimation of the biting
preferences of a population of vectors. Behavioral
observations with modifications as ours provide a more
objective tool for assisting host preferences.
We explored the effects of alcohol consumption and
pregnancy on human attractiveness to natural population of
malaria and LF vectors. The results demonstrated enough
evidence of the enhanced proportion of mosquitoes attraction
to pregnant women and alcohol drinkers against the other
cohorts (non-pregnant women and water drinkers). Similar
results have been differentially reported elsewhere in Gambia
and Burkina Faso [10, 26]. This is a vivid reflection that
mosquitoes caught engaged in odour-mediated flight
(mosquito activation) and mosquito orientation that is odour-
mediated anemotactic response. These processes in host
seeking are important and facilitate vector-human contacts [27,
6]. Water consumption and non pregnancy affected these
behaviour and probably suggested that the other cohorts were
responsible for increased attractiveness. Thus strong evidence
that alcoholism and pregnancy increased human attractiveness
to An.gambiae and Culex quinquefasciatus, the principal
vectors of malaria and LF in Africa.
The differential attractiveness to mosquitoes between human
host is still incompletely understood. Increased attractiveness
to pregnant women has been linked with increased body
temperature and exhaled breath [28], release of pregnancy
specific volatile substances in their breath or skin surface [29,
28]. Thus, they may be physiologically more attractive to
mosquito and are therefore more exposed than non-pregnant
women. This increased attractiveness combined with impaired
immunity and the adherence factors in the placenta have been
found to enhance susceptibility of pregnant women to malaria
[30].
Alcohols are known to be quickly absorbed from the gastro-
intestinal track into the blood and metabolized [31]. Fiftheen
minutes have equally been found to be sufficient interval for
alcohol to be present in blood, breath, urine and sweat [32].
While it is clear that alcohol consumption leads to decrease
body temperature that of carbon dioxide (CO2) remains
unclear. Though it is widely accepted that CO2 attracts blood
feeding insects, increased exhaled breath with CO2 analyser
could not account for attractiveness [26]. This could be because
compounds called attractants also can act as repellents at high
concentrations. Probably metabolism of alcohol induce
changes in breath or odour markers. Mosquitoes may have
also evolved preferences for alcoholics due to reduced host
defensive behaviour or nutritious blood meal. Further inquest
to eliminate the possibility that other ingredients in palm wine
could be driving force apart from alcohol require future
studies.
Consumption of alcohol is a widespread phenomenon and
most pressing global health priorities [33]. Palm wine used
herein is a very popular drink in South Eastern, Nigeria. It is
more commonly savored by the Yorubas, Urhobos and Igbos
at various joints in the evening after a day’s work basically to
relax [34]. Thus, increase attractiveness raises crucial issues on
control of malaria and LF. It is a fcat that local control of both
malaria and LF can only be reached if people who are bitten
the most by their vectors can be identified. By confirming
alcoholics and pregnant women as risk factors, our study has
showcased a potential underlying cause of heterogeneous
biting and also provided insights into the feasibility of
targeted interventions. This findings may be underestimation
since alcohol contributes substantially to the global burden of
diseases [35] and together with pregnancy both are known to
compromise host immune defense against parasites. Nelson
and Kolls [36] had observed that moderate or chronic alcohol
intake can have strong immunosuppressive effects. By
extension alcoholics are both at risk of exposure to mosquito
vectors as well as being more vulnerable to the parasites.
Interestingly, most men in this part of the country would drink
palm wine or other alcohols preparatory to sexual activities
with their partners including wives. Also the non fermented
sap (called fresh) is proposed to pregnant women and
lactating mothers as well as infants whose mothers can not
produce the necessary milk for their nursing because of the
nutritional wealth [37]. Given the importance of alcohol intake
in the groups that are most at risk from malaria and LF, this is
a possibility that require urgent attention.
As recommended in the Abuja Declaration [38], treated bed
nets should be employed urgently in Ebonyi State, Nigeria
and elsewhere to protect pregnant women and alcohol
drinkers (including other high risk group especially during the
riding season.
Acknowledgement
Our sincere gratitude goes to all Zoology lecturers of Imo
State University, Owerri. We thank the volunteers for
Journal of Entomology and Zoology Studies
~ 945 ~
participation. Thanks are also given to Mr. James Okoro for
recruitment of the volunteers. Prof. CN Ukaga and Prof. AN
Okere made reading suggestions.
Author’s contributions
Conceived and designed the study: AAA, BEBN, JII
Analyzed the data: JII, MON, GU
Wrote the article: AAA, JII, BEBN
Obtained ethical approval: BEBN, GU
Recruited the volunteers for study: MNE, CAI, GU.
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