Epidemiology of Mansonella perstans in the middle belt of Ghana
Debrah et al. Parasites & Vectors
Epidemiology of Mansonella perstans in the middle belt of Ghana
Linda Batsa Debrah 0 1
Norman Nausch 3
Vera Serwaa Opoku 0
Wellington Owusu 0
Yusif Mubarik 0
Daniel Antwi Berko 0
Samuel Wanji 4
Laura E. Layland 2
Achim Hoerauf 2
Marc Jacobsen 3
Alexander Yaw Debrah 6
Richard O. Phillips 5
0 Kumasi Centre for Collaborative Research into Tropical Medicine (KCCR) , Kumasi , Ghana
1 Department of Clinical Microbiology, Kwame Nkrumah University of Science and Technology , Kumasi , Ghana
2 Institute for Medical Microbiology, Immunology and Parasitology, University Hospital of Bonn , Bonn , Germany
3 Department of General Pediatrics , Neonatology, and Pediatric Cardiology , University Children's Hospital , Duesseldorf , Germany
4 Department of Microbiology and Parasitology, University of Buea , Buea , Cameroon
5 Department of Medicine, Kwame Nkrumah University of Science and Technology , Kumasi , Ghana
6 Faculty of Allied Health Sciences of Kwame Nkrumah University of Science and Technology , Kumasi , Ghana
Background: Mansonellosis was first reported in Ghana by Awadzi in the 1990s. Co-infections of Mansonella perstans have also been reported in a small cohort of patients with Buruli ulcer and their contacts. However, no study has assessed the exact prevalence of the disease in a larger study population. This study therefore aimed to find out the prevalence of M. perstans infection in some districts in Ghana and to determine the diversity of Culicoides that could be potential vectors for transmission. Methods: From each participant screened in the Asante Akim North (Ashanti Region), Sene West and Atebubu Amantin (Brong Ahafo Region) districts, a total of 70 μl of finger prick blood was collected for assessment of M. perstans microfilariae. Centre for Disease Control (CDC) light traps as well as the Human Landing Catch (HLC) method were used to assess the species diversity of Culicoides present in the study communities. Results: From 2,247 participants, an overall prevalence of 32% was recorded although up to 75% prevalence was demonstrated in some of the communities. Culicoides inornatipennis was the only species of Culicoides caught with the HLC method. By contrast, C. imicola (47%), C. neavei (25%) and C. schultzei (15%) were caught by the CDC light trap method. A wide diversity of other Culicoides spp. was also identified but correlation was only found between the prevalence of C. inornatipennis and M. perstans during the dry season. Conclusions: Here we demonstrate for the first time that M. perstans is highly prevalent in three districts in Ghana. We found a wide spectrum of Culicoides spp. Culicoides inornatipennis was the most anthropophilic and is therefore likely to be the species responsible for transmission of infection but formal proof has yet to be obtained.
Mansonellosis; Mansonella perstans; Culicoides; Microfilariae; Epidemiology
Amongst the known human filarial infections that
parasitize man, mansonellosis is the least studied even
though more than 100 million individuals are estimated
to be infected . Prevalence of mansonellosis has
mainly been reported in sub-Saharan Africa and parts of
Central and South America with about 600 million
individuals being at risk of infection in about 33
countries [1, 2]. To date, mansonellosis in man is elicited
by three known agents: M. perstans, M. streptocerca and
M. ozzardi. These agents vary in morphological and
anatomical features as well as in their geographical
locations . Whereas M. perstans and M. streptocerca
occur mainly in western, eastern and central Africa, M.
ozzardi is only prevalent in South America .
As with other filariae, M. perstans requires a vector
and is transmitted by female flies of the genus Culicoides
(biting midges). The overall life-cycle is similar to those
of other nematode infections such as onchocerciasis,
lymphatic filariasis and loiasis where humans are the
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definitive host. In brief, infective larvae are introduced
into the host during a blood meal and develop into adult
worms that reside in the coelomic cavity, peritoneal and
pleural cavities as well as mesenteric perirenal and
retroperitoneal tissues . They produce thousands of
unsheathed microfilariae (MF) that appear in the blood
stream with no particular periodicity and are taken up
by another biting midge for transmission to continue
. The exact lifespan of M. perstans adult worms has
not been deciphered although there is a report of the
presence of MF in the blood of a person who left the
endemic community 10 years earlier .
Mansonellosis has previously been thought of as
nonpathogenic [1, 6] but there have been associations of
some clinical manifestations with MF release, such as
eosinophilia and ocular disorders [7–9]. Other studies
have implicated M. perstans in the disease progression
of clinical malaria  and co-infections have been
shown to influence infant morbidity in Uganda [11–13].
In Ghana, M. perstans was detected in the 1990s 
but its relevance was not documented until its
association with Mycobacterium ulcerans was noted in Buruli
ulcer endemic communities in the Asante Akim North
District . Epidemiological surveys on M. perstans
prevalence in Ghana are lacking and the distribution of
different Culicoides species serving as potential vectors
is not known.
Thus given the paucity of information regarding M.
perstans prevalence in Ghana and also the existence
of different species of vector(s) involved in the
transmission of M. perstans in Africa [16–18], we carried
out epidemiological studies of M. perstans to assess
the burden of infection and to further identify the
diversity of Culicoides species that are attracted by
light and humans.
Mansonella perstans prevalence was determined in
2,247 participants from areas of the Middle Belt of
Ghana between July 2014 and September 2015. From
the Ashanti Region, eight communities (Sereboso,
Nhyieso, Dukusen, Beemu, Bebuso, Ananekrom, Afrisere
and Abutantri) were selected in the Ashanti Akim North
District based on previous reports of the disease .
From the Brong Ahafo region, five communities
(Akyeremade Battor, Drobe, Kofi Gyan, Lemu and Shafa) in the
Sene West and five communities (Duabone No. 1,
Duabone No. 2, Garadima, Issifu Akuraa and Seneso) in the
Atebubu-Amantin Districts were also selected due to
considerable migration of people from the Ashanti
Akim North District to these communities. These three
districts are in tropical rainforest areas with similar
ecological characteristics. Entomological surveys were
also performed in communities in the Ashanti Akim
North District to determine diversity of Culicoides
species that are attracted to light and/or humans (Fig. 1).
General demographic information such as age, sex,
and history of previous Mass Drug Administration
(MDA) were obtained from the consented participants.
A total of 70 μl finger pricked blood samples was taken
under sterile conditions for parasitological assessment.
Entomological assessment of Culicoides spp. was carried
out during the same period.
Microfilariae assessment by direct finger pricking
The middle finger of the volunteer’s left hand was
wiped and massaged simultaneously to ensure adequate
blood flow to the tip of the finger. The skin of the tip
of the finger was disinfected with 70% alcohol, pricked
with a sterile lancet and 20 μl of blood pipetted onto a
clean-labelled microscope slide. A coverslip was placed
on the blood and directly observed under 10× objective
lens of the light microscope for the presence of motile
Microfilariae assessment by counting chamber technique
To confirm that the MF identified in the direct finger
prick blood were M. perstans, 50 μl of blood was
additionally transferred from the pricked finger into already
prepared 1.5 ml Eppendorf tubes containing 950 μl of
3% acetic acid and mixed thoroughly to haemolyse the
red cells. The solution was poured into the Sedgewick
counting chamber ensuring the absence of air bubbles.
The presence or absence of M. perstans MF was
assessed under a light microscope using the 10×
objective lens. The MF were identified morphologically as M.
perstans based on the absence of sheath, extension of
nuclei to the bluntly rounded tip and their small size
(usually about 200 μm).
Seasonal collections of Culicoides species were carried
out from June to September 2014 for the wet season and
November 2014 to February 2015 for the dry season,
which are the two main seasonal variations in Ghana.
Culicoides species were collected during the first week
of each month.
Light trap collections
Centre for Disease Control’s (CDC) New Standard
Miniature light traps from John W. Hock Company, Florida,
USA, were mounted in proximity to both breeding sites
and human habitations. Each study community was
divided into four parts and a light trap mounted in each
part for the trapping of the midges in the dry and wet
seasons. The same collection sites were used at both
Fig. 1 Spatial-epidemiological map of study communities
sampling times. Attracted by UV light emitted by the
trap, Culicoides spp. and other flies were trapped in a
Petri plate containing 80% alcohol placed in the
suspended trap. Catches were made from 6:00 to 9:00 h for
the morning periods and from 16:00 to 17:00 h for the
evening periods. The trap catches were removed at the
end of the three hours collection and each trap assigned
a unique number with respect to its position in the field.
An overnight trap was additionally mounted from 18:00
to 6:00 h. The trapped flies were transferred into labelled
50 ml falcon tubes containing 80% alcohol and placed in
a cold box for transportation to the laboratory. The
number of flies caught by each trap (6:00–9:00 h, 16:00–
17:00 h and 18:00–6:00 h) was recorded and the flies
identified morphologically .
Human landing catches
Volunteers from the various communities were given
training on how to collect midges using the human
landing catch method. They were then deployed to their
various communities, and collection of Culicoides was
supervised by a trained staff member to reduce bias.
Midges were captured daily by 4 trained collectors
stationed near human habitations in the study
communities. Blood-seeking female midges were collected using
locally made aspirators when they were attempting to
take a blood meal on the collectors. The catching times
were made to coincide with that of the aforementioned
light traps. The caught midges were aspirated and stored
into labelled transparent plastic cups covered with a fine
net and blocked with cotton wool at the base. Midges
were knocked-down by freezing for few minutes and
then transferred into a labelled eppendorf tube
containing 80% ethanol. They were then transported to
the laboratory for morphological identification on the
Descriptive statistics was used to obtain general descriptive
information using the StatView®, Version 5 for Windows.
Data were analysed using IBM SPSS statistics software
version 22 and P-values less than 0.05 (P < 0.05) considered
statistically significant. Prism 6 software was used for
plotting the graphs from data generated. Geospatial maps were
Ashanti Akim North District had the highest overall
prevalence of 33% with some communities recording over
70% microfilarial prevalence. In Sene West and Atebubu
Amantin Districts the prevalence rates were similar to
those of Ashanti Akim North District at 31% (Table 1).
Within the various districts the prevalence differed from
one community to the other. Communities in the Ashanti
Akim North District showed the highest variation with 2%
in Ananekrom and 75% in Beemu (Additional file 1: Table
S1; Fig. 2d). Sampled areas in the Atebubu Amantin and
Sene West Districts were more comparable with M.
perstans prevalence ranging from 22–41% and 18–46%,
respectively (Additional file 1: Table S1; Fig. 2e, f ).
Further analysis was carried out for Drobe, a
community where participants had received Ivermectin for the
treatment of onchocerciasis for more than five years
under Mass Drug Administration (MDA) program.
MDA had taken place 3 months prior to the present
study. From 107 patients screened in that community,
58 (54.2%) had taken part in MDA and of those, 35
individuals were M. perstans MF positive. Twenty of 35
(60%) individuals had taken part in MDA for more than
three years. As this study did not include MDA
treatment as a factor, the impact of MDA on M. perstans
infection was not evaluated in detail.
Co-infection with Wuchereria bancrofti MF was
coincidentally identified in five people from Abutantri
community in the Ashanti Akim North District. The MF
were differentiated by their size and presence of sheath
around the MF.
From June 2014 to October 2015 an entomological
survey to identify diversity of Culicoides species in Ashanti
created using http://www.spatialepidemiology.
MannWhitney U-tests were carried out for the determination of
the differences in demographic information between males
and females and Spearman’s correlation was used to
check for correlation between M. perstans prevalence
and Culicoides abundance.
Characteristics of the study populations according to
A total of 2,247 participants from 18 communities in
Ashanti Akim North District, Atebubu Amantin District
and Sene West Districts was screened for the presence
of M. perstans MF in their blood. Upon comparison of
participating districts, there was no significant difference
in gender or age distribution with the exception of
participants from the Sene West District where the
proportion of female volunteers was significantly higher
than males (Table 1).
Prevalence of M. perstans infection in study communities
There was statistical significance in microfilarial
prevalence between males and females, with the exception of
participants from Sene West District. In all three
districts, there were associations between the M. perstans
infection prevalence and age of study participants (χ2 = 24.3,
df = 8, P = 0.0020; χ2 = 25.1, df = 8, P = 0.0015; and χ2 = 28.3,
df = 8, P = 0.0004, respectively). In the Ashanti Akim
North District the prevalence increased with age
with an exceptionally high prevalence within the 14–
19 years age group (Fig. 2a). In Sene West and
Atebubu Amantin Districts (Fig. 2b, c) microfilarial
prevalence increased from age group 9–13 years until
it plateaued from age 20–25 years.
Table 1 Characterization of volunteers in the study districts
Mean age yrs (range)
aSignificant differences observed in Sene West District (Mann-Whitney U-Test, U = 29,539, Z = -2.727, P = 0.0064)
bNo significant difference between MF positive and gender (Fisher’s exact test, P = 0.435)
cOne community in the Sene West District had taken part in the national mass drug administration programme (MDA)
Abbreviations: M, male; F, female, MF, microfilarae
Fig. 2 Distribution of M. perstans microfilariae within age groups for Ashanti Akim North District (a), Sene West District (b), Atebubu Amantin
District (c), as well as distribution within specific communities for Ashanti Akim North District (d), Sene West District (e) and Atebubu Amantin
District (f). There were associations between microfilarial prevalence and age in the Ashanti Akim North District (χ2 = 24.3, df = 8, P = 0.0020;
Fig. 2a), Sene West District (χ2 = 25.1, df = 8, P = 0.0015; Fig. 2b) and Atebubu Amantin District (χ2 = 28.3, df = 8, P = 0.0004; Fig. 2c). Green line
depicts the community with co-infections of Wuchereria bancrofti. Red line shows the community with ongoing Mass Drug
Akim North District was undertaken. A total of 2,207
Culicoides species were caught in eight communities in
the Ashanti Akim North District in the communities
where the screening of volunteers for M. perstans was
also performed. Culicoides species were identified by
wing morphology as previously described by Boormann
& Glick [19, 20]. Results presented are for the evening
(16:00–17:00 h) and overnight (18:00–6:00 h) collections
since no Culicoides species was caught in the morning
either by light trap or HLC method.
In the dry season, 546 Culicoides were collected with
the CDC light traps and 364 by the HLC method. The
overall Culicoides species caught in the rainy season was
higher (1,297), with 737 flies caught by the CDC light
traps and 560 using the HLC method. The evening catch
(16:00–17:00 h) for the wet and dry seasons yielded 833
and 631, respectively, whilst the overnight Culicoides
collection (18:00–6:00 h) yielded 464 and 279 for the
wet and dry season respectively (Additional file 2:
Table S2 and Additional file 3: Table S3).
Interestingly, C. inornatipennis was the only species
collected when the HLC method was used irrespective
of seasons (wet and dry) or collection times (evening
and overnight). This species was recorded in all the
communities where the screening was done but was
never present in the light trap collections. Figure 3
shows that there was some species diversity in the total
trap collection with the highest recorded Culicoides
species being C. imicola (47%) followed by C. neavei
(25%) then C. schultzei (15%) in both seasons at all
times. Less than 6% of all the Culicoides collected in the
evening and overnight collections belonged to other
Culicoides species (Additional file 2: Table S2 and
Additional file 3: Table S3).
These species were also not present in the HLC
method. Although the total number of Culicoides
collected were higher in the wet season when compared
with the dry season the species diversity was
comparable. A non-parametric correlation analysis revealed a
significant correlation between M. perstans prevalence
and C. inornatipennis only in the dry season (Table 2).
But there was no correlation among any of the other
Culicoides species regardless of the season.
Even though M. perstans was suspected to be present in
Ghana (Awadzi et al. ), verification was only
ascertained when MF were coincidentally found in stained
peripheral blood mononuclear cells (PBMCs) from
patients with Buruli ulcer . The overall prevalence of
Fig. 3 Overnight trap collection (a), evening trap collections (b) and
human landing catch collections (c) Comparison of different Culicoides
species obtained using light traps and human landing catch collections
within the dry (black bars) or wet season (grey bars)
M. perstans in this study was found to be 32%, with a
wide variation between 2 and 75% (Additional file 1:
Table S1). This is understandable since M. perstans
distribution is known to vary from areas of low
endemicity to areas where almost everyone is infected
[11, 21, 22]. This prevalence rate is high compared
with several areas in which this infection has been
reported [2, 6, 23, 24] even though higher prevalence
rates of over 50% have also been reported in other
studies [6, 25–27].
Generally, the prevalence of M. perstans infection
was dependent on host gender since our survey
indicated that males had a higher chance of acquiring the
infection than females probably because males are
more exposed than females. However, in the Sene
West District, males and females appeared to have
equal chances of acquiring the infection. This is in
conformity with previous gender associations [7, 11]
but others could not confirm this [6, 28, 29].
There have also been suggestions that age influences
M. perstans infection. It is noteworthy that in our study,
young volunteers from nine years of age were infected
with M. perstans and the rate of infection increased with
age as was observed elsewhere [3, 6, 23]. The 20 to
45year-old volunteer group had a higher chance of being
infected when compared to those in other age groups,
probably because they are more active and therefore
more likely to be exposed to vector bites. It is possible
that the cumulative effect of reinfection plays a role in
adults getting infected than children. In low
transmission communities the differences in MF counts between
adults and children suggested a slow steady increase
with age  whereas high transmission areas had a
more rapid increase with age . There was a
progressive rise in prevalence with age irrespective of high
transmission or low transmission .
The selected communities in this study were
surrounded by vegetation (plantain farms) and livestock
that are known to be breeding grounds for biting midges
but the community with the highest prevalence (> 50%)
had plantain vegetation that was more dense or swampy
with a lot of compost material from the decaying of the
plantain stems and droppings from the livestock.
Probably that might be the preferred breeding ground for the
midges as was observed in other studies [1, 16, 31].
The wide distribution of M. perstans MF in the
districts suggests a broad distribution of the vector in
the Ashanti Akim District. The communities with the
high microfilarial prevalence were also noted to have
high distribution of C. innonatipennis collected with the
HLC method. Although previously C. austeni (currently
C. milnei), C. grahami and C. fulvithorax were noted for
transmission of the parasite [16–18, 31] their proportion
in this study was less than 6%, and there was no
significant correlation with the prevalence of M. perstans in
the dry and wet seasons. The vegetation in M. perstans
endemic communities comprised of plantain farms,
shrubs and decaying plant matters which are known to
favour the breeding of Culicoides .
Trap collections gave seven different species (C.
grahami, C. milnei, C. neavei, C. imicola, C. fulvithorax,
C. schultzei and C. accraensis) whereas HLC gave only
*Signifcant at P < 0.05
Table 2 Correlation between M. perstans prevalence and Culicoides spp. abundance: evening trap and human landing catch collections
one species (C. inornatipennis). This suggests that of all
the collected species, only C. inornatipennis was
preferentially anthropophilic. Similarly, this finding is in
consonance with those of Viennet et al.  who
collected a higher diversity of species (15 species) using the
UV light trap compared to direct aspiration.
To our knowledge, this is the first study investigating
the prevalence of mansonellosis in Ghana in a large
study population. Our study proves the presence of
mansonellosis in Ghana with over 30% of the people in
the study communities being infected. This study
therefore provides a platform for additional investigations
into the relevance of this filarial, especially its role in
coinfections. Interestingly, this study also revealed that the
diversity of Culicoides, obtained in an endemic area,
depends on the type of trap. Here we show that the
human landing catch method collected only one species
(C. inornatipennis) whereas the CDC light traps caught
seven different species (C. grahami, C. milnei, C. neavei,
C. imicola, C. fulvithorax, C. schultzei and C. accraensis)
but not C. inornatipennis. Such findings need to be
taken into consideration when performing entomological
studies on Culicoides species. The species responsible
for transmitting M. perstans in Ghana is likely to be C.
inornatipennis, but formal proof has yet to be obtained.
Additional file 1: Table S1. Demographic sistribution of volunteers in
study communities. (DOCX 83 kb)
Additional file 2: Table S2. Evening trap and hlc collections (4–7 pm)
for dry season and wet season. (DOCX 106 kb)
Additional file 3: Table S3. Overnight trap collections for dry season
and wet season (6 pm – 6 am). (DOCX 67 kb)
We thank all the volunteers in the study, as well as the Ashanti Akim North
District HeaIth Directorate in the Ashanti Region, Sene West and Atebubu
Amantin District HeaIth Directorates in the Brong Ahafo Region for their
cooperation. We are also grateful to Deutsche Forschungsgemeinschaft
(DFG) for funding this work.
Availability of data and materials
The datasets supporting the conclusions of this article are included within
the article and in Additional file 1: Table S1, Additional file 2: Table S2 and
Additional file 3: Table S3.
AH, MJ, LEL, ROP and AYD designed the study setup. SW trained VSO on
Culicoides species collection and identification. LBD, VSO, WO, DAB and YM
performed the fieldwork. LBD and NN performed the analysis of the data.
All authors read and approved the final manuscript.
Consent for publication
Consent to publish was obtained by the participants and the guardians of
participants below 18 years of age who are considered in Ghana as minors.
Ethics approval and consent to participate
Approval of the study was granted by the Committee on Human Research,
Publication, and Ethics of the School of Medical Sciences (SMS) of Kwame
Nkrumah University of Science and Technology (KNUST) (Ref: CHRPE/AP/433/
13). The District Health Directorates, chiefs, opinion leaders and community
health liaison officers in participating communities were also consulted.
Consent/assent was further obtained from all participants aged nine years and
above who were willing to take part in the study either by thumb-printing or
signing the Informed Consent Form. For children below 18 years, parental
consent was additionally obtained.
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