Hindawi
Journal of Parasitology Research
Volume 2023, Article ID 7500676, 10 pages
https://doi.org/10.1155/2023/7500676
Research Article
Malaria, Urogenital Schistosomiasis, and Anaemia in Pregnant
Ghanaian Women
Naa Adjeley Frempong ,1,2 Charity Ahiabor ,3 William K. Anyan,2 Atikatou Mama ,4
Kwadwo Asamoah Kusi ,5 Michael F. Ofori ,5 Bright Adu ,5 Alex Yaw Debrah ,6
Abraham K. Anang,7 Nicaise T. Ndam ,8 and David Courtin 8
1Clinical Microbiology Department, Kwame Nkrumah University of Science and Technology, Ghana
2Parasitology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana,
Legon, Ghana
3Science Laboratory Technology, Accra Technical University, Ghana
4Inserm U 1016, Institut Cochin, Université de Paris, 75014, France
5Immunology Department, Noguchi Memorial Institute for Medical Research, College of Health Sciences, University of Ghana,
Legon, Ghana
6Faculty of Health Sciences, Kwame Nkrumah University of Science and Technology, Ghana
7Institute of Environment and Sanitation Studies(IESS), University of Ghana, Legon, Ghana
8Université Paris Cité, MERIT, IRD, Paris, France
Correspondence should be addressed to Naa Adjeley Frempong; ntawiah@noguchi.ug.edu.gh
Received 19 April 2023; Revised 3 September 2023; Accepted 8 September 2023; Published 29 September 2023
Academic Editor: José F. Silveira
Copyright © 2023 Naa Adjeley Frempong et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Background. Anaemia is common in sub-Saharan Africa, and parasitic infections could worsen its burden during pregnancy.
Moreover, women become susceptible to malaria during pregnancy. We investigated Plasmodium falciparum (P. falciparum)
and Schistosoma haematobium (S. haematobium) infections and determined their association with anaemia during pregnancy.
Methods. A cross-sectional study involving 707 pregnant women attending antenatal care visits (ANC) and 446 at delivery was
conducted in Battor and Adidome hospitals. Pregnant women were screened by microscopy and qPCR for P. falciparum and S.
haematobium infections. Haemoglobin (Hb) levels were determined, and most participants received intermittent preventive
treatment during pregnancy (IPTp) during ANC till delivery. Regression analyses were performed for associations between
parasite infection and anaemia. Results. P. falciparum microscopy prevalence at ANC and delivery was 8% and 2%,
respectively, and by PCR 24% at ANC and 12% at delivery. Anaemia prevalence at ANC was 52% and 49% at delivery. There
was an increased risk of anaemia with P. falciparum infection (aOR = 1 92; p = 0 04). IPTp (p = 0 003) and age (p = 0 004) were
associated with increased Hb levels at delivery. S. haematobium prevalence by microscopy was 4% at ANC and 2% at delivery.
No significant correlation between S. haematobium and Hb levels was observed (coef = − 0 62 g/dl; p = 0 07). Conclusion.
High anaemia prevalence was observed during pregnancy, and P. falciparum infection was associated with anaemia at ANC.
Low S. haematobium prevalence could be attributed to previous praziquantel treatment during mass drug administration.
Routine diagnosis and treatment of S. haematobium infections in endemic areas could be initiated to reduce schistosomiasis
during pregnancy.
1. Background mortality [1], exposing the foetus to several complications
including anaemia, still birth, intrauterine growth retarda-
About 1.5 billion infections resulting from malaria and hel- tion, and low birth weight infants [2, 3]. Malaria and schis-
minthiases contribute to pregnancy-related morbidity and tosomiasis are widespread parasitic infections in tropical
2 Journal of Parasitology Research
and subtropical regions including Ghana [4, 5] and pose a during pregnancy, including intermittent preventive treat-
double disease burden during pregnancy in coendemic areas. ment during pregnancy (IPTp) and insecticide treated nets
Disease burden seems to be greater in women of reproduc- (ITNs) during first antenatal care visit (ANC) [29–31]. Fur-
tive age [6], often leading to lowered immunity, increased thermore, intensive case search by screening and treatment
susceptibility to other infections, and poor pregnancy out- exists for malaria prevention during pregnancy at ANC
comes [7, 8]. Another critical complication of malaria and [32]. However, routine schistosomiasis diagnosis and pre-
schistosomiasis is anaemia, which could have severe conse- ventive chemotherapy are not fully exhaustive. We investi-
quences on the health of the mother [9]. gated prevalence of malaria and urogenital schistosomiasis
The World Health Organization (WHO) estimates that and associated anaemia in two study hospitals at ANC and
out of 40 million pregnancies reported in sub-Saharan at the point of delivery.
Africa, 13.3 million cases have been linked to pregnancy-
associated malaria (PAM) [10]. Despite enormous control 2. Methods
and prevention strategies for the fight against malaria, it
remains a disease of public health importance in Ghana with 2.1. Ethics. Ethical clearance was obtained from the Ghana
a total of 5 million cases including at least 390,000 hospital Health Service (GHS) with protocol number GHS-ERC 06/
admissions [11]. Plasmodium falciparum infections contrib- 06/16 and Noguchi Memorial Institute for Medical Research
ute to 18% of outpatient department cases, leading to 14% of (NMIMR-IRB CPN 071/15-16).
hospital admissions and 3% maternal deaths [12]. As part of
the e 2.2. Study Area and Population. This study was carried outfforts aimed at fighting malaria, the program hopes to
reduce malaria mortality by 90% and malaria incidence by in Adidome Government Hospital (AH) and Battor Catholic
50% by 2025 [11]. WHO estimates that 40% of pregnant Hospital (BH), located in Adidome and Battor which are cap-
women worldwide are anaemic [13, 14] and the situation is ital towns of Central and North Tongu Districts of the Volta
no different in Ghana as it stands at 47% ranging from 37 Region, respectively, in Ghana [33]. The Tongu District is
to 53% [15]. Malaria has been identified as an important located in southeastern Ghana and mainly inhabited by the
independent risk factor for anaemia [16] and contributes Ewe tribe, with farming and fishing as major occupations.
to about 3-15% of anaemia cases and 25% of the total severe A total of 110,891 people inhabit North Tongu and 83,803
anaemia in pregnant women from malaria endemic coun- Central Tongu District [34]. The presence of the Volta River
tries [16]. The destruction of P. falciparum-infected erythro- and its numerous tributaries, dams, and dugouts in the dis-
cytes [17] and defective erythropoiesis in the bone marrow trict constitute a great potential for irrigation farming and
could lead to anaemia [16]. fishing. Heavy reliance of these dugouts for fresh water
Schistosomiasis, another known cause of anaemia [18], source and income generation activities makes it a prime
affects nearly 200 million people worldwide with considerable environment for schistosomiasis transmission through
economic impact and morbidity [6, 7, 19]. As a disease of human contact with infected vector snails [35]. In the Volta
poverty, 97% of schistosomiasis infections and 85% of at-risk Region, schistosomiasis is endemic [36], with a prevalence
population live in Africa [20]. Schistosoma haematobium prev- of 10% in children [37], and malaria prevalence has been
alence in pregnancy ranges from 0.30 to 4.53% in Northern ranked the third highest in 16 administrative regions [38].
Ghana and Dangme East District [21, 22]. A recent systematic 2.3. Study Design. A cross-sectional study was conducted in
review and meta-analysis study linked schistosomiasis to anae- women aged 16–45 years, attending ANC for the first time
mia, while mass drug administration (MDA) among pregnant and the maternity ward for delivery in AH and BH from
women reduced anaemia by 23% [18, 23]. In S. haematobium November 2016 to March 2019. Study participants had posi-
infections, the human host loses blood and iron when S. hae- tive urine pregnancy test, ultrasound scan of foetus, and were
matobium eggs with terminal spines pass through the urogen- HIV negative.Womenwith history of a debilitating condition
ital tract. Additionally, inflammation in response to dislodged in pregnancy and those receiving anthelmintics and malaria
eggs in host tissues could be the common cause of low haemo- treatment prior to enrolment at ANC were exempted from
globin (Hb) levels and anaemia [24]. our study. After consent was given by participants, question-
A problem of underreported data on schistosomiasis exists naire data was captured using CSPro (V6.2)-based electronic
in pregnancy. Therefore, it is necessary to generate accurate tablets while other relevant disease prevention tools that
data on pregnant women who form a high-risk group to guided the study were gathered from hospital records. Each
improve and guide schistosomiasis control strategies. Further- participant provided urine and blood samples for S. haemato-
more, a meta-analysis exposed a primary concern of scanty bium and P. falciparum diagnosis, respectively. During the
data on schistosomiasis outcomes in pregnancy [18]. WHO
first ANC, biological samples were collected before the
highly recommends anthelmintic therapy after the first tri- administration of IPTp. At the point of delivery, the number
mester of pregnancy [25–27] to improve maternal and infant of IPTp doses was gathered from hospital records.
health [7, 14]. In Ghana, although on-going programs exist
to control schistosomiasis and targeting elimination in the 2.4. Sample Collection and Analyses
future [28], the neglected tropical disease program reports
suboptimal treatment during pregnancy. 2.4.1. Blood. Hb levels of pregnant women were determined
Malaria and schistosomiasis are coendemic in Ghana using a Sysmex haematology analyser [39] at the time of
[4], and enormous malaria control efforts have been invested sampling at ANC and delivery. A thick blood film was
Journal of Parasitology Research 3
Table 1: Characteristics of participants during ANC and delivery.
Variable Study site N Mean ± SD or N (%) p value
ANC
AH 393 25 96 ± 6 5 0.005∗
Age (years)
BH 314 27 32 ± 6 1
AH 393 124/269 (46.1) 0.227
Primigravidae/multigravidae (%)
BH 314 90/224 (40.2)
AH 388 14 56 ± 7 1 0.002∗
Gestational age (weeks)
BH 307 16 19 ± 7 0
AH 393 359/393 (91.3) 0.398
Bed net use (N , %) (yes)
BH 313 289/313 (92.3)
AH 393 10 618 ± 1 5 0.002∗
Hb
BH 314 10 975 ± 1 4
AH 348 14/348 (4) 0.689
S. haematobium (N , %)
BH 314 11/324 (3.4)
AH 357 101/357 (28.3) 0.008∗
P. falciparum (N , %)
BH 320 59/320 (18.4)
Delivery
AH 329 314/329 (95) 0.020∗
IPTp use (%)
BH 114 114//114 (100)
AH 248 248/248 (100) 0.455
Bed net usage (N , %) (yes)
BH 111 111/111 (100)
AH 329 10 85 ± 1 1 0.913
Hb (g/dl)
BH 114 10 87 ± 1 5
AH 277 40/277 (14) 0.003∗
P. falciparum (N , %)
BH 102 4/102 (4)
∗Significance. N (%), total number of participants, and percentage are in parenthesis. Mean ± SD: mean ± standard deviation. Total prevalence of
S. haematobium at delivery was 3/192 (1.6%). Primigravid, first pregnancy; multigravid, more than one pregnancy.
prepared for each sample, stained with Giemsa, and Anaemia in pregnancy was classified using WHO guidelines
observed under the microscope to determine Plasmodium into normal (>11), mild (10-10.99), moderate (7.0-9.99), and
spp. [40, 41]. Plasmodium falciparum parasites were counted severe (<7) groups [51].
per 200 or 500 white blood cells (WBC) in thick blood film,
and parasite density was estimated per microlitre (μl) of 2.5. Statistical Analysis. Statistical analyses were performed
blood. A minimum of 100 fields was counted before each using SPSS version 22 (IBM). A Plasmodium parasite classi-
slide was determined as negative [42, 43]. fication was applied by estimating the median parasitaemia
Blood was blotted onto filter paper, and DNA was of pregnant women at a threshold of 2,500μl parasites/
extracted and amplified using quantitative PCR (qPCR) for blood. Bivariable analyses were performed using the non-
P. falciparum determination according to previous methods parametric chi-square or Kruskal-Wallis test for associations
[44–46]. between variables and Hb. Multivariable linear regression
analyses were performed for variables that showed a p value
2.4.2. Urine. Each of 40ml urine collected was gently swirled < 0.2 in a bivariable analyses. A logistic regression model
to ensure uniform distribution of parasite ova, and 10ml of determined factors including parasitic infections associated
urine was drawn and passed through a holder fitted with fil- with anaemia in pregnancy.
ter membrane [47]. Subsequently, the filter membranes were
placed on a microscope slide to observe and count S. haema- 3. Results
tobium eggs under a microscope at a magnification of 10x
[48, 49]. For quality control, 10 out of 100 prepared slides 3.1. Characteristics of Participants. The characteristics of
were randomly selected from each box by another indepen- study participants at ANC and delivery have been summa-
dent trained microscopist for examination [50]. S. haemato- rized (Table 1). A total of 707 pregnant women were
bium infection intensity was expressed as the number of eggs recruited at ANC (AH = 393, BH = 314) and 446 at delivery
per 10ml urine with a threshold (<49 eggs/10ml of urine) (AH = 330, BH = 116). Pregnant women in BH were older
for light intensity and (≥50/10ml) for heavy intensity [48]. with significantly higher Hb levels compared to AH. These
4 Journal of Parasitology Research
Table 2: Anaemia status of participants.
ANC Delivery
Anaemia status (Hb g/dl)
Adidome (N , %) Battor (N , %) p value Adidome (N , %) Battor (N , %) p value
Normal 175 (44.7) 167 (53.2) 166 (50.3) 60 (51.7)
Mild 104 (26.5) 72 (22.9) 0.015∗ 124 (37.6) 27 (23.3) 0.002∗
Moderate 105 (26.8) 75 (23.9) 39 (11.8) 29 (25.0)
Severe 8 (2.0) 0 1 (0.3) 0
Total 392 314 330 116
∗Statistically significant. At ANC and delivery, at a threshold of 95% confidence, anaemia status varied between two hospitals: ANC (p = 0 015) and delivery
(p = 0 002). Anaemia status of pregnant women was determined using WHO guidelines into normal (>11 g/dl), mild (10-10.99 g/dl), moderate (7.0-9.9 g/dl),
and severe (<7 g/dl) groups.
women from BH attended their first ANC much later in observed that more than two (≥2) IPTp doses received dur-
their pregnancy than those in AH. At delivery, many preg- ing pregnancy were positively associated with increased Hb
nant women (95% from AH and 100% from BH) reported levels compared to only one dose.
to have been treated with IPTp during pregnancy. Similarly, Subsequently, Hb levels of pregnant women were classi-
a high proportion of them (90% and 96%) indicated that fied using WHO recommendations for anaemia. Women
they slept in bed nets at ANC and delivery. Malaria preva- infected with P. falciparum had a higher risk of being anae-
lence in AH was significantly higher than BH at ANC and mic at ANC (aOR = 1 92, p = 0 04). The odds of pregnant
delivery, but there was no statistical difference in urogenital women developing anaemia as they get older was lowered
schistosomiasis prevalence in the two hospitals at ANC. (aOR = 0 95, p = 0 001) (Table 4). Furthermore, we grouped
anaemia status of pregnant women into mild, moderate, and
3.2. Malaria and Urogenital Schistosomiasis Prevalence severe, and P. falciparum infection (aOR: 15.19, p = 0 006)
among Pregnant Women. Malaria prevalence by microscopy and age (aOR: 0.79, p = 0 037) were associated with severe
was 8% (54/677) at ANC and 2% (9/379) at delivery and by anaemia when compared to women without anaemia (refer-
PCR was 24% (160/677) at ANC and 12% (44/379) at deliv- ence group). Similarly, malaria (aOR: 2.26, p = 0 07) and age
ery. Median parasitaemia was 2,020 parasites/μl of blood. At (aOR: 0.94, p < 0 0001) were associated with the risk of
ANC, the geometric mean parasitaemia for P. falciparum- becoming moderately anaemic at ANC. At delivery, IPTp
infected women was 1,995 (95% CI 1,259-3,162) parasites/μl. use (aOR: 0.79, p = 0 03) was significantly associated with
Urogenital schistosomiasis prevalence at ANC at AH was protection against mild anaemia. No association was
4% (14/348) and at BH 3% (11/324); 0.7% (5/662) had observed between P. falciparum parasitaemia levels and
P. falciparum and S. haematobium coinfections. From a anaemia (p value, 0.59).
total of 192 urine samples collected at delivery, only 2% S. haematobium-infected women at ANC presented
were positive for S. haematobium in BH (3/192). lower Hb levels than uninfected women (coef.: -0.62 g/dl;
Out of 28 pregnant women (25 at ANC and 3 at delivery) 95% CI (-1.26; 0.06)), although this was not statistically sig-
who had S. haematobium infections, the mean egg intensity nificant (p = 0 07). In a multivariable linear model, this effect
was 13 eggs/10ml (1-61 eggs/ml). Only one participant was remained not significant (p = 0 21) when adjusted for other
classified as high intensity (61 eggs/10ml) by standard proto- covariates (Table 3). Nonetheless, the only participant with
cols [25] with the remaining 27 falling within low intensity high S. haematobium infection intensity had the least Hb
(<50 eggs/10ml) category. level (5.4 g/dl) within severe anaemia range (<7.0 g/dl).
3.3. Anaemia and Parasitic Infections in Pregnant Women.
Anaemia status of pregnant women has been summarized 4. Discussion
(Table 2). Anaemia prevalence at ANC for women at AH
and BH was 55% (217/392) and 47% (147/314), respectively. Anaemia is a major health concern during pregnancy [22,
At delivery, anaemia prevalence was 50% at AH and 48% at 52], and the presence of malaria and schistosomiasis could
BH. All severe cases of anaemia were observed in AH, and increase its burden [18, 52]. Innovative strategies targeted
no pregnant woman reported with severe anaemia at BH, at pregnancy-associated malaria (PAM) include prompt
either at ANC or delivery. diagnosis and preventive treatment at ANC [31, 53] to
P. falciparum infection was significantly related with achieve a “zero malaria” target by 2030 [54, 55]. Schistoso-
decreased Hb levels (p = 0 002), and age was associated with miasis is one of the neglected tropical diseases (NTDs) tar-
an increased level of Hb (p < 0 001, linear regression model) geted for elimination as a public health problem by 2030
in pregnant women from ANC (Table 3). At delivery, Hb [19, 25]. However, in Ghana, pregnant women are exempted
levels for women who had taken IPTp during their preg- from MDA, and there seems to be no routine diagnosis and
nancy were significantly higher than those who had not been treatment during ANC programs. We investigated malaria-
treated (p = 0 003). Age was also associated with an and schistosomiasis-related anaemia in women attending
increased Hb level at delivery (p = 0 004). It was also ANC and delivery in AH and BH.
Journal of Parasitology Research 5
Table 3: Factors influencing Hb level in pregnant women at ANC and delivery.
Linear regression models (Hb levels of g/dl)
Variables SE p value
Coefficient (CI 95%)
ANC
P. falciparum -0.48 (-0.78, -0.18) 0.15 0.002∗
S. haematobium -0.46 (-1.18, 0.27) 0.37 0.215
Study area 0.10 (-0.16, 0.35) 0.13 0.461
Age 0.05 (0.03, 0.07) 0.01 <0.0001∗
Delivery
IPTp (yes/no) 0.94 (0.31, 1.57) 0.32 0.003∗
Age 0.05 (0.03, 0.07) 0.01 0.004∗
IPTp dose [1] 0.67 (-0.12, 1.48) 0.41 0.097
IPTp dose (>2) 1.07 (0.36, 1.79) 0.36 0.003∗
Age 0.03 (-0.002, 0.065) 0.02 0.066
CI: confidence interval; SE: standard error. Asterisk (∗) indicates factors that significantly influence Hb levels at ANC or delivery at p < 0 05.
Table 4: Risk factors for anaemia during pregnancy (logistic regression).
ANC Delivery
Variable
aOR (95% CI) p value aOR (95% CI) p value
Malaria 1.92 (1.00, 3.67) 0.040∗ NS NS NS
Maternal age 0.95 (0.93, 0.98) 0.001∗ 0.95 (0.89, 1.00) 0.04∗
IPTp NA NA NA 0.73 (0.57, 0.93) 0.01∗
No significant difference between S. haematobium infection and anaemia. aOR: adjusted odds ratio; CI: confidence interval; NA: not available (no IPTp
treatment during first ANC); NS: not statistically signi cant. ∗fi statistical significance.
The Ghana Demographic Health Survey Report reported We observed a significant association of malaria and
that 45% of pregnant women were anaemic in Ghana [56]. anaemia, suggesting that malaria contributes to anaemia
Our study recorded that over 50% of pregnant women were during pregnancy [16]. Using the logistic regression model,
anaemic which is a clear indication of a higher prevalence of pregnant women infected with P. falciparum have higher
anaemia in pregnant women in our study areas than the odds of being anaemic. Furthermore, when anaemia was
national average. Anaemia prevalence studies conducted in stratified (mild, moderate, and severe), malaria remained
Tamale and Dangme East District in Ghana showed higher strongly associated with higher risk of severe anaemia. The
prevalence of 63% and 66%, respectively [22, 52], which odds of anaemia in pregnant women as they get older was
was higher than our study prevalence, indicating a concern lowered in our study.
of high anaemia and the need to intensify its reduction in An older population of pregnant women in BH than in
pregnancy [52]. AH indicated a higher number of primigravid women in
We observed better Hb outcomes with age, similar to AH (55%) than BH (42%). Younger women in our study
studies in Bangladesh, China, and Ghana [57–59]. However, chose to attend ANC earlier at AH compared to BH. Malaria
Kwabre East Municipality of Ghana reported a higher risk prevalence at AH and BH at delivery was significantly lower
of anaemia in older women, and no variation of age and than ANC, although participants at ANC were not the same
Hb was recorded by Akowuah et al. and Lumbanraja as delivery. This report testifies the benefits of routine ANC
et al. [59, 60]. program which includes malaria diagnosis and IPTp in
P. falciparum infection was associated with decreased Hb ensuring healthy pregnancies and reduction in malaria prev-
levels in pregnant women, and age was strongly associated alence [30]. Adherence to IPTp protocol in the study partic-
with increased Hb levels for ANC and at the point of deliv- ipants as a preventive treatment for malaria during
ery. As previously reported, the destruction of P. falciparum- pregnancy was commendable, especially with more than 2
infected erythrocytes during schizont rupture is linked to doses [30].
decreased Hb levels during pregnancy [17]. We observed that IPTp was associated with increased Hb
Our study observed age to be another factor associated outcomes [52], and more than 2 doses of IPTp received dur-
with malaria, and this could be as a result of parity-related ing pregnancy led to improved Hb levels at the point of
immunity [31] and a gradual build-up of immunity to P. fal- delivery, agreeing with previous studies by Wilson et al. in
ciparum infection in older women which reduces their infec- Ghana [61]. However, reports from Sekondi Takoradi in
tion risk compared to younger women [17]. Ghana showed that Hb levels were not different from IPTp
6 Journal of Parasitology Research
users and nonusers [62]. They associated this difference to We confirm in Ghana that while there is routine preven-
the gradual emergence of resistance in P. falciparum parasite tive treatment of malaria in pregnancy, routine diagnosis
to IPTp as has been observed by others [46, 62, 63]. Inade- and anthelminthic treatment for pregnant women after
quate malaria immunity and compromised drug quality their first trimester are yet to be implemented. Women aged
[52] were also identified as factors that could influence Hb. 18-25 years living in endemic areas live almost a quarter of
IPTp played a protective role in preventing anaemia during their reproductive lives being pregnant and more than 50%
pregnancy. When adjusted for age, this protective role still of reproductive lives lactating [6]. Suspension of anthel-
remained significant. Our findings are similar to observation minthic treatment for a year or more could have severe
of better Hb outcomes and IPTp by Agyeman et al. [52]. consequences on morbidity and quality of life for these
Urogenital schistosomiasis is another parasitic infection women [6, 25].
known to be associated with anaemia in pregnancy [18]. Starting a program at ANC to routinely diagnose and
Its prevalence of 4% at ANC and 2% at delivery was within treat pregnant women could improve Hb levels as previous
the range (0.30-4.53%) observed by others in northern MDA among pregnant women reduced anaemia by 23%
region and Dangme East District of Ghana [21, 22, 64]. [18, 23]. Furthermore, deworming of pregnant women has
Our study did not find an association between S. haemato- been associated with a 14% reduction in neonatal death risk
bium infections and anaemia, even though previous studies proportionally in low and high transmission countries [79].
have reported an association [18, 22, 24]. Tay et al. found
a significant association between S. haematobium infections 5. Study Limitations
and anaemia [22], but infection intensities were not reported
in their study to suggest if intensities played a role in the At delivery, we were faced with a difficulty of collecting urine
anaemia observed [22]. We are of the view that no associa- samples from pregnant women, but an effort was made to
tion between S. haematobium infection on Hb levels could recruit as many participants as possible. Urogenital schisto-
result from lack of statistical power due to the low number somiasis prevalence was estimated by microscopy which has
of S. haematobium infections (n = 25) observed in our study a lower sensitivity compared to molecular methods; there-
at ANC. Low S. haematobium prevalence could be related to fore, we anticipate that a number of schistosomiasis cases
age of study participants. may have been missed in low intensity infections in our
Although schistosomiasis affects all age groups, there is a study population.
higher risk of infection in school-aged children, who harbor
peak infections [35, 65–68] and are actively and constantly 6. Conclusion
engaged in water contact activities such as swimming and
fetching water for domestic purposes. Individuals aged We report that anaemia is still a concern for pregnant
below 16 years have been identi ed as the main group that women at ANC and delivery. P. falciparum infection wasfi
actively shed S. haematobium eggs in most endemic commu- associated with low Hb levels with increased odds of becom-
nities [69, 70]. Typically, most of the participants were older ing anaemic in pregnancy. However, more than two IPTp
than 20 years when prevalence of schistosomiasis is lowest doses administered during pregnancy were associated with
compared to younger children (<20) who are more exposed increased Hb levels among pregnant women. S. haemato-
and/or susceptible [71, 72]. This could explain the low inten- bium-related anaemia was not significant in our study.
sities of infection observed in our study. Another reason for While routine diagnosis and treatment for PAM were imple-
age variation with schistosomiasis could be related to immu- mented in our study hospitals, no evidence of routine diag-
nity. As has been found previously, older women are capable nosis and treatment was seen for schistosomiasis during
of developing robust immunity which tends to lower their ANC. We suggest routine diagnostic tools which are rapid,
risk of reinfection [73]. It would not be surprising if these sensitive, and cheaper as well as treatment of S. haemato-
women may have been previously treated during MDA by bium infections in endemic areas to reduce schistosomiasis
Volta River Authority (VRA), Ministry of Health (MOH), during pregnancy.
and Ghana Health Service (GHS) before their current preg-
nancy, ensuring lowered S. haematobium prevalence [74]. Data Availability
The challenge for pregnant women is their exemption from The data that support the findings of this study are available
MDA, although they are an important risk group who could from the corresponding author (Naa Adjeley Frempong)
be fueling schistosomiasis transmission cycle. upon reasonable request.
We observed that 96% of pregnant women had low
intensity S. haematobium infections and therefore could Conflicts of Interest
not determine S. haematobium intensity and its association
with anaemia. Nonetheless, the only high infection intensity No competing interest has been identified.
(61 eggs/10ml) recorded the lowest Hb level, agreeing with
observations from other studies [24, 72, 75, 76]. Anaemia Authors’ Contributions
due to schistosomiasis results from blood loss as eggs with
terminal spines pass through the urogenital tract in S. hae- NAF, AKA, DC, MO, and NTN were responsible for the
matobium infection [24, 77, 78], leading to low Hb levels conception and design of the study or analysis and interpre-
in the host. tation of data. NAF, AKA AYD, MO, KAK, WKA, and DC
Journal of Parasitology Research 7
were responsible for drafting the paper or substantially revis- [9] M. Getachew, D. Yewhalaw, K. Tafess, Y. Getachew, and
ing it. NAF, DC, NTN, AKA, MFO, AYD, AM, WKA, CA, A. Zeynudin, “Anaemia and associated risk factors among
and BA were responsible for approving the final version to pregnant women in Gilgel Gibe dam area, southwest Ethiopia,
be published. NAF, DC, AKA, MKO, AYD, AM, WKA, Southwest Ethiopia,” Parasites and Vectors, vol. 5, no. 1,
KAK, BA, NTN, and CA were responsible for accepting pp. 1–8, 2012.
accountability for all aspects of the work. [10] World Health Organization, World malaria report 20222022
[cited 2022 Feb 27]. https://www.who.int/teams/global-
malaria-programme/reports/world-malaria-report-2022.
Acknowledgments [11] Speakupafrica.org, “Ghana launches cross-parliamentary cau-
cus on malaria to accelerate elimination efforts,” 2022 Jul 14.
We thank the Ghana Health Service for granting us the https://www.speakupafrica.org/ghana-launches-cross-
permission to work in the study hospitals. Our gratitude parliamentary-caucus-on-malaria-to-accelerate-elimination-
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