Prevalence of Malaria Parasite among Pregnant Women Attending to Saudi Kassala Teaching Hospital in Kassala State, Eastern Sudan

Objective Malaria during pregnancy is a priority area for malaria research and control as pregnant women represent a high risk group for severe malaria, and the presentation of malaria during pregnancy varies according to the level of transmission in the area; so the aim of this study is to determine the prevalence rates of malaria parasite among pregnant women attending to Saudi Kassala Teaching hospital in Kassala state, 2022. Methods A cross-sectional study was carried out in Saudi Kassala Teaching hospital in Kassala State. This study involved one hundred and eighty-five blood samples collected from pregnant women who was then examined by using blood films and ICT for malaria, and the data were collected by a structured questionnaire and analyzed using SPSS version 21. Results The prevalence of malaria among pregnant women was 2.2% (95% CI: 0.006–0.054). There was no significant difference among the different age groups with respect to the prevalence of malaria (P value = 0.483). The prevalence of malaria in rural residency was 2.2%, and this was significantly more common than the urban residency (P value = 0.021). When compared across the gestational trimesters, there was no significant difference between them (P value = 0.518). The number of gravidity is not related to malaria infection (P value = 0.737). The presence of symptom compliant of malaria during pregnancy does not suggest the presence of malaria (P value = 0.152). No difference was found between the different educational levels with respect to the prevalence of malaria (P value = 0.362). The result showed that there was 1 (0.5%) negative result in ICT which was positive in blood film for malaria (BFFM) and there were 3 (1.6%) positive malaria parasites by both methods in all 185 samples with statistically insignificant differences (P = 0.703). Conclusion Plasmodium falciparum was only species detected in this study. Malaria among pregnant women was more prevalent in rural areas. However, other factors such as age, gestational age, gravidity, and educational level do not affect the prevalence of malaria in pregnant women. The presence of symptomatic compliant of malaria during pregnancy does not suggest the presence of malaria. The use of ICT or BFFM has similar diagnostic outcome for malaria in pregnancy.


Introduction
Malaria is caused by Plasmodium species, and P. falciparum is more common in Africa.According to WHO, Sudan carries the heaviest burden accounting for 61% of deaths in the Eastern Mediterranean [1].Tere are geographically variations in the epidemiology of this [2].Of all the species of Plasmodium parasites, Plasmodium falciparum is responsible for the highest disease burden [3].Te other species have low disease burdens [4].An interaction between the host, the vector, and the parasite is needed for propagation of the disease [5].Other rare modes of transmission include transplacental, through blood transfusions, or through contaminated needles or syringes [6].Te early symptoms of malaria are fu-like presentation which is similar among the diferent species of malaria [7].Te main symptom of malaria is fever, and other symptoms may include nausea, vomiting, anorexia chills, headache, and myalgia [8].In pregnancy, malaria is a major health issue; it has been associated with many maternal and fetal complications such as anemia with pregnancy and stillbirth, respectively [9].In sub-Saharan Africa, malaria in pregnancy is a disease burden caring mortalities as well as morbidities [10].Tis is mainly due to Plasmodium falciparum [11].In areas with low malarial transmission, 25% of severe anemia with pregnancy is due to malaria, and placental malaria doubles the risk of low birth weight.However, in areas with high malarial transmission, malaria-related fetal growth restriction may be twice as high as malaria-related preterm delivery [12].Pregnant women are more liable to malaria which adversely afects pregnancy.It is one of the chief causes of maternal mortality in Sudan, especially with Plasmodium falciparum which cause high levels of parasitemia, hypoglycemia, acute pulmonary edema, fetal distress, premature labor, spontaneous abortions, and still births [13].Te present study aims to determine the prevalence rate of malaria parasite among pregnant women attending to Saudi Kassala Teaching hospital in Kassala State, as the malaria trend increases by as much as over 40% between 2015 and 2020 [1].

Study Design and Study Population.
Te study was a descriptive cross-sectional hospital-based study, conducted from February to September 2022.It was conducted in Saudi Kassala Teaching hospital in Kassala state among 185 pregnant women attending the hospital for either monthly follow-up visit or delivery.Kassala state is located in the east of the Sudan.It has a total population of 1.5 million [14].
Tis state is served by Saudi Kassala teaching hospital, which is the only hospital that provides antenatal and delivery service to the state population.In 2022, the hospital had 7498 spontaneous vaginal deliveries, 18 assisted vaginal deliveries through ventouse suction, and 5,586 cesarean section [15].
Sample size was calculated using the following formula: where z is the normal standard deviation (1.96), p is the frequency of occurrence of an event, q is the frequency of nonoccurrence of an event, and d is the degree of precision (0.05) [16].
So, when the margin of error is 5%, confdence level is 95%, and prevalence is 13.7% [17].( Te calculated sample is 182; however, a sample of 185 was taken for more accuracy and precision.
2.1.1.Inclusion Criteria.Inclusion criteria included pregnant women attending Saudi Kassala Teaching hospital from February to September 2022.

Exclusion Criteria.
Exclusion criteria included pregnant women referred from outside of the state of Kassala and pregnant women who were diagnosed with malaria by laboratories other than the Saudi Kassala Teaching hospital laboratory.

Methodology of Laboratory Investigations.
A 5 ml of blood sample was collected from pregnant women in EDTA container.Tin and thick microscopic examination and immunochromatographic test (ICT) were used for confrming the diagnosis.

Blood Films.
Tick and thin blood flms were airdried.Methanol was used to fx the thin flms.10% Giemsa solution was used to stain the flms, and the stain was allowed for 10 minutes, then washed with clean water, and left to air-dry.100x magnifcation lenses under oil immersion were used to view the flms [18].

Rapid MAT Test. Tis test has a membrane strip coated with monoclonal antibodies. Te frst test line for
Plasmodium falciparum is coated with monoclonal antibodies against histidine-rich protein 2 while the second line for Plasmodium vivax is coated with monoclonal antibodies specifc to lactate dehydrogenase [19].
At room temperature, port A in the test kit was flled with 5 µl of anticoagulated blood using a micropipette, and two drops of bufer was added in port B using plastic dropper.Te results were interpreted after 20 minutes [18].

Data Collection and Analysis.
After estimating the sample, a questionnaire was designed to collect the demographic data as well as data related to the gestational age, gravidity, and malaria symptoms during pregnancy.
Te data were analyzed using frequencies and crosstabulation using chi-square in Statistical Package for Social Science (SPSS) computer program version 21.Pregnant women who are less than 16 years of age were married, and as a result, they were considered emancipated, and the informed written consent was taken accordingly.

Ethical Approval and
Informed written consent from illiterate pregnant women was taken with the participation of the husband as a legal guardian.
Of the 185 women approached, the data were successfully collected and no refusal was noted.
All the methods were carried out in accordance with local regulations and guidelines.

Results
Of the total 185 pregnant women selected, the response rate was 100%.Te result showed that out of 185 pregnant women, only 4 (2.2%, 95% CI: 0.6-5.4) were infected with malaria parasite, and all of them were infected by Plasmodium falciparum (Table 1).
Te number of samples examined for malaria parasites among pregnant women in each age group was 85, 88, and 12 in age groups of 15-25 years, 26-35 years, and 36-45 years, respectively; the result showed that 3 (3.5%)were positive in the age group 15-25 years and 1 (1.1%) in the age group of 26-35 years.Tere was no signifcant diference among the diferent age groups with respect to the prevalence of malaria at P value � 0.483 (Table 2).
Te result revealed that all the positive cases of malaria were found among pregnant women living in rural residency 4 (5.0%) compared with 0 (0%) positive cases in the urban residency, and these diferences in rates were signifcant at P � 0.021 (Table 3).
Te result showed that out of the 70 illiterate pregnant women, 3 (3.4%)were positive for malaria parasite, and out of the 39 who had secondary educational level, 1 (2.6%) was positive for malaria parasite, while the other educational groups level was negative for malaria parasite with statistically insignifcant diferences in rates at P � 0.362 (Table 4).
When compared across the gestational trimesters, the result showed that pregnant women in frst and second trimesters were negative for malaria, while, in third trimester, the result showed 4 (2.8%) positive for malaria, with statistically insignifcant diferences rate at P � 0.518 (Table 5).
Out of the 39 pregnant women complaining of malaria symptoms which include fever, nausea, vomiting, anorexia, chills, headache, and myalgia [8], only 2 (5.1%) were positive for malaria.Among the remaining 146 pregnant women who had no symptoms, only 2 (1.4%) were positive for malaria parasite; thus, the presence of malaria symptoms does not suggest the presence or absence of malaria (Table 7).
Te result showed that there was 1 (0.5%) negative result in ICT which was positive in BFFM and there were 3 (1.6%)positive malaria parasites by both methods in all 185 samples, with statistically insignifcant diferences at P � 0.703 (Table 8).

Discussion
Te study showed that the prevalence of malaria among pregnant women was 2.2% (95% CI: 0.6-5.4).Meanwhile, the department of statistics at Saudi Kassala Teaching hospital recorded a prevalence of 1.79% in 2020 and 1.57% in 2011.Tis is relatively similar to the results of our study, and these indicate that malaria among pregnant women was relatively stable throughout the last 3 years [15].
According to our study, Plasmodium falciparum was the only species of malaria parasite detected, and this was similar to that of a study done in Al Jabalian Locality, White Nile state, Sudan, which has similar result [20].Tis also is in accordance with the World Health Organization (WHO), where Plasmodium falciparum is the predominate species in Africa [21].
We found that the highest prevalence of malaria in pregnancy was 3.5% recorded among age group of 15-25 years.However, there was no signifcant association between the prevalence of malaria and the age group of pregnant women, and this fnding is similar to another study done in eastern Sudan [17].Tis similarity may be because both studies were conducted in same region, i.e., eastern Sudan.
Malarial infection was signifcantly higher in women from rural areas compared to woman from urban areas; this fnding was similar to the fndings reported by Omer and colleagues [10].Tis higher prevalence among rural areas may be attributed to the low socioeconomic status at the rural communities.
Even though malaria prevalence is relatively higher in the noneducated group (4.3%), there is no signifcant association between the education level and malaria infection, and this fnding agrees with the fnding reported by Suliman and colleagues [20].
Tere is no association between the gestational age and malaria, and this fnding is similar to that of a study done by Tahita and colleagues [22].
Tis study showed no signifcant association between malaria and gravidity, and this fnding was similar to that of another study done in eastern Sudan by Adam and colleagues [17].
Our study shows that symptoms of malaria were not discriminative for malaria infections (value � 0.152).Tis is similar to the fndings of the study done by Tahita and colleagues [22].Te difculty of discrimination may be because certain malaria-related symptoms may mimic pregnancy-related symptoms.
When the blood flms and ICTs were compared for the diagnosis of malaria parasite, the diference between the two modalities was not statistically signifcant (P value � 0.751).Tis was similar to the results obtained by Latha and colleagues where rapid diagnostic test was found equally sensitive to microscopy [23].

Conclusions
Plasmodium falciparum was the only species detected in this study.Malaria among pregnant women was more prevalent in rural areas.However, other factors such as age, gestational age, gravidity, and educational level do not afect the prevalence of malaria in pregnant women.
Te presence of symptomatic compliant of malaria during pregnancy does not suggest the presence of malaria.
Te use of ICT or BFFM has similar diagnostic outcome for malaria in pregnancy.

Journal of Tropical Medicine
Consent to Participate.All the examination protocols were approved by the ethical committees of both the faculty of medicine and health sciences at 2 Journal of Tropical Medicine the University of Kassala and Saudi Kassala Teaching hospital in Kassala State.Te informed written consent was taken from each pregnant women participated in this study.

Table 2 :
Prevalence of malaria among pregnant women by age group.

Table 3 :
Prevalence of malaria among pregnant women by residency.

Table 4 :
Prevalence of malaria among pregnant women by educational level.

Table 5 :
Prevalence of malaria among pregnant women by gestational age.

Table 6 :
Prevalence of malaria among pregnant women by gravidity.

Table 1 :
Overall prevalence of malaria among pregnant women.

Table 7 :
Prevalence of malaria among pregnant women by symptoms.

Table 8 :
Comparison between BFFM and ICT in diagnosis of malaria among pregnant women.