Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 19  |  Issue : 1  |  Page : 43-48

Co-infection of malaria and intestinal parasites among pregnant women in Edo State, Nigeria


1 Department of Medical Laboratory Science, University of Benin, Benin City, Edo State, Nigeria
2 Department of Animal and Environmental Biology, University of Benin, Benin City, Edo State, Nigeria
3 Department of Obstetrics and Gynaecology, Central Hospital, Benin City, Edo State, Nigeria

Date of Web Publication7-Jun-2017

Correspondence Address:
Frederick O Akinbo
Department of Medical Laboratory Science, University of Benin, Benin City, Edo State
Nigeria
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jomt.jomt_42_16

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  Abstract 


Background: Parasitic infection is a cause of maternal and neonatal morbidity and mortality. This study was conducted to determine the co-infection of Plasmodium falciparum and intestinal parasites among the pregnant women in Edo State, Nigeria.
Materials and Methods: A total of 601 participants, consisting of 401 pregnant women attending antenatal clinics and 200 non-pregnant controls, were recruited in this study. The blood and stool specimens were collected from each participant. P. falciparum and intestinal parasites were diagnosed using standard techniques.
Results: An overall prevalence of 43.1% of co-infection of P. falciparum and intestinal parasites was observed among the pregnant women. P. falciparum parasitaemia prevalence was 24.9%, whereas the prevalence of intestinal parasites was 18.2%. The most common co-infections among the pregnant women were either P. falciparum/Entamoeba histolytica (16.7%) or P. falciparum/Ascaris lumbricoides (16.7%). Pregnancy status, gestational age and anaemia correlated with the co-infection of P. falciparum/intestinal parasites.
Conclusion: Measures to reduce P. falciparum/intestinal parasite co-infection and their effect on pregnant women are advocated.

Keywords: Benin city, co-infection, intestinal parasites, P. falciparum


How to cite this article:
Akinbo FO, Olowookere TA, Okaka CE, Oriakhi MO. Co-infection of malaria and intestinal parasites among pregnant women in Edo State, Nigeria. J Med Trop 2017;19:43-8

How to cite this URL:
Akinbo FO, Olowookere TA, Okaka CE, Oriakhi MO. Co-infection of malaria and intestinal parasites among pregnant women in Edo State, Nigeria. J Med Trop [serial online] 2017 [cited 2020 Aug 14];19:43-8. Available from: http://www.jmedtropics.org/text.asp?2017/19/1/43/207593




  Introduction Top


Globally, parasitic infections are among the most widespread of all chronic human infections.[1],[2] Maternal mortality continues to be a major health challenge in developing countries with almost 600,000 women dying annually due to complications of pregnancy and child birth.[3]

Every single day, Nigeria loses about 2300 under-5 year olds and 145 women of childbearing age, which makes the country the second largest contributor to the under-5 and maternal mortality rate in the world. It was also emphasized that a woman’s chance of dying from pregnancy and childbirth in Nigeria is one in 13, and survivors suffer because of several ailments and disabilities.[4] A previous study from Edo State gave a maternal mortality rate of 2282 out of 100,000 deliveries.[5] About 99% of all maternal mortality occurs in women living in rural and poor communities. Pregnancy is associated with immunosuppression and an increased risk of infection including parasitic infections and severe forms of malaria[6],[7],[8] Malaria during pregnancy is a major public health problem in endemic tropical and subtropical countries, because it is responsible for substantial proportions of foetal and maternal morbidity and mortality.[9] There exists an extensive geographic overlap between Plasmodium falciparum and helminth infections in Africa.[10] It has been observed that women with intestinal helminth infections are 4.8 times more likely to suffer from malaria.[11] Intestinal helminthiases have also been known to aggravate pre-existing anaemia, which is common among the pregnant women in sub-Sahara Africa, by decreasing the appetite, thereby leading to reduction in food and iron intake. In addition, they also cause blood loss of their own, as in the case of hookworm infection.[12] Nevertheless, co-infection of P. falciparum and hookworm has been reported to have an additive impact on haemoglobin by increasing the susceptibility to P. falciparum, which could have a great consequence on the pregnancy outcome, because it results in intrauterine growth retardation, low birth weight, pre-term delivery and neonatal mortality.[13] The adverse perinatal outcomes may include, but not restricted to, premature, hypotrophic neonates and stillbirths in the malarial population, which may be linked to intervillous macrophages that decrease the maternal blood output and the perivillous excess of fibrin that reduces the materno-foetal exchanges.[14]

Intestinal helminthic infection during pregnancy may contribute significantly to the degree of anaemia in pregnant women as a result of high parity, low nutritional status and poor personal hygiene, which are predominantly observed in developing countries.[15] However, studies on the co-infection of P. falciparum and intestinal parasites among the pregnant women in Edo State, Nigeria are lacking. This study was conducted to determine the prevalence of co-infection of P. falciparum and intestinal parasites and the correlates of co-infection among the pregnant women in Edo State.


  Materials and methods Top


Study area

This study was conducted at the Central Hospital, Benin City, Edo State, a secondary health institution that receives referrals from Primary Health Care centres across the state.

Study population

This study was conducted between November 2014 and March 2016. A total of 601 participants, consisting of 401 pregnant women attending antenatal clinics at the Central Hospital and 200 non-pregnant apparently healthy women who served as controls, were randomly recruited. The sample size was determined using the following formula:



where N is the sample size, p is the prevalence of co-infection of malarial and intestinal parasites in the previous study, q is 100−p and l is a permissible error (5% of p).

Assuming a prevalence of 72.7%, therefore, q = 27.3 and l = 3.635, N = 4 × 72.7 × 27.3/3.6352 and N = 600.8 rounded up to 601.

Therefore, 601 samples were collected.

Asymptomatic pregnant women who accepted to participate were recruited for this study. The participants on anti-malarial or anti-parasitic agents, those who recently concluded a course of treatment for malaria or enteric parasites and those who did not consent to participate were excluded from this study. A structured questionnaire was administered to obtain the demographic characteristics from each participant. Informed consent was obtained from each participant prior to specimen collection. The protocol for the study was approved by the Ethics and Research Committee, Ministry of Health, Benin City, Edo State, Nigeria.

Collection and processing of specimens

The blood and stool specimens were collected from each participant. About 5 ml of venous blood was collected from each participant and dispensed into an ethylenediaminetetraacetic acid container and mixed. Freshly voided stool specimen was collected from each participant into a pre-labelled universal container. P. falciparum was diagnosed using a previously described method.[11] Briefly, thick and thin blood films were made from each blood specimen, allowed to air-dry and stained in 10% Giemsa stain solution for 30 min. The stained films were rinsed in a buffer solution and drained. The films were examined for the presence of Plasmodium and speciation.[16]

The haemoglobin concentration was determined using an automated analyzer − Sysmex Kx-21 (Sysmex Cooperation, Kobe, Japan). Anaemia was defined as haemoglobin concentration <11 g/dl.[17]

The stool specimens were processed using formol-ether concentration technique, and the smears were examined for intestinal parasites using a previously described method.[18] Briefly, 1 g of the stool specimen was mixed in 4 ml of formal saline. The mixture was then sieved, and, to the filtrate, 4 ml of diethyl ether was added and agitated. The mixture was centrifuged for 1 min at 3000 rpm. The supernatant was discarded, and saline/iodine preparations were made from the deposit. The smears were examined for the presence of intestinal parasites.

Statistical analysis

The data obtained were analyzed using chi-square (X2) test and odds ratio (OR). All statistical analyses were performed using the statistical software INSTAT® (Graph PAD software Inc., La Jolla, CA, USA).


  Results Top


A total of 173 (43.1%) out of 401 pregnant women and 11 (5.5%) out of 200 non-pregnant women had both intestinal parasitic and malaria parasitic infections. A prevalence of 18.2 and 24.9% of intestinal parasitic infection and malaria parasitaemia respectively were observed among the pregnant women. Pregnancy was significantly associated with co-infection [OR = 13.037; 95% confidence interval (CI) = 6.879, 24.709; P < 0.0001]. Similarly, pregnancy was associated with P. falciparum and intestinal parasitic infections individually (OR = 10.742; 95% CI = 4.621, 24.971; P < 0.0001; OR = 8.680; 95% CI = 3.447 and 21.855; P < 0.0001). P. falciparum was the only species of malaria parasite observed in this study [Table 1].
Table 1: Effect of pregnancy status on parasitic infections

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Age, marital status and location did not significantly affect the prevalence of malaria and intestinal parasitic co-infections (P > 0.05). The pregnant women in their 3rd trimester had a significantly higher prevalence of co-infection of malaria and intestinal parasites (P = 0.0376), whereas anaemia during pregnancy, only, was significantly associated (OR = 4.829; 95% CI = 2.895, 8.054; P < 0.0001) with co-infection of malaria and intestinal parasites [Table 2]. P. falciparum (24.9%), Ascaris lumbricoides (9%), hookworm (3%), Trichuris trichiura (2.5%), Entamoeba histolytica (2.7%) and Giardia lamblia (1%) were the parasites recovered in this study with P. falciparum (3%), A. lumbricoides (2%) and hookworm (0.5%) recovered only from non-pregnant women at lower prevalence than that recovered from their pregnant counterparts [Table 3].
Table 2: Effect of risk factors on the co-infection of P. falciparum/intestinal parasites

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Table 3: Frequency of parasites recovered among the pregnant and non-pregnant women

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Co-infection of both P. falciparum/E. histolytica and P. falciparum/A. lumbricoides predominated with a prevalence of 16.7% each among the pregnant women. There was no co-infection of malaria and intestinal parasites observed among the non-pregnant women [Table 4].
Table 4: Parasitic combinations among the pregnant women

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  Discussion Top


Parasitic infection during pregnancy has serious consequences for the mother and her child.[19] An overall prevalence of 43.1% of co-infection of P. falciparum/intestinal parasites was observed among the pregnant women. The prevalence of co-infection observed in this study is similar to the 48.3% reported by Egwunyenga et al.[15] However, our prevalence is higher than the 7.7% in Southwest Ethiopia,[20] 13% in Anambra State, Nigeria[21] and 16.6% in Ghana.[22] Geographical zones described on the basis of simple geography, altitude, vegetation and the location of settlements have been found to correlate spatially with parasite infections.[23] This may explain the reason for our finding. Pregnancy has been reported to lower immunity as a result of general immunosuppression sustained by an elevated level of serum cortisol, which allows foetal allograft retention but renders the women susceptible to various infectious diseases.[24] Helminthes infection has been reported to influence susceptibility to other infections including malaria.[25],[26] An explanation for this observation is that the presence of T-regulatory cells is amplified during helminthes infection, and if present in sufficient amount, could induce a non-specific suppression,[27] making individuals susceptible to infections such as malaria.[28] The prevalence of co-infection of P. falciparum/intestinal parasites was strongly associated with pregnancy status, and the pregnant women appear to have 3–24-fold increased risk of acquiring P. falciparum and intestinal parasitic infections. The prevalence of 24.9% of malarial infection reported in our study is similar to the 21.9% observed by Noedl et al.[29] in Cameroon, but lower than the 36.3% reported in Ghana, 44.8% in Edo State, Nigeria and 63% in Ghana.[22],[30],[31] Soil contamination by open defecation and poor sanitary habits are a major risk in the transmission of intestinal parasitic infections in the community.[32],[33] The prevalence of 18.2% of intestinal parasitic infection among the pregnant women in our study is similar to the 17% in Uganda[34] but differ from the 33.4% in Adamawa State, Nigeria, 34% in Mexico and 42.2% in Southeastern Nigeria. [35, 36, 37] The reasons for these variations could be because of differences in geographical locations and sanitary practices.

The pregnant women within the 21–30 years age group are seen to be less hygiene conscious than the older women[28] and are more likely to acquire infectious agents through that habit. Surprisingly, age did not significantly affect the co-infection of P. falciparum and intestinal parasites among the pregnant women. This finding agrees with the work of Getachew et al.[20] The reason for this finding is unclear.

Generally, gestational age significantly affected the prevalence of co-infection of P. falciparum/intestinal parasites among the pregnant women, and those in the 3rd trimester presented with the highest prevalence (51%). The reason for this observation may be due to the fact that many pregnant women, especially those in their 3rd trimester, registered late for antenatal care.[38]

Reduced mean haemoglobin concentration levels are attributed to chronic loss of blood and iron.[15] Hookworm and other soil-transmitted helminths and malaria during pregnancy have been reported as the cause of pathological chronic loss of blood and iron in the tropics.[39],[40] Low nutritional status and staple foods such as rice, cassava and maize are poor sources of folate and iron and, altogether, have been implicated to aggravate anaemia in Plasmodium/intestinal helminthes co-infection among the pregnant women.[41] Anaemia significantly affected the prevalence of co-infection of P. falciparum/intestinal parasites among the pregnant women in this study. This finding is consistent with the study of Egwunyenga et al.[15] in Eku, Jos and Bauchi, where lower haemoglobin levels were observed.

The locations of the residence of the pregnant women did not affect significantly the prevalence of co-infection of P. falciparum/intestinal parasites. Poor sanitary conditions and life style difference of the communities could serve as breeding sites for mosquitoes and, thus, increase the risk of being bitten and acquiring Plasmodium infection. This may explain the reason for our observation.

P. falciparum, A. lumbricoides, hookworm, T. trichiura, E. histolytica and G. lamblia were the parasites recovered among the pregnant women. Similar parasites were recovered among the pregnant women in a study conducted by Egwunyenga et al.[15] except for E. histolytica and G. lamblia. Generally, P. falciparum was the most prevalent parasite observed. This finding agrees with the study of Egwunyenga et al.[15]

The most common co-infection was between P. falciparum/E. histolytica and P. falciparum/A. lumbricoides. Other combinations with a decreasing order of prevalence were A. lumbricoides/T. trichiura, A. lumbricoides/hookworm, P. falciparum/hookworm, P. falciparum/A. lumbricoides/T. trichiura, hookworm/T. trichiura, P. falciparum/T. trichiura, E. histolytica/hookworm, P. falciparum/A. lumbricoides/hookworm, P. falciparum/T. trichiura/hookworm and A. lumbricoides/G. lamblia/hookworm. The reason for this co-infection could be due to behavioural and environmental factors leading to increased exposure to these infectious agents.[42]


  Conclusion Top


An overall prevalence of 43.1% of co-infection of P. falciparum/intestinal parasites was observed among the pregnant women in Edo State, with P. falciparum having a prevalence of 24.9 and 18.2% for intestinal parasitic infection. Pregnancy status, gestational age and anaemia significantly affected the co-infection of P. falciparum/intestinal parasites among the pregnant women. P. falciparum, A. lumbricoides, hookworm, T. trichiura, E. histolytica and G. lamblia were the parasites recovered among the pregnant women, whereas P. falciparum, A. lumbricoides and hookworm were the parasites recovered among the non-pregnant women. P. falciparum was the predominant parasite observed in this study. The most common co-infection was between P. falciparum/E. histolytica and P. falciparum/A. lumbricoides. Measures to reduce the effects of co-infection of P. falciparum/intestinal parasites on pregnant women are advocated.

Acknowledgements

We thank the Management of Edo State Hospital Management Board for permission to conduct this study. The authors also appreciate the patients who participated in this study for their co-operation.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


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