Open Access

Prevalence and risk factors for Plasmodium falciparum malaria in pregnant women of eastern Sudan

Malaria Journal20054:18

DOI: 10.1186/1475-2875-4-18

Received: 15 January 2005

Accepted: 13 April 2005

Published: 13 April 2005

Abstract

Background

Pregnant women are more susceptible to malaria, which is associated with serious adverse effects on pregnancy. The presentation of malaria during pregnancy varies according to the level of transmission in the area. Our study aimed to demonstrate the prevalence and risk factors for malaria (age, parity and gestational age) among pregnant women of eastern Sudan, which is characterized by unstable malaria transmission.

Methods

The prevalence and possible risk factors for Plasmodium falciparum malaria were investigated in 744 pregnant Sudanese women attending the antenatal clinic of New Haifa Teaching Hospital, eastern Sudan, during October 2003-April 2004.

Results

A total 102 (13.7%) had P. falciparum malaria, 18(17.6%) of these were severe cases (jaundice and severe anaemia). Univariate and multivariate analysis showed that, age and parity were not associated with malaria. Women who attended the antenatal clinic in the third trimester were at highest risk for malaria (OR = 1.58, 95% CI = 1.02–2.4; P < 0.05).

Women with malaria had significantly lower mean haemoglobin (9.4 g/dl, 95% CI 9.1–9.7 versus 10.7, CI 10.6–10.8, P < 0.05). A significantly lower haemoglobin was observed in those with severe falciparum malaria compared to non-severe form (8.3 g/dl, 95% CI 7.6–9.1 versus 9.4, 95% CI 9.1–9.7, P = < 0.05).

Conclusion

The results suggest that P. falciparum malaria is common in pregnant women attending antenatal care and that anaemia is an important complication. Preventive measures (chemoprophylaxis and insecticide-treated bednets) may be beneficial in this area for all women irrespective of age or parity.

Background

Pregnant women are more susceptible to malaria, which causes serious adverse effects including abortion, low birth weight and maternal anaemia. It is the leading cause maternal mortality in Sudan [17].

The presentation of malaria during pregnancy varies according to the pre-existing immunity of the mother. Women living in areas of low transmission have little immunity to malaria which can cause severe syndromes, such as cerebral malaria and pulmonary oedema. In contrast, those who live in areas of stable malaria transmission enjoy greater immunity and experience fewer symptoms during episodes of malaria, although they commonly develop severe anaemia as consequence of the infection [1, 2, 5, 8, 9].

Understanding the epidemiology of malaria during pregnancy provides important insight into relevant immunological processes and facilitates decision on control strategies. Although there are extensive studies in highly endemic African countries [1, 2, 5, 6, 1012], there is little published data available for Sudan, an African country where P. falciparum malaria transmission is unstable in the eastern region [13]. The study was conducted to investigate the prevalence and associated risk factors for P. falciparum malaria in pregnant women from eastern Sudan.

Patients and methods

Data collection

Pregnant women attending antenatal clinic (booking visit) of the New Haifa Teaching Hospital, eastern Sudan, during the period October 2003-May 2004 were approached to participate in the study. After verbal consent, questionnaires were administered requesting demographic informations on age, parity, gestational age and history of maternal illness. Gestational age was calculated from the last menstrual period and confirmed by ultrasound, when clinically indicated. Physical examination was completed to identify signs of severe malaria [14] and also obstetrical examination (blood pressure, pallor, fundal level and foetal heart sound).

Laboratory methods

Thick and thin blood films were prepared from capillary blood, stained with Giemsa and 100 oil immersion fields were examined. Parasite density was determined by counting parasites and 200 leucocytes, assuming each woman has 6,000 leucocytes/μl. All the slides were double-checked blindly.

The haemoglobin concentration was estimated by the haematic acid method [15] in the first two months and, subsequently, using Haemocure haemoglobinometer (HemCue AB, Angelhom, Sweden). Ferrous sulfate (200 mg/day) and folic acid tablets (0.25 mg/day) were supplied.

Ethical clearance

The study received ethical clearance from the Research Board of the Faculty of Medicine, University of Khartoum.

Statistical analysis

Data were entered in a computer using SPSS for windows. Comparisons between means and percentages were done by Students' t-test, ANOVA, X2 and Fisher's exact tests as appropriate. P < 0.05 was regarded as significant. Multivariate logistic regression was performed with malaria as the dependent variable, using age, parity and gestation as independent variables. These variables were categorized and used as follows: median age, ≤ 25 years versus >25 years); gravidae as primigravidae, secundigravidae, multigravidae (3–5)or grandmultigravidae >5; gestation as first (< 14 weeks), second (14–28 weeks) and third (> 28 weeks) trimester.

Results

Malaria and pregnancy

A total of 744 pregnant women attended the antenatal clinic of New Haifa Teaching Hospital during the study, 29.5% were primigravidae.

Table 1 summarizes patient characteristics for all sub-groups. 102 (13.7%) of women were infected with P. falciparum, 18(17.6%) of these were severe cases (jaundice and severe anaemia). Malaria prevalence and intensity (parasite count) were not significantly different amongst the different gravidity sub-groups (P > 0.05). The highest prevalence (18.3%) occurred in grandmultigravidae and the highest intensity (11,511 parasites/μl) was observed in primigravidae (Table 1).
Table 1

Characteristics of pregnant women in the study subjects *

Characteristics

Total

Primi-gravidae

Secundi-gravidae

Multi-gravidae

Grand-multigravidae

P Value

 

N (744)

N (220)

N (131)

N (322)

N (71)

 

Age (years)

26.6(9.9)

21.2(2.9)

25.7(2.3)

28.2(3.8)

34.9 (3.2)

< 0.001

Gestation (weeks)

27.7 (7.7)

27.3(8.09)

28.1(6.9)

27.6(7.6)

28.3(28.3)

0.18

Haemoglobin (g/dl)

10.5(1.4)

10.5(1.3)

10.3(1.6)

10.6(1.3)

10.3(1.2)

0.2

Malaria (total)

102(13.7)

32(14.5)

14(10.7)

43(13.4)

13(18.3)

0.4

Non severe

84(11.3)

28(12.7)

9(6.9)

34(10.6)

13 (18.3)

0.08

Severe

18(2.4)

4(1.8)

5(3.8)

9 (2.8)

0

0.3

Parasite count (parasites/μl)

6,586 (19,640.2)

11,511 (3,222)

6,817 (14,383)

3,504 (7,729)

4,497 (7,748)

0.4

*Data as mean (SD) or number (%) as appropriate

Mean (SD) age (26.2 ± 5.7 years versus 25.9 ± 5.3 years, P > 0.05) and parity (2.4 ± 2.4 versus 2.1 ± 2.1, P > 0.05) were not significantly different between infected and non-infected women. Two of 18 (11.1%), 29 of 290 (10%) and 71 of 436 (16.3%) women were infected in the first, second and third trimester respectively (P = 0.05).

Factors associated with malaria infection

Univariate and multivariate analysis indicated that, age and parity were not significantly associated with malaria infection. The third trimester was significantly associated with malaria infection (OR = 1.58, 95% CI = 1.02–2.4; P < 0.05)(Table 2).
Table 2

Risk factor analysis

 

Univariate

Multivariate

Variable

OR

95% CI

P

OR

95% CI

P

Age ≤ 25

1.03

0.68–1.5

0.40

0.90

0.52–1.6

0.74

Parity

      

Primigravidae

1.10

0.70–1.7

0.60

0.76

0.32–1.8

0.55

Secundigravidae

0.72

0.39–1.3

0.20

0.50

0.21–1.4

0.22

Multigravidae

0.96

0.62–1.4

0.80

0.74

0.37–1.4

0.41

Grandmultigravidae

1.40

0.77–2.7

0.20

3.20

0.27–46.2

0.30

Gestational age

      

First trimester

0.61

0.27–1.3

0.15

0.51

0.22–1.1

0.11

Second Trimester

0.71

0.45–1.3

0.09

0.67

0.41–1.08

0.10

Third trimester

1.50

1.02–2.4

0.02

1.58

1.02–2.4

0.03

OR: odds ratio

Malaria and haemoglobin

Mean haemoglobin was significantly lower in infected women (9.4 g/dl, 95% CI 9.1–9.7versus 10.7, CI 10.6–10.8, P < 0.05). A lower haemoglobin also occurred in women with severe malaria (9.4 g/dl, 95% CI 9.1–9.7versus 8.3, 95% CI 7.6–9.1 P < 0.05).

Discussion

This study investigated the morbidity pattern of P. falciparum malaria during pregnancy in an area of New Haifa, which is characterized by unstable transmission [13]. The malaria prevalence was 13.7% and 18 women (17.6%) were severe cases. With the exception of the neighbouring country Ethiopia [6], malaria prevalence was much lower than in other African countries characterized by intense malaria transmission [1012]. Several severe cases occured. In areas of unstable transmission, pregnant women are more susceptible to severe falciparum malaria than their non-pregnant peers [16] and different manifestations of severe falciparum malaria including cerebral malaria have been reported among pregnant women of central Sudan [17].

The study showed no significant association between malaria and parity, which is also reported from other areas and locations with intense malaria transmission [10, 12, 18]. In areas where transmission is high and the level of acquired pregnancy immunity against malaria is expected to be significant, primigravidae will be more affected [1, 2, 11].

In contrast to the previous observations [1012], age was not significantly associated with malaria in the present study. Lander et al have also reported no significant association between malaria infection and maternal age [18].

Women who attended the antenatal clinic in the third trimester had about a 1.5-fold higher risk of malaria parasitaemia. This is in line with some observations, although several studies report the second and early third trimesters as the time of peak prevalence [1, 3, 4, 1012]. Dicko et al reported the first trimester as the main risk period [19].

The mean haemoglobin was significantly lower in women with malaria infection and significantly lower in severe cases. Reduction of haemoglobin has been reported in areas of unstable transmission in Thailand and in Ethiopia, as well as in areas with stable transmission [3, 6]. Regardless of transmission level and pre-pregnancy level of malaria immunity, maternal anaemia remains the most frequent consequence of malaria during pregnancy [4].

Conclusion

The results suggest that prevalence of P. falciparum malaria is considerable in pregnant women in this part of Sudan and severe cases do occur. Preventive measures (chemoprophylaxis and insecticide-treated bednets) may be beneficial in this area for all women irrespective of their age or parity.

Declarations

Acknowledgements

We wish to thank all the patients for their excellent cooperation and we are very grateful to the local health authority in Kassala State and to the entire staff of New Haifa Teaching Hospital. Thanks are also extended to Mr. A. A. Hufazalla for his excellent technical assistance.

Authors’ Affiliations

(1)
New Haifa Teaching Hospital
(2)
Albayan College for Science, Sudan University for Science and Technology
(3)
Department of Biochemistry, Faculty of Medicine, University of Khartoum

References

  1. Brabin BJ: An analysis of malaria in pregnancy in Africa. Bull World Health Organ. 1983, 61: 1005-1016.PubMed CentralPubMedGoogle Scholar
  2. McGregor IA: Epidemiology, malaria and pregnancy. Am J Trop Med Hyg. 1984, 33: 517-525.PubMedGoogle Scholar
  3. Nosten F, Ter Kuile FO, Maelankirri L, Decludt B, White NJ: Malaria during pregnancy in an area of unstable endemicity. Trans R Soc Trop Med Hyg. 1991, 85: 424-429. 10.1016/0035-9203(91)90205-D.View ArticlePubMedGoogle Scholar
  4. Menendez C: Malaria during pregnancy: A priority area of malaria research and control. Parasitol Today. 1995, 11: 178-183. 10.1016/0169-4758(95)80151-0.View ArticlePubMedGoogle Scholar
  5. Dafallah SE, EL-Agib FH, Bushra GO: Maternal mortality in a teaching hospital in Sudan. Saudi Med J. 2003, 24: 369-373.PubMedGoogle Scholar
  6. Newman RD, Hailmariam A, Jimma D, Degefie A, Kebede D, Rietveld AC, Nahlen BL, Barnwell JW, Steketee RW, Parise ME: Burden of malaria during pregnancy in areas of stable and unstable transmission in Ethiopia during a nonepidemic year. J Infect Dis. 2003, 187: 1765-1772. 10.1086/374878.View ArticlePubMedGoogle Scholar
  7. Adam I, Elbashir MI: Maternal death due to servere pulmonary edema caused by falciparum malaria: case report. East Mediterr Health J. 2004,Google Scholar
  8. Okoko BJ, Enwere G, Ota MOC: The epidemiology and consequences of maternal malaria: a review of immunological basis. Acta Trop. 2003, 87: 193-205. 10.1016/S0001-706X(03)00097-4.View ArticlePubMedGoogle Scholar
  9. Shulman CE, Dorman EK: Importance and prevention for malaria in pregnancy. Trans R Soc Trop Med Hyg. 2003, 97: 30-35. 10.1016/S0035-9203(03)90012-5.View ArticlePubMedGoogle Scholar
  10. Rogerson SJ, Van den Broek NR, Chaluluka E, Qongwane C, Mhango CG, Molyneux ME: Malaria and anaemia in antenatal women in Blantyre, Malawi: a twelve- months survey. Am J Trop Med Hyg. 2000, 62: 335-340.PubMedGoogle Scholar
  11. Bouyou-Akotet MK, Ionete-Collard DE, Mabika-Manfoumbi M, Kendjo E, Matsiegui P-B, Mavoungou E, Kombila M: Prevalence of Plasmodium falciparum infection in pregnant women in Gabon. Malar J. 2003, 2: 18-10.1186/1475-2875-2-18.PubMed CentralView ArticlePubMedGoogle Scholar
  12. Dicko A, Mantel C, Aly Thera M, Doumbia S, Diallo M, Diakete M, Sagara I, Doumbo O: Risk factors for malaria infection and anemia for pregnantwomen in the Sahel area of Bandiagara, Mali. Acta Trop. 2003, 89: 17-23. 10.1016/j.actatropica.2003.07.001.View ArticlePubMedGoogle Scholar
  13. Al Gadal AA: Malaria in the Sudan. Proceedings of the Conference on Malaria in Africa. Edited by: Buck AA. 1986, Washington, DC: American Institute of Biological Sciences, 156-159.Google Scholar
  14. World Health Organization: Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000, 94 (suppl 1):
  15. Sahli H: Lehrbuch der Klinischen unter Suchungsmethoden. 1984, Leipzig: DeutickeGoogle Scholar
  16. Luxemburger C, Ricci F, Nosten F, Raimond D, Bathet S, White NJ: The epidemiology of severe malaria in an area of unstable and low transmission in Thailand. Trans R Soc Trop Med Hyg. 1997, 91: 256-262. 10.1016/S0035-9203(97)90066-3.View ArticlePubMedGoogle Scholar
  17. Adam I, Mirghani OM, Saed OK, Ahmed SM, Mohamadani AA, Ahmed HM, Mackenzie CD, Homeida MM, Elbashir MI: Quinine therapy in severe Plasmodium falciparum malaria during pregnancy in Sudan. East Mediterr Health J. 2004,Google Scholar
  18. Lander J, Leroy V, Simonon A, Karita E, Bogaerats J, Clercq AD, Van de Perre P, Dabis F: HIV infection, malaria, and pregnancy: a prospective cohort study in Kigali, Rwanda. Am J Trop Med Hyg. 2002, 66: 56-60.Google Scholar
  19. Adam I, Elbashir MI: Comments on the article: Risk factors for malaria infection and anemia for pregnant women in the Sahel area of Bandiagara, Mali. Acta Trop. 2005,Google Scholar

Copyright

© Adam et al; licensee BioMed Central Ltd. 2005

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.