The Open Public Health Journal




ISSN: 1874-9445 ― Volume 12, 2019
RESEARCH ARTICLE

Adherence to Intermittent Preventive Treatment of Malaria in Pregnancy with Sulfadoxine–Pyrimethamine and Associated Factors: A Cross-Sectional Survey in Benin’s Public Hospitals.



Aguemon Badirou1, Damien Barikissou Georgia1, *, Padonou Sètondji Géraud Roméo1, Kouwanou Modeste Luc1, Ouendo Edgard Marius2
1 Department of Public Health, Faculty of Health Sciences, University of Abomey-Calavi, Cotonou, Bénin
2 Regional Institute of Public Health (IRSP), University of Abomey-Calavi, Ouidah, Bénin

Abstract

Background:

Gestational malaria is a public health problem, thus responsible for morbidity and mortality risk to both the foetus and the mother. The intermittent preventive treatment with sulfadoxine-pyrimethamine during pregnancy (IPTp-SP) is one of the strategies recommended by the WHO to prevent this pathology and its consequences during pregnancy. In Benin, the adherence rate remains below the programmatic targets. This study aimed to identify the factors associated to the adherence to at least two IPTp-SP doses for postpartum women of the University Hospital HKM of Cotonou (CNHU-HKM) and the University Hospital for Mother and Child (CHU-MEL) of Cotonou.

Methods:

A cross-sectional hospital-based study was conducted over a 3-month-period, from July to September 2015 in the field of gynaecology and obstetrics departments of the two hospitals. All the mothers who had delivered and were still hospitalized at the time of the study were enrolled.

Results:

During their last pregnancy, 63.11% of women had taken at least two doses of IPTp-SP. Four determinants of adherence to the two IPTp-SP doses were associated to the adherence to two doses of IPTp-SP: i) adequate knowledge of the number of doses of SP to be taken during the pregnancy (p-value<0.0001), ii) participation in communication for social and behavioural change on IPTp-SP (p-value<0.0001), iii) adequate knowledge of the number of tablets per dose of SP (p-value=0.0100), and iv) comprehensive knowledge of malaria prevention measures during pregnancy (p-value=0.0200).

Conclusion:

Raising and improving women's knowledge on malaria are necessary to achieve ITPp-SP adherence. Particular emphasis should therefore be placed on communication for social and behavioural change for pregnant women, family decision-makers, community leaders and healthcare workers.

Keywords: Malaria, Intermittent preventive treatment, Pregnancy, Pregnancy, Social and behaviour change communication, IPTp-SP adherence, Postpartum women.


Article Information


Identifiers and Pagination:

Year: 2018
Volume: 11
First Page: 28
Last Page: 36
Publisher Id: TOPHJ-11-28
DOI: 10.2174/1874944501811010028

Article History:

Received Date: 29/12/2017
Revision Received Date: 18/01/2018
Acceptance Date: 18/01/2018
Electronic publication date: 31/01/2018
Collection year: 2018

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© 2018 Badirou et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Public Health, Faculty of Health Sciences, University of Abomey-Calavi, Cotonou, Bénin; Tel: 97483574; Fax: 21304096; E-mail: barikiss2000@yahoo.fr




1. INTRODUCTION

Malaria is a major public health problem with substantial risks for the mother, her fetus and the neonate, particularly in highly endemic countries in most of the sub-Saharan Africa. More than 90% of the total malaria deaths occur in this region [1World Health Organization (WHO). World Malaria Report 2014 2014. 142]. In Benin, malaria is the leading cause of care-seeking, hospitalization and death, with 40.6%, 29.2% and 26% of cases recorded [2Ministry of Health (MoH). Year book of health statistics 2013 Cotonou (BENIN) 2014. 243] in 2013, respectively. Pregnant women and infants are the most affected with higher mortality and morbidity. Malaria is the most frequent infection during pregnancy worldwide [3Carles G. State of play, progress and expectations in the treatment and prevention of malaria during pregnancy. Med Trop 2011; 71: 335-8.]. It remains one of the major causes of mother and infant health degradation in hyperendemic areas of Plasmodium falciparum transmission [4Hviid L. Le paludisme chez la femme enceinte. Med Trop 2006; 66: 130-2.].

Since 1990, preventing malaria during pregnancy has been based on the weekly administration of chloroquine prophylaxis in sub-Saharan Africa [5Steketee RW, Nahlen BL, Parise ME, Menéndez C. The burden of malaria in pregnancy in malaria-endemic areas.Am J Trop Med Hyg 2001; 64(1,2): 28-35.]. This strategy resulted in a limited efficiency due to limited adherence to treatment outside the medical community and the development of resistance to chloroquine in P. falciparum [6Steketee RW, Wirima JJ, Slutsker L, Heymann DL, Breman JG. The problem of malaria and malaria control in pregnancy in sub-Saharan Africa. Am J Trop Med Hyg 1996; 55(1): 2-7., 7Sirima SB, Sawadogo R, Moran AC, et al. Failure of a chloroquine chemoprophylaxis program to adequately prevent malaria during pregnancy in Koupéla District, Burkina Faso. Clin Infect Dis 2003; 36(11): 1374-82.]. The World Health Organization (WHO) has therefore, developed and recommended a new strategy: Intermittent Preventive Treatment (IPTp) of Sulfadoxine-Pyrimethamine (SP) during pregnancy (IPTp-SP) to daily or weekly replace chemoprophylaxis with chloroquine for some women in pregnancy antenatal care.

IPTp-SP is an integral part of the World Health Organization's (WHO) three-pronged approach to the prevention and treatment of malaria during pregnancy, which also includes the use of Insecticide-Treated Nets (ITNs), and a rapid and effective case management [8World Health Organization (WHO). Strategic framework for the prevention and control of malaria during pregnancy in the african region 2005., 9World Health Organization (WHO). WHO Policy Guidance Document: Intermittent preventive treatment for malaria during pregnancy with sulfadoxine-pyrimethamine -TPIp-SP 2014.]. Until 2012, IPTp-SP consisted of administering at least two doses of SP to pregnant women spaced in time by at least a month [8World Health Organization (WHO). Strategic framework for the prevention and control of malaria during pregnancy in the african region 2005.]. Updated in October 2012 by the WHO, the IPTp-SP is now recommended for all pregnant women at each Planned Prenatal Consultation (PPC) from the second trimester to the delivery period, if doses are administered at least a month apart [9World Health Organization (WHO). WHO Policy Guidance Document: Intermittent preventive treatment for malaria during pregnancy with sulfadoxine-pyrimethamine -TPIp-SP 2014.-11World Health Organization (WHO). Updated WHO policy recommendation: Intermittent preventive treatment of malaria in pregnancy using sulfadoxine-pyrimethamine (IPTp-SP) 2012.]. Through the National Malaria Control Program (NMCP), Benin has adopted this intervention since 2004 and the implementation has been effective since 2006 [12d’Almeida TC, Agboton-Zoumenou MA, Garcia A, et al. Field evaluation of the intermittent preventive treatment of malaria during pregnancy (IPTp) in Benin: Evolution of the coverage rate since its implementation. Parasit Vectors 2011; 4: 108.].

In countries where the IPT-SP has been implemented for several years, studies show that the rate of the second-dose intake was remarkably lower [8World Health Organization (WHO). Strategic framework for the prevention and control of malaria during pregnancy in the african region 2005., 13van Eijk AM, Hill J, Larsen DA, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: A synthesis and meta-analysis of national survey data, 2009-11. Lancet Infect Dis 2013; 13(12): 1029-42.-15Rogerson SJ, Chaluluka E, Kanjala M, Mkundika P, Mhango C, Molyneux ME. Intermittent sulfadoxine-pyrimethamine in pregnancy: Effectiveness against malaria morbidity in Blantyre, Malawi, in 1997-99. Trans R Soc Trop Med Hyg 2000; 94(5): 549-53.]. In Benin, recent studies reported an improvement in the coverage of IPTp-SP since its adoption, ranging from 3% in 2006 [16National Institute of Statistics and Economic Analysis (INSAE). Demographic and health survey (EDSB III) Benin 2007. 71] to 35% in 2008 [17National Malaria Control Program (NMCP). Mid-term review of the project to support malaria control Cotonou 2009.] and to 46% in 2010 [18National Malaria Control Program (NMCP). MIS evaluation report of malaria control activities in Benin Cotonou (BENIN) 2010. 117]. Nevertheless, the coverage of the IPT-SP is far from satisfactory, as it is still below the NMCP target of 100% of pregnant women receiving full IPTp-SP in 2015 [19National Malaria Control Program (NMCP). Malaria Control Strategic Plan 2011-2015 Cotonou (BENIN) 2010. 102]. Furthermore, Benin performance is far from the new recommendation of WHO which requests five IPT-SP doses during pregnancy. This study aimed to measure the adherence rate to IPTp-SP for mothers and identify its determinants for decision-making.

2. METHODS

2.1. Study Area

The study was conducted in two gynaecological and obstetric departments in Cotonou: the University Clinic of Gynaecology and Obstetrics (CUGO) of the National University Hospital of Cotonou (CNHU-HKM) and the Gynaecology and Obstetrics Department of the Mother and Child Lagoon Hospital (CHU-MEL). The CNHU-HKM and the CHU-MEL are the two referral centres for Gynaecology and Obstetrics in Benin.

Services offered in the facility include family planning, antenatal care, delivery, postnatal care, child welfare clinic, laboratory and pharmacy services.

2.2. Study Design

A cross-sectional hospital-survey was carried out over a period of three months from July to September 2015.

2.3. Sample Size Estimation

The sample size for the study was calculated using Schwartz’s formula: n = Z2pq/i2. Where, Z = 1.96 at 95% confidence interval, p = 60% (IPT2 coverage in Benin in 2014) [20National Institute of Statistics and Economic Analysis (INSAE). Multiple Indicator Cluster Survey 2014. 22], i = precision level of 0.05 and q = 1 − p. The required sample size estimated was 368.

2.4. Inclusion/exclusion criteria

All the women with the following characteristics were eligible for participation: (i) had delivered in one of the two hospitals during the study, (ii) was still hospitalized at the time of the study, (iii) have had at least one prenatal consultation conducted by a health worker at any health facility in Benin and (iv) have given free and written consent to take part in the study. Those who had a postpartum pathology and / or complications were not included.

The dependent variable was defined as a person who took at least two doses of SP during the last pregnancy. We adopted this definition because the last WHO recommendation, requiring a dose of IPTp-SP in all consultation from the second trimester of pregnancy (a total of five doses), was not yet appropriately distributed in Benin. The independent variables were related to sociocultural and socio-demographic factors of the respondents, their obstetric history, their knowledge on malaria and IPTp-SP, the perception of the conduct of NPCs by the respondents and the awareness of the IPTp-SP and health care supply.

2.5. Data Analysis

Data were analysed using EPI INFO 7.0 version. The mean, median and standard deviation were determined for the quantitative variables. The proportions were calculated for qualitative variables. We used the Chi-square test to compare two proportions when the theoretical numbers were at least 5 and the fisher test when theoretical numbers were more than 5. To identify the factors associated to the adherence to at least two doses of SP during the last pregnancy, univariate and multivariate logistic regression analyses were performed. At the end of the bivariate analysis, the independent variables associated with the observance of IPTp-SP with a p-value less or equal to 0.20 were introduced in the logistic regression model. The Odd Ratio (OR) was used to estimate the association between the dependent variable and the independent variables. A significant threshold of 5% was considered.

3. RESULTS

3.1. Sample Description

A total of 366 women who gave birth were involved in the survey, including 48.63% at CUGO (at the CNHU-HKM) and 51.37% at CHU-MEL. The mean age of women was 28.12 ± 5.52 years. The age group 25-34 was the majority (60.93%). In terms of marital status, women in common-law unions were in the majority, accounting for 65.30% of the sample. Most of the women surveyed lived in urban areas, with 47.27% in Cotonou and 34.15% in other cities. Women in trade and craft sectors accounted for 27.05% and 24.32% of the sample, respectively. Regarding the distance between their homes and the health facilities, 54.92% of the women travelled more than 5 km. Women with no formal education on one hand and those with primary education on the other hand, each accounted for 24.59%. The ethnic groups, most represented among the women in the sample were the Fon and relatives with 38.8% and Adja and relatives with 26.23%. Concerning the religion of women, Catholics come first with 46.72% followed by Evangelicals with 29.51%, and Muslims with 11.48% of the total.

For gynaecological history, 36.07% of women were primiparous and 27.87% of the primigravida (Table 1).

Table 1
Distribution of women with infants according to their obstetric history in CNHU-HKM and CHU-MEL, 2015.


3.2. Adherence Rate IPTp-SP

The proportion of women taking at least two doses of SP during pregnancy was 63.11%. This rate was 62.92% and 63.30% at the CNHU-HKM and the CHU-MEL, respectively.

3.3. Determinants of Adherence to IPTp-SP

In univariate analysis, age, marital status, religion, place of residence, distance from home and health facility, level of education and customary prohibitions of medication use during pregnancy are not significantly associated with adherence to IPTp-SP. Only the need for a third-party authorization to monitor pregnancy showed a significant association with adherence to IPTp-SP, p-value = 0.0030 (Table 2). No factors related to the obstetric history of the respondents were significantly associated with adherence to IPTp-SP in this study (Table 3). Women's adequate knowledge of malaria prevention measures during pregnancy (p-value <0.0001), the number of tablets per dose of IPTp-SP (p-value <0.0001), and the number of doses of IPTp-SP to be taken during pregnancy (p-value <0.0001) were significantly associated with adherence to IPTp-SP (Table 4). Among the health-related factors, only participation in a IPTp-SP information session was significantly associated with adherence to TPIp-SP, p-value <0.0001, (Table 5).

Table 2
Association between the adherence to IPTp-SP and socio-demographic, univariate analysis in CNHU-HKM and CHU-MEL, 2015.


Table 3
Association between obstetrical history and adherence to ITPIp-SP, univariate analysis, in CNHU-HKM and CHU-MEL, 2015.


Table 4
Association between adherence to IPTp-SP and factors related to women’s knowledge of malaria and IPT-SP, univariate analysis in CNHU-HKM and CHU-MEL, 2015.


Table 5
Association between adherence of IPTp-SP and factors related to health care, univariate analysis in CNHU-HKM and CHU-MEL, 2015.


In multivariate analysis, four variables were selected in the final model. These four variables remained associated with adherence to the IPTp-SP adjusted to each other. The women who had adequate knowledge of the doses of IPTp-SP to be taken during pregnancy were 4.70 times more likely to respect the adherence to IPTp-Sp compared to the women who did not have adequate knowledge. The variable “participation of women in an information session on the IPTp-SP during pregnancy” was 4.61 times more likely to adhere to the IPTp-SP compared to women who did not participate to an information session. Similarly, the comprehensive knowledge of the number of tablets per dose of IPTp-SP multiplies the chance of adherence by 3.32. Finally, women who had adequate knowledge of malaria prevention measures during pregnancy were 2.56 times more likely to adhere to ITPp-SP than those who did not have comprehensive knowledge (Table 6).

Table 6
Determinants of adherence to IPTp-SP in multivariate analysis in CNHU-HKM and CHU-MEL, 2015.


4. DISCUSSION

We obtained almost the same defiance IPTp-SP rates at the University Hospital-HKM of Cotonou and the University Hospital “Mother and Child Lagoon” (CHU-MEL) with 62.92% and 63.30%, respectively. This similarity is justified by the fact that these two places are the referral in Benin and receive women with almost the same profile. The overall adherence rate was 63.11% for the entire sample. This rate, although rather good, is far from satisfactory, as it is still far from the objective of the National Malaria Control Program (NMCP) in Benin, which is to reach a 100% coverage for the second dose of the IPTp-SP in 2015 [19National Malaria Control Program (NMCP). Malaria Control Strategic Plan 2011-2015 Cotonou (BENIN) 2010. 102].

The adherence rate to IPTp-SP was higher than those reported by the 2011-2012 Demographic Health Survey (DHS) in Benin [19National Malaria Control Program (NMCP). Malaria Control Strategic Plan 2011-2015 Cotonou (BENIN) 2010. 102] and by the WHO in 2014, based on data from 2013 [1World Health Organization (WHO). World Malaria Report 2014 2014. 142]. The DHS 2011-2012 reported a rate of only 23% taking at least two doses of SP during pregnancy. As for the World Malaria Report published by the WHO in 2014, it reported an overall rate of 43% worldwide. This reflects an evolution of efforts to improve adherence to IPTp-SP in Benin. A lower rate of 52.5% was observed in the health zone of Pobè/Adja-Ouèrè/Kétou [21Tiendrebéogo J, Drabo MK, Saizonou J, et al. Factors associated with the low coverage of Intermittent Preventive Treatment for pregnant women in the Benin health zone of Pobè-Adja-Ouèrè-Kétou. Sante Publique 2015; 27(1): 99-106.] in 2012. Earlier in 2009 [12d’Almeida TC, Agboton-Zoumenou MA, Garcia A, et al. Field evaluation of the intermittent preventive treatment of malaria during pregnancy (IPTp) in Benin: Evolution of the coverage rate since its implementation. Parasit Vectors 2011; 4: 108.], in a study carried out in eight maternities in Benin, the adherence to IPTp-SP that was almost similar to that of the present study (68.43%) was noted. Globally, it seemed that the adherence to IPTp-SP has increased in the health centre survey in Benin.

In a survey conducted in Tanzania in 2012 [22Exavery A, Mbaruku G, Mbuyita S, Makemba A, Kinyonge IP, Kweka H. Factors affecting uptake of optimal doses of sulphadoxine-pyrimethamine for intermittent preventive treatment of malaria in pregnancy in six districts of Tanzania. Malar J 2014; 13: 22.], the adherence rate of IPT-SP was estimated at 28.5%. In Malawi [23Mwandama D, Gutman J, Wolkon A, et al. The use of intermittent preventive treatment in pregnancy and insecticide-treated bed nets for malaria prevention by women of child-bearing age in eight districts in Malawi. Malar J 2015; 14: 316.], however, a higher adherence rate of 72% was observed in 2009. Furthermore, in this study, only 18.03% of respondents took a minimum of three doses of IPT-SP during pregnancy. This rate is comparable to the World Malaria Report published by the WHO in 2014, which was 17%. Since it has been recommended to take a monthly consultation as from the 3rd month of pregnancy, five doses of IPTp-SP should be given to pregnant women according to the WHO recommendation. Then, Benin NMCP recommendation for IPTp-SP on pregnant women moved from two doses to tree doses since 2016. This new recommendation is not yet evaluated; however, efforts should be undertaken by the NMCP to disseminate this recommendation for better adherence.

Regarding the determinants of IPTp-SP adherence, three of the identified determinants were related to the knowledge on malaria prevention, and more specifically on IPTp-SP. This finding is in accordance with those of other authors [23Mwandama D, Gutman J, Wolkon A, et al. The use of intermittent preventive treatment in pregnancy and insecticide-treated bed nets for malaria prevention by women of child-bearing age in eight districts in Malawi. Malar J 2015; 14: 316.-25Odongo CO, Bisaso RK, Byamugisha J, Obua C. Intermittent use of sulphadoxine-pyrimethamine for malaria prevention: A cross-sectional study of knowledge and practices among Ugandan women attending an urban antenatal clinic. Malar J 2014; 13: 399.] who have shown a poor knowledge of women on IPTp-SP, particularly the number of tablets per dose. In addition, they identified other factors such as low antenatal coverage and prenatal consultations in the private sector. Thus, according to one of these studies, good knowledge on the use of SP during pregnancy was significantly predictive of good adherence to IPTp-SP [25Odongo CO, Bisaso RK, Byamugisha J, Obua C. Intermittent use of sulphadoxine-pyrimethamine for malaria prevention: A cross-sectional study of knowledge and practices among Ugandan women attending an urban antenatal clinic. Malar J 2014; 13: 399.]. In 2010, in Nigeria, another study showed that women’s comprehensive knowledge of malaria including its prevention during pregnancy through the use of IPTp-SP was associated with good adherence to IPTp-SP [25Odongo CO, Bisaso RK, Byamugisha J, Obua C. Intermittent use of sulphadoxine-pyrimethamine for malaria prevention: A cross-sectional study of knowledge and practices among Ugandan women attending an urban antenatal clinic. Malar J 2014; 13: 399.]. All this confirms that adequate knowledge on IPTp-SP by pregnant women could improve their adherence. A better communication strategy for Behaviour and Social Change needs to be implemented in order to improve women's knowledge on IPTp-SP.

The participation of women in communication sessions on IPTp-SP has also been shown in our study to be a determining factor in adherence to IPTp-SP in our study population. In 2012, in Tanzania, an almost similar result was observed [22Exavery A, Mbaruku G, Mbuyita S, Makemba A, Kinyonge IP, Kweka H. Factors affecting uptake of optimal doses of sulphadoxine-pyrimethamine for intermittent preventive treatment of malaria in pregnancy in six districts of Tanzania. Malar J 2014; 13: 22.]. Indeed, the fact that informing women about the dangers of malaria during pregnancy was the main determinant of adherence to the IPTp-SP. The communication sessions, individual or collective, can improve women’s knowledge on the IPTp-SP and therefore, promote better adherence to this strategy. The lack of communication to social and behaviour change may be related to a low quality of prenatal care services, as these services are responsible to inform the pregnant woman about the IPTp-SP, and its use during pregnancy. However, more than 90% (331 of 366) of the pregnant women surveyed were followed by qualified health workers (doctor or midwife). Prenatal care providers should be more aware of the health services they addressed to women, and more specifically concerning the IPTp-SP recommendations. Mass and health facility communication for social and behaviour change are mainly concerned. The health system must develop, and ensure their implementation.

Previous studies have identified other factors associated with adherence or non-adherence to IPTp-SP. This is evidenced by the WHO 2014 World Malaria Report [1World Health Organization (WHO). World Malaria Report 2014 2014. 142], which found that poverty was the main determinant of non-adherence to IPTp-SP. Age below 20 years, lack of formal education, rural life and parity superior to one were also identified as negative influences on IPTp-SP adherence. On the other hand, a study carried out in Nigeria in 2010 showed that the primiparae adhered better to the IPTp-SP compared to the secondipares and the multipares [14Nduka FO, Nwosu E, Oguariri RM. Evaluation of the effectiveness and compliance of intermittent preventive treatment (IPT) in the control of malaria in pregnant women in south eastern Nigeria. Ann Trop Med Parasitol 2011; 105(8): 599-605.]. In Uganda between 2008 and 2009, a cross-sectional study on 500 women who were pregnant the previous year revealed that women were more likely to observe IPTp-SP if administered during the prenatal consultation [26Sangaré LR, Stergachis A, Brentlinger PE, et al. Determinants of use of intermittent preventive treatment of malaria in pregnancy: Jinja, Uganda. PLoS One 2010; 5(11): e15066.].

CONCLUSION

The study found that raising and improving women's knowledge on malaria are necessary to achieve ITPp-SP adherence. Particular emphasis should therefore be placed on communication for social and behavioural change on pregnant women, family decision-makers, community leaders and health workers.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study was conducted in two gynaecological and obstetric departments in Cotonou: the University Clinic of Gynaecology and Obstetrics (CUGO) of the National University Hospital of Cotonou (CNHU-HKM) and the Gynaecology and Obstetrics Department of the Mother and Child Lagoon Hospital (CHU-MEL). The CNHU-HKM and the CHU-MEL are the two referral centres for Gynaecology and Obstetrics in Benin.

HUMAN AND ANIMAL RIGHTS

All human research procedures followed were in accordance with the ethical standards of the committee responsible for human experimentation (institutional and national), and with the Helsinki Declaration of 1975, as revised in 2008.

CONSENT FOR PUBLICATION

All the women have given free and written consent to take part in the study.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGMENTS

Declared none.

REFERENCES

[1] World Health Organization (WHO). World Malaria Report 2014 2014. 142
[2] Ministry of Health (MoH). Year book of health statistics 2013 Cotonou (BENIN) 2014. 243
[3] Carles G. State of play, progress and expectations in the treatment and prevention of malaria during pregnancy. Med Trop 2011; 71: 335-8.
[4] Hviid L. Le paludisme chez la femme enceinte. Med Trop 2006; 66: 130-2.
[5] Steketee RW, Nahlen BL, Parise ME, Menéndez C. The burden of malaria in pregnancy in malaria-endemic areas.Am J Trop Med Hyg 2001; 64(1,2): 28-35.
[6] Steketee RW, Wirima JJ, Slutsker L, Heymann DL, Breman JG. The problem of malaria and malaria control in pregnancy in sub-Saharan Africa. Am J Trop Med Hyg 1996; 55(1): 2-7.
[7] Sirima SB, Sawadogo R, Moran AC, et al. Failure of a chloroquine chemoprophylaxis program to adequately prevent malaria during pregnancy in Koupéla District, Burkina Faso. Clin Infect Dis 2003; 36(11): 1374-82.
[8] World Health Organization (WHO). Strategic framework for the prevention and control of malaria during pregnancy in the african region 2005.
[9] World Health Organization (WHO). WHO Policy Guidance Document: Intermittent preventive treatment for malaria during pregnancy with sulfadoxine-pyrimethamine -TPIp-SP 2014.
[10] World Health Organization (WHO). Guidelines for the Treatment of Malaria 3rd ed. 3rd ed.2015.
[11] World Health Organization (WHO). Updated WHO policy recommendation: Intermittent preventive treatment of malaria in pregnancy using sulfadoxine-pyrimethamine (IPTp-SP) 2012.
[12] d’Almeida TC, Agboton-Zoumenou MA, Garcia A, et al. Field evaluation of the intermittent preventive treatment of malaria during pregnancy (IPTp) in Benin: Evolution of the coverage rate since its implementation. Parasit Vectors 2011; 4: 108.
[13] van Eijk AM, Hill J, Larsen DA, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: A synthesis and meta-analysis of national survey data, 2009-11. Lancet Infect Dis 2013; 13(12): 1029-42.
[14] Nduka FO, Nwosu E, Oguariri RM. Evaluation of the effectiveness and compliance of intermittent preventive treatment (IPT) in the control of malaria in pregnant women in south eastern Nigeria. Ann Trop Med Parasitol 2011; 105(8): 599-605.
[15] Rogerson SJ, Chaluluka E, Kanjala M, Mkundika P, Mhango C, Molyneux ME. Intermittent sulfadoxine-pyrimethamine in pregnancy: Effectiveness against malaria morbidity in Blantyre, Malawi, in 1997-99. Trans R Soc Trop Med Hyg 2000; 94(5): 549-53.
[16] National Institute of Statistics and Economic Analysis (INSAE). Demographic and health survey (EDSB III) Benin 2007. 71
[17] National Malaria Control Program (NMCP). Mid-term review of the project to support malaria control Cotonou 2009.
[18] National Malaria Control Program (NMCP). MIS evaluation report of malaria control activities in Benin Cotonou (BENIN) 2010. 117
[19] National Malaria Control Program (NMCP). Malaria Control Strategic Plan 2011-2015 Cotonou (BENIN) 2010. 102
[20] National Institute of Statistics and Economic Analysis (INSAE). Multiple Indicator Cluster Survey 2014. 22
[21] Tiendrebéogo J, Drabo MK, Saizonou J, et al. Factors associated with the low coverage of Intermittent Preventive Treatment for pregnant women in the Benin health zone of Pobè-Adja-Ouèrè-Kétou. Sante Publique 2015; 27(1): 99-106.
[22] Exavery A, Mbaruku G, Mbuyita S, Makemba A, Kinyonge IP, Kweka H. Factors affecting uptake of optimal doses of sulphadoxine-pyrimethamine for intermittent preventive treatment of malaria in pregnancy in six districts of Tanzania. Malar J 2014; 13: 22.
[23] Mwandama D, Gutman J, Wolkon A, et al. The use of intermittent preventive treatment in pregnancy and insecticide-treated bed nets for malaria prevention by women of child-bearing age in eight districts in Malawi. Malar J 2015; 14: 316.
[24] Onyeneho NG, Orji BC, Okeibunor JC, Brieger WR. Characteristics of Nigerian women taking sulfadoxine/pyrimethamine twice during pregnancy for the prevention of malaria. Int J Gynaecol Obstet 2013; 123(2): 101-4.
[25] Odongo CO, Bisaso RK, Byamugisha J, Obua C. Intermittent use of sulphadoxine-pyrimethamine for malaria prevention: A cross-sectional study of knowledge and practices among Ugandan women attending an urban antenatal clinic. Malar J 2014; 13: 399.
[26] Sangaré LR, Stergachis A, Brentlinger PE, et al. Determinants of use of intermittent preventive treatment of malaria in pregnancy: Jinja, Uganda. PLoS One 2010; 5(11): e15066.

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Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


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