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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Birth prevalence of neural tube defects and associated risk factors in Africa: a systematic review and meta-analysis</title><author><name sortKey="Oumer, Mohammed" sort="Oumer, Mohammed" uniqKey="Oumer M" first="Mohammed" last="Oumer">Mohammed Oumer</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Human Anatomy, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Epidemiology, College of Medicine and Health Sciences,</institution><institution>Institute of Public Health, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation></author><author><name sortKey="Tazebew, Ashenafi" sort="Tazebew, Ashenafi" uniqKey="Tazebew A" first="Ashenafi" last="Tazebew">Ashenafi Tazebew</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Departments of Pediatrics and Child Health, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation></author><author><name sortKey="Silamsaw, Mezgebu" sort="Silamsaw, Mezgebu" uniqKey="Silamsaw M" first="Mezgebu" last="Silamsaw">Mezgebu Silamsaw</name><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Internal Medicine, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">33882899</idno><idno type="pmc">8058994</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8058994</idno><idno type="RBID">PMC:8058994</idno><idno type="doi">10.1186/s12887-021-02653-9</idno><date when="2021">2021</date><idno type="wicri:Area/Pmc/Corpus">000091</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000091</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Birth prevalence of neural tube defects and associated risk factors in Africa: a systematic review and meta-analysis</title><author><name sortKey="Oumer, Mohammed" sort="Oumer, Mohammed" uniqKey="Oumer M" first="Mohammed" last="Oumer">Mohammed Oumer</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Human Anatomy, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Epidemiology, College of Medicine and Health Sciences,</institution><institution>Institute of Public Health, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation></author><author><name sortKey="Tazebew, Ashenafi" sort="Tazebew, Ashenafi" uniqKey="Tazebew A" first="Ashenafi" last="Tazebew">Ashenafi Tazebew</name><affiliation><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Departments of Pediatrics and Child Health, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation></author><author><name sortKey="Silamsaw, Mezgebu" sort="Silamsaw, Mezgebu" uniqKey="Silamsaw M" first="Mezgebu" last="Silamsaw">Mezgebu Silamsaw</name><affiliation><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Internal Medicine, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</nlm:aff></affiliation></author></analytic><series><title level="j">BMC Pediatrics</title><idno type="eISSN">1471-2431</idno><imprint><date when="2021">2021</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p id="Par1">Neural tube defects are common congenital anomalies that result from early malformation in the development of the spinal cord and brain. It is related to substantial mortality, morbidity, disability, and psychological and economic costs. The aim of this review is to determine the pooled birth prevalence of neural tube defects and associated risk factors in Africa.</p></sec><sec><title>Methods</title><p id="Par2">The first outcome of this review was the pooled birth prevalence of the neural tube defects and the second outcome was the pooled measure of association between neural tube defects and associated risk factors in Africa. We systematically searched PubMed, PubMed Central, Joanna Briggs Institute, Google Scopus, Cochrane Library, African Journals Online, Web of Science, Science Direct, Google Scholar, and Medline databases. The heterogeneity of studies was assessed using the Cochrane Q test statistic, I<sup>2</sup> test statistic, and, visually, using Forest and Galbraith’s plots. A random-effect model was applied to get the pooled birth prevalence of neural tube defects. Subgroup, sensitivity, meta-regression, time-trend, and meta-cumulative analyses were undertaken. The fixed-effect model was used to analyze the association between neural tube defects and associated risk factors.</p></sec><sec><title>Results</title><p id="Par3">Forty-three studies with a total of 6086,384 participants were included in this systematic review and meta-analysis. The pooled birth prevalence of the neural tube defects was 21.42 (95% CI (Confidence Interval): 19.29, 23.56) per 10,000 births. A high pooled birth prevalence of neural tube defects was detected in Algeria 75 (95% CI: 64.98, 85.02), Ethiopia 61.43 (95% CI: 46.70, 76.16), Eritrea 39 (95% CI: 32.88, 45.12), and Nigeria 32.77 (95% CI: 21.94, 43.59) per 10,000 births. The prevalence of neural tube defects has increased over time. Taking folic acid during early pregnancy, consanguineous marriage, male sex, and substance abuse during pregnancy were assessed and none of them was significant.</p></sec><sec><title>Conclusions</title><p id="Par4">The pooled birth prevalence of neural tube defects in Africa was found to be high. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">BMC Pediatr</journal-id><journal-id journal-id-type="iso-abbrev">BMC Pediatr</journal-id><journal-title-group><journal-title>BMC Pediatrics</journal-title></journal-title-group><issn pub-type="epub">1471-2431</issn><publisher><publisher-name>BioMed Central</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">33882899</article-id><article-id pub-id-type="pmc">8058994</article-id><article-id pub-id-type="publisher-id">2653</article-id><article-id pub-id-type="doi">10.1186/s12887-021-02653-9</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Birth prevalence of neural tube defects and associated risk factors in Africa: a systematic review and meta-analysis</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0003-4289-8712</contrib-id><name><surname>Oumer</surname><given-names>Mohammed</given-names></name><address><email>Mohammed.Oumer@uog.edu.et</email><email>mohammedoumer58@gmail.com</email></address><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Tazebew</surname><given-names>Ashenafi</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Silamsaw</surname><given-names>Mezgebu</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Human Anatomy, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Epidemiology, College of Medicine and Health Sciences,</institution><institution>Institute of Public Health, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Departments of Pediatrics and Child Health, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</aff><aff id="Aff4"><label>4</label><institution-wrap><institution-id institution-id-type="GRID">grid.59547.3a</institution-id><institution-id institution-id-type="ISNI">0000 0000 8539 4635</institution-id><institution>Department of Internal Medicine, College of Medicine and Health Sciences,</institution><institution>School of Medicine, University of Gondar,</institution></institution-wrap>Gondar, Amhara Ethiopia</aff></contrib-group><pub-date pub-type="epub"><day>21</day><month>4</month><year>2021</year></pub-date><pub-date pub-type="pmc-release"><day>21</day><month>4</month><year>2021</year></pub-date><pub-date pub-type="collection"><year>2021</year></pub-date><volume>21</volume><elocation-id>190</elocation-id><history><date date-type="received"><day>19</day><month>10</month><year>2020</year></date><date date-type="accepted"><day>8</day><month>4</month><year>2021</year></date></history><permissions><copyright-statement>© The Author(s) 2021</copyright-statement><license><ali:license_ref specific-use="textmining" content-type="ccbylicense">https://creativecommons.org/licenses/by/4.0/</ali:license_ref><license-p><bold>Open Access</bold>This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated in a credit line to the data.</license-p></license></permissions><abstract id="Abs1"><sec><title>Background</title><p id="Par1">Neural tube defects are common congenital anomalies that result from early malformation in the development of the spinal cord and brain. It is related to substantial mortality, morbidity, disability, and psychological and economic costs. The aim of this review is to determine the pooled birth prevalence of neural tube defects and associated risk factors in Africa.</p></sec><sec><title>Methods</title><p id="Par2">The first outcome of this review was the pooled birth prevalence of the neural tube defects and the second outcome was the pooled measure of association between neural tube defects and associated risk factors in Africa. We systematically searched PubMed, PubMed Central, Joanna Briggs Institute, Google Scopus, Cochrane Library, African Journals Online, Web of Science, Science Direct, Google Scholar, and Medline databases. The heterogeneity of studies was assessed using the Cochrane Q test statistic, I<sup>2</sup> test statistic, and, visually, using Forest and Galbraith’s plots. A random-effect model was applied to get the pooled birth prevalence of neural tube defects. Subgroup, sensitivity, meta-regression, time-trend, and meta-cumulative analyses were undertaken. The fixed-effect model was used to analyze the association between neural tube defects and associated risk factors.</p></sec><sec><title>Results</title><p id="Par3">Forty-three studies with a total of 6086,384 participants were included in this systematic review and meta-analysis. The pooled birth prevalence of the neural tube defects was 21.42 (95% CI (Confidence Interval): 19.29, 23.56) per 10,000 births. A high pooled birth prevalence of neural tube defects was detected in Algeria 75 (95% CI: 64.98, 85.02), Ethiopia 61.43 (95% CI: 46.70, 76.16), Eritrea 39 (95% CI: 32.88, 45.12), and Nigeria 32.77 (95% CI: 21.94, 43.59) per 10,000 births. The prevalence of neural tube defects has increased over time. Taking folic acid during early pregnancy, consanguineous marriage, male sex, and substance abuse during pregnancy were assessed and none of them was significant.</p></sec><sec><title>Conclusions</title><p id="Par4">The pooled birth prevalence of neural tube defects in Africa was found to be high. The risk factors evaluated were not found significant.</p></sec><sec><title>Supplementary Information</title><p>The online version contains supplementary material available at 10.1186/s12887-021-02653-9.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Africa</kwd><kwd>Neural tube defects</kwd><kwd>Systematic review and meta-analysis</kwd></kwd-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2021</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Background</title><p id="Par13">Neural tube defects are common congenital anomalies that result from early malformation in the development of the brain and spinal cord [<xref ref-type="bibr" rid="CR1">1</xref>–<xref ref-type="bibr" rid="CR8">8</xref>]. It is the main cause of fetal loss and disabilities in neonates and it is considered a significant public health problem [<xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR9">9</xref>–<xref ref-type="bibr" rid="CR17">17</xref>]. The defects occur around 28th day after conception due to the failure of neurulation or alterations in the morphogenesis or histogenesis of the nervous tissue [<xref ref-type="bibr" rid="CR1">1</xref>–<xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR8">8</xref>].</p><p id="Par14">Because of its complicated embryologic history, abnormal development of the spinal cord and brain is common [<xref ref-type="bibr" rid="CR1">1</xref>]. Anencephaly, encephalocele, and spina bifida are the main types of neural tube defects [<xref ref-type="bibr" rid="CR18">18</xref>–<xref ref-type="bibr" rid="CR23">23</xref>]. The defects are correlated with substantial mortality, morbidity, disability, and psychological and economic costs [<xref ref-type="bibr" rid="CR24">24</xref>]. Patients with these defects mostly have problems related to neurogenic bladder, orthopedic complications, kidney involvement, and hydrocephalus [<xref ref-type="bibr" rid="CR25">25</xref>]. Patients with neural tube defects face lifelong physical problems that need lifetime medical care that add a significant burden to the affected patients and their families [<xref ref-type="bibr" rid="CR25">25</xref>–<xref ref-type="bibr" rid="CR27">27</xref>]. The challenges of parents begin with high distress at the time of diagnosis with defects during pregnancy and face either the grief of a termination/stillbirth or financial and emotional challenges of caring for a child with defects [<xref ref-type="bibr" rid="CR25">25</xref>]. The lifetime direct medical costs and indirect costs for affected patients, parents, families, and at the national level are found very significant [<xref ref-type="bibr" rid="CR25">25</xref>]. Prevention ensures that this multi-factorial burden does not have to happen at all [<xref ref-type="bibr" rid="CR25">25</xref>, <xref ref-type="bibr" rid="CR28">28</xref>], and more literature is needed to fill the gaps. Worldwide, neural tube defects are among the top five most serious birth defects [<xref ref-type="bibr" rid="CR13">13</xref>]. There are more than 400,000 births born affected by neural tube defects each year, causing around 88,000 deaths [<xref ref-type="bibr" rid="CR9">9</xref>, <xref ref-type="bibr" rid="CR13">13</xref>, <xref ref-type="bibr" rid="CR29">29</xref>]. More than 10 % of newborns’ mortality happened due to the malformation of the spinal cord and brain [<xref ref-type="bibr" rid="CR9">9</xref>]. In Africa, the most common birth defects are neural tube defects. It affects approximately 1–3/1000 births annually [<xref ref-type="bibr" rid="CR18">18</xref>, <xref ref-type="bibr" rid="CR30">30</xref>–<xref ref-type="bibr" rid="CR32">32</xref>]. In addition to its burden, stigmatization towards neural tube defects by the community has been documented elsewhere in Africa [<xref ref-type="bibr" rid="CR13">13</xref>, <xref ref-type="bibr" rid="CR33">33</xref>, <xref ref-type="bibr" rid="CR34">34</xref>], affecting the quality of life of caring families with social, economic, and emotional distress.</p><p id="Par15">The factors causing neural tube defects are genetic, nutritional, environmental, or a combination of these [<xref ref-type="bibr" rid="CR1">1</xref>, <xref ref-type="bibr" rid="CR12">12</xref>, <xref ref-type="bibr" rid="CR13">13</xref>, <xref ref-type="bibr" rid="CR18">18</xref>, <xref ref-type="bibr" rid="CR35">35</xref>]. Epidemiologic studies have revealed that folic acid supplements and/or a vitamin-B taken before conception and continued for at least 3 months during pregnancy reduce the occurrence of neural tube defects [<xref ref-type="bibr" rid="CR1">1</xref>, <xref ref-type="bibr" rid="CR23">23</xref>, <xref ref-type="bibr" rid="CR29">29</xref>, <xref ref-type="bibr" rid="CR36">36</xref>, <xref ref-type="bibr" rid="CR37">37</xref>]. Folic acid/folate intake can be increased either through consumption of a folic acid-containing supplement or consumption of staple foods fortified with folic acid in addition to a diet high in natural food of folate [<xref ref-type="bibr" rid="CR13">13</xref>, <xref ref-type="bibr" rid="CR21">21</xref>]. Importantly, the folic acid fortification was revealed to significantly decrease the prevalence of the defects in countries around the globe [<xref ref-type="bibr" rid="CR1">1</xref>, <xref ref-type="bibr" rid="CR37">37</xref>]. The prevalence of folic acid supplementation in Africa varies widely and showed folate deficiencies. Nevertheless, it is still difficult to conclude on the extent of folate deficiencies in Africa due to the limited amount of data available [<xref ref-type="bibr" rid="CR38">38</xref>]. In addition, neural tube defects are influenced by certain drugs (e.g., valproic acid, if given during 4th-week development as the neural folds are fusing), prenatal factors (e.g., maternal infection or thyroid disorder, Rh factor incompatibility, and some hereditary conditions), presence of chronic disease during pregnancy, and substance use during pregnancy [<xref ref-type="bibr" rid="CR1">1</xref>, <xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR12">12</xref>, <xref ref-type="bibr" rid="CR14">14</xref>, <xref ref-type="bibr" rid="CR18">18</xref>, <xref ref-type="bibr" rid="CR25">25</xref>, <xref ref-type="bibr" rid="CR39">39</xref>].</p><p id="Par16">The aim of this systematic review and meta-analysis is to determine the pooled birth prevalence of neural tube defects and to identify the pooled measure of association between the neural tube defects and associated risk factors in Africa.</p></sec><sec id="Sec2"><title>Methods</title><p id="Par17">The preferred reporting items for systematic reviews and meta-analysis (PRISMA) statements were adapted to report the present review of meta-analysis [<xref ref-type="bibr" rid="CR40">40</xref>] (Supplementary file <xref rid="MOESM1" ref-type="media">1</xref>). The international prospective register of a systematic review (PROSPERO) registered (CRD registration number is CRD42020169443) this review (<ext-link ext-link-type="uri" xlink:href="https://www.crd.york.ac.uk/">https://www.crd.york.ac.uk/</ext-link>).</p><sec id="Sec3"><title>Review outcomes</title><p id="Par18">The first outcome of this review was the pooled birth prevalence of neural tube defects. The second outcome was the pooled measure of association between neural tube defects and associated risk factors in Africa. Birth prevalence of neural tube defects is defined as the number of neural tube defect cases of live births and/or stillbirths at birth from the total number of births (live births and/or stillbirths) during the study period.</p></sec><sec id="Sec4"><title>Study eligibility criteria</title><p id="Par19">The inclusion criteria for this review were published and unpublished studies in any period (the study period was not restricted for inclusion), and study designs that report the birth prevalence (live births and/or stillbirths) and/or associated risk factors of neural tube defects in Africa. Case reports, anonymous reports, editorials, and conferences were excluded. The study was excluded if the total number of cases as well as the total number of births were under-reported for the prevalence objective.</p></sec><sec id="Sec5"><title>Searching strategies and information sources</title><p id="Par20">PubMed, PubMed Central, Google Scopus, Medline, Cochrane Library, JBI Library, Web of Science, Science Direct, Popline, CINAHL, African Journals Online, UCSF, WHO, and Embase databases were systematically searched up to April 18, 2020, for relevant studies. Grey literature and other sources were retrieved using Google and advanced Google Scholar searches. Reference lists, bibliographies, of identified studies were navigated for additional studies. The corresponding authors were contacted for missing important data. The primary search was performed in an advanced PubMed database, using Medical Subject Heading [MeSH] terms, (Supplementary file <xref rid="MOESM2" ref-type="media">2</xref>). Besides, the search in other databases was performed using the mentioned core search terms interchangeably (neural tube defects, newborns/live births/stillbirths, and Africa).</p></sec><sec id="Sec6"><title>Study selection</title><p id="Par21">After retrieving all studies from the databases, we exported citations to the bibliographic software, Endnote Version 7 Software, to remove the duplicate studies. Then, the reviewers screened studies based on the abstract and title for possible inclusion. Two reviewers (MO and AT) independently considered the criteria (pre-determined selection criteria) to select studies. The first two authors, independent of each other, selected all articles. Studies were deeply reviewed entirely in order to identify the final included article.</p></sec><sec id="Sec7"><title>Methodological quality</title><p id="Par22">We used the Joanna Briggs Institute (JBI) quality appraisal scale to assess the risk of bias in each study [<xref ref-type="bibr" rid="CR41">41</xref>]. Essentially, two reviewers (MO and MS) independently assessed the quality of each study. Disagreements raised between reviewers were solved based on discussions or by taking the average score of the two reviewers. The JBI quality appraisal scales were adapted for the cohort studies, cross-sectional studies, case-control studies, and for the studies reporting the prevalence data (Supplementary file <xref rid="MOESM3" ref-type="media">3</xref>). The study was considered low risk if the study scored five and above points in all quality assessment items.</p></sec><sec id="Sec8"><title>Data extraction</title><p id="Par23">After including the eligible studies, three reviewers (AT, MS, and MO) extracted all essential data independently using a standardized, pre-specified, data abstraction format. The pre-specified format minimized the reviewers’ conflict of interest in the data extraction process but for any discrepancy of interests raised, the discussion was used to solve raised issues. If necessary, the main author of the study was communicated.</p><p id="Par24">The data extraction format included first author, study country, publication year, sample size, study duration, study design, prevalence period, study setting, birth outcome, the birth prevalence of neural tube defects, and associated risk factors (adjusted odds ratio with a confidence interval of the variables were taken based on available literature). Prevalence reports of all studies in the different denominators have been converted into per 10, 000 births to maintain uniformity. Then, we have used per 10, 000 prevalence estimates for reporting the findings of this review. The assessed factors were folic acid supplementation during early pregnancy, consanguineous marriage, male newborn, and substance abuse during pregnancy.</p><sec id="Sec9"><title>Meta-analyses</title><p id="Par25">The data analyses were conducted using STATA Version 14 Statistical Software. The data were extracted in Microsoft Excel and it was exported into STATA 14 Software for further analyses. For all studies, the median value, interquartile range, and the minimum and maximum values of neural tube defects were calculated.</p><p id="Par26">The heterogeneity between the studies was assessed using visual and statistical techniques. Visually, the Galbraith plot and Forest plot were used to assessing the presence of heterogeneity. The Q test and I-Squared (I<sup>2</sup>) test statistics were considered to examine the variations. The heterogeneity was declared as low, moderate, or high when the I<sup>2</sup> test statistic result became 25 %, 50 %, and 75 %, respectively [<xref ref-type="bibr" rid="CR42">42</xref>]. This review displayed that there was significant heterogeneity among studies (<italic>P</italic>-value < 0.001). Thus, we adopted the random effect model to get the birth prevalence of neural tube defects [<xref ref-type="bibr" rid="CR43">43</xref>]. However, the analysis demonstrated that there was a non-significant heterogeneity in estimating an association, and the fixed-effect model was adopted to analyze the association between neural tube defects and factors [<xref ref-type="bibr" rid="CR44">44</xref>].</p><p id="Par27">Given the variations in estimating the pooled birth prevalence, we conducted a subgroup analysis based on identified covariates to reduce the heterogeneity. Random effect meta-regression analyses were accounted for to determine the source of heterogeneity. We performed the sensitivity analyses to evaluate the influence of the study on the overall pooled estimates (the outputs of influence/sensitivity analyses were displayed graphically as well). We performed the time-trend analysis in order to visualize the random variations in the time sequence. A meta-cumulative analysis was done to display the pattern of effects and to show the significance of cumulative effect over the publication years.</p><p id="Par28">The publication bias was checked using Egger’s regression test (and Begg’s test) statistics [<xref ref-type="bibr" rid="CR45">45</xref>, <xref ref-type="bibr" rid="CR46">46</xref>] and we declared the presence of significant publication bias if a <italic>P</italic>-value became less than 0.05. Egger’s plot and the funnel plot were also considered. The trim and fill analyses were considered to mitigate the publication bias.</p></sec></sec></sec><sec id="Sec10"><title>Results</title><p id="Par29">The comprehensive search of databases yielded 413 studies about neural tube defects and associated risk factors in Africa. Of 223 unduplicated studies, we excluded 156 after reviewing the titles and abstracts. The remaining sixty-seven studies were screened and sixteen were excluded because of the outcome interests. Thus, fifty-one studies were assessed for eligibility, and 43 studies, were fulfilled the criteria, were included in this systematic review and meta-analysis (Fig. <xref rid="Fig1" ref-type="fig">1</xref>). All included original studies were cross-sectional (29), case-control (5), and prospective cohort (9) study designs [<xref ref-type="bibr" rid="CR2">2</xref>–<xref ref-type="bibr" rid="CR23">23</xref>, <xref ref-type="bibr" rid="CR47">47</xref>–<xref ref-type="bibr" rid="CR68">68</xref>]. Of these studies, we used thirty-six for prevalence estimates and all these were cross-sectional and prospective study designs [<xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR5">5</xref>–<xref ref-type="bibr" rid="CR17">17</xref>, <xref ref-type="bibr" rid="CR47">47</xref>–<xref ref-type="bibr" rid="CR55">55</xref>, <xref ref-type="bibr" rid="CR57">57</xref>–<xref ref-type="bibr" rid="CR68">68</xref>]. The total number of participants included was 6086, 384. Ten studies had been conducted in Ethiopia [<xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR5">5</xref>, <xref ref-type="bibr" rid="CR9">9</xref>–<xref ref-type="bibr" rid="CR11">11</xref>, <xref ref-type="bibr" rid="CR17">17</xref>–<xref ref-type="bibr" rid="CR20">20</xref>, <xref ref-type="bibr" rid="CR64">64</xref>], five in Tunisia [<xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR21">21</xref>–<xref ref-type="bibr" rid="CR23">23</xref>], eight in Nigeria [<xref ref-type="bibr" rid="CR6">6</xref>, <xref ref-type="bibr" rid="CR12">12</xref>, <xref ref-type="bibr" rid="CR15">15</xref>, <xref ref-type="bibr" rid="CR16">16</xref>, <xref ref-type="bibr" rid="CR50">50</xref>, <xref ref-type="bibr" rid="CR51">51</xref>, <xref ref-type="bibr" rid="CR65">65</xref>, <xref ref-type="bibr" rid="CR66">66</xref>], two in Algeria [<xref ref-type="bibr" rid="CR4">4</xref>, <xref ref-type="bibr" rid="CR7">7</xref>], six in South Africa [<xref ref-type="bibr" rid="CR55">55</xref>, <xref ref-type="bibr" rid="CR59">59</xref>, <xref ref-type="bibr" rid="CR60">60</xref>, <xref ref-type="bibr" rid="CR63">63</xref>, <xref ref-type="bibr" rid="CR67">67</xref>, <xref ref-type="bibr" rid="CR68">68</xref>], two in Sudan [<xref ref-type="bibr" rid="CR48">48</xref>, <xref ref-type="bibr" rid="CR62">62</xref>], and two in Ghana [<xref ref-type="bibr" rid="CR49">49</xref>, <xref ref-type="bibr" rid="CR57">57</xref>]. Study was conducted in Kenya [<xref ref-type="bibr" rid="CR13">13</xref>], Eritrea [<xref ref-type="bibr" rid="CR14">14</xref>], Libya [<xref ref-type="bibr" rid="CR52">52</xref>], Egypt [<xref ref-type="bibr" rid="CR53">53</xref>], Cameron [<xref ref-type="bibr" rid="CR54">54</xref>], Malawi [<xref ref-type="bibr" rid="CR58">58</xref>], Tanzania [<xref ref-type="bibr" rid="CR61">61</xref>], and Democratic Republic (DR) of Congo [<xref ref-type="bibr" rid="CR47">47</xref>] (Table <xref rid="Tab1" ref-type="table">1</xref>). The period prevalence, birth outcome, study setting, and study quality were presented in Table <xref rid="Tab2" ref-type="table">2</xref>. In addition to studies explained in Table <xref rid="Tab2" ref-type="table">2</xref>, studies done by Atlaw et al. [<xref ref-type="bibr" rid="CR18">18</xref>], Berihu et al. [<xref ref-type="bibr" rid="CR19">19</xref>], Aynalem et al. [<xref ref-type="bibr" rid="CR20">20</xref>], Nasri et al. [<xref ref-type="bibr" rid="CR21">21</xref>], Bourouba et al. [<xref ref-type="bibr" rid="CR4">4</xref>], Kitova et al. [<xref ref-type="bibr" rid="CR22">22</xref>], and Nasri et al. [<xref ref-type="bibr" rid="CR23">23</xref>] were declared low risk.
<fig id="Fig1"><label>Fig. 1</label><caption><p>Study selection flow diagram, a figure adapted from the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) group statement</p></caption><graphic xlink:href="12887_2021_2653_Fig1_HTML" id="MO1"></graphic></fig><table-wrap id="Tab1"><label>Table 1</label><caption><p>The characteristics of the studies included in the systematic review and meta-analysis, 2020</p></caption><table frame="hsides" rules="groups"><thead><tr><th>First author</th><th>Year</th><th>Country</th><th>Study design</th><th>Sample size</th><th>Duration/months</th><th>Prevalence per 10, 000 births</th></tr></thead><tbody><tr><td>Gedefaw et al. [<xref ref-type="bibr" rid="CR2">2</xref>]</td><td>2018</td><td>Ethiopia</td><td>Cross-sectional</td><td>8677</td><td>7</td><td>63</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR3">3</xref>]</td><td>2014</td><td>Tunisia</td><td>Cross-sectional</td><td>3,803,889</td><td>240</td><td>2</td></tr><tr><td>Adane et al. [<xref ref-type="bibr" rid="CR5">5</xref>]</td><td>2018</td><td>Ethiopia</td><td>Cross-sectional</td><td>19,650</td><td>36</td><td>52</td></tr><tr><td>Anyanwu et al. [<xref ref-type="bibr" rid="CR6">6</xref>]</td><td>2015</td><td>Nigeria</td><td>Cross-sectional</td><td>1456</td><td>9</td><td>27</td></tr><tr><td>Houchar et al. [<xref ref-type="bibr" rid="CR7">7</xref>]</td><td>2008</td><td>Algeria</td><td>Cross-sectional</td><td>28,500</td><td>36</td><td>75</td></tr><tr><td>Berihu et al. [<xref ref-type="bibr" rid="CR9">9</xref>]</td><td>2018</td><td>Ethiopia</td><td>Cross-sectional</td><td>14,903</td><td>9</td><td>131</td></tr><tr><td>Taye et al. [<xref ref-type="bibr" rid="CR10">10</xref>]</td><td>2019</td><td>Ethiopia</td><td>Cross-sectional</td><td>76,201</td><td>6</td><td>40</td></tr><tr><td>Abebe et al. [<xref ref-type="bibr" rid="CR11">11</xref>]</td><td>2020</td><td>Ethiopia</td><td>Cross-sectional</td><td>45,951</td><td>60</td><td>41</td></tr><tr><td>Nnadi et al. [<xref ref-type="bibr" rid="CR12">12</xref>]</td><td>2016</td><td>Nigeria</td><td>Prospective</td><td>10,163</td><td>36</td><td>22</td></tr><tr><td>Githuku et al. [<xref ref-type="bibr" rid="CR13">13</xref>]</td><td>2014</td><td>Kenya</td><td>Cross-sectional</td><td>6041</td><td>72</td><td>3</td></tr><tr><td>Estifanos etal [<xref ref-type="bibr" rid="CR14">14</xref>].</td><td>2017</td><td>Eritrea</td><td>Cross-sectional</td><td>39,803</td><td>24</td><td>39</td></tr><tr><td>Toma et al. [<xref ref-type="bibr" rid="CR15">15</xref>]</td><td>2018</td><td>Nigeria</td><td>Cross-sectional</td><td>1046</td><td>35</td><td>250</td></tr><tr><td>Audu et al. [<xref ref-type="bibr" rid="CR16">16</xref>]</td><td>2004</td><td>Nigeria</td><td>Cross-sectional</td><td>2250</td><td>48</td><td>80</td></tr><tr><td>Legesse et al. [<xref ref-type="bibr" rid="CR17">17</xref>]</td><td>2019</td><td>Ethiopia</td><td>Prospective</td><td>956</td><td>7</td><td>63</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR8">8</xref>]</td><td>2015</td><td>Tunisia</td><td>Cross-sectional</td><td>764,431</td><td>48</td><td>2</td></tr><tr><td>Atlaw et al. [<xref ref-type="bibr" rid="CR18">18</xref>]</td><td>2019</td><td>Ethiopia</td><td>Case-control</td><td>462</td><td>6</td><td>–</td></tr><tr><td>Berihu et al. [<xref ref-type="bibr" rid="CR19">19</xref>]</td><td>2019</td><td>Ethiopia</td><td>Case-control</td><td>617</td><td>9</td><td>–</td></tr><tr><td>Aynalem etal [<xref ref-type="bibr" rid="CR20">20</xref>].</td><td>2018</td><td>Ethiopia</td><td>Case-control</td><td>180</td><td>7</td><td>–</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR21">21</xref>]</td><td>2015</td><td>Tunisia</td><td>Case-control</td><td>150</td><td>7</td><td>–</td></tr><tr><td>Bourouba et al. [<xref ref-type="bibr" rid="CR4">4</xref>]</td><td>2018</td><td>Algeria</td><td>Case-control</td><td>130</td><td>12</td><td>–</td></tr><tr><td>Kitova et al. [<xref ref-type="bibr" rid="CR22">22</xref>]</td><td>2013</td><td>Tunisia</td><td>Prospective</td><td>150</td><td>36</td><td>–</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR23">23</xref>]</td><td>2016</td><td>Tunisia</td><td>Prospective</td><td>132</td><td>9</td><td>–</td></tr><tr><td>Ahuka et al. [<xref ref-type="bibr" rid="CR47">47</xref>]</td><td>2006</td><td>DR Congo</td><td>Cross-sectional</td><td>8824</td><td>96</td><td>10</td></tr><tr><td>Oumer et al. [<xref ref-type="bibr" rid="CR48">48</xref>]</td><td>2016</td><td>Sudan</td><td>Cross-sectional</td><td>36,785</td><td>12</td><td>28</td></tr><tr><td>Alhassan et al. [<xref ref-type="bibr" rid="CR49">49</xref>]</td><td>2017</td><td>Ghana</td><td>Cross-sectional</td><td>35,426</td><td>48</td><td>16</td></tr><tr><td>Alrede et al. [<xref ref-type="bibr" rid="CR50">50</xref>]</td><td>1992</td><td>Nigeria</td><td>Prospective</td><td>5, 977</td><td>36</td><td>70</td></tr><tr><td>Ekanem et al. [<xref ref-type="bibr" rid="CR51">51</xref>]</td><td>2008</td><td>Nigeria</td><td>Cross-sectional</td><td>127,929</td><td>276</td><td>5</td></tr><tr><td>Singh et al. [<xref ref-type="bibr" rid="CR52">52</xref>]</td><td>2000</td><td>Libya</td><td>Prospective</td><td>15, 938</td><td>12</td><td>8</td></tr><tr><td>Mohammed etal [<xref ref-type="bibr" rid="CR53">53</xref>].</td><td>2011</td><td>Egypt</td><td>Cross-sectional</td><td>5000</td><td>7</td><td>16</td></tr><tr><td>Njamnshi et al. [<xref ref-type="bibr" rid="CR54">54</xref>]</td><td>2008</td><td>Cameron</td><td>Cross-sectional</td><td>52,710</td><td>120</td><td>19</td></tr><tr><td>Sayed et al. [<xref ref-type="bibr" rid="CR55">55</xref>]</td><td>2008</td><td>South Africa</td><td>Prospective</td><td>53,000</td><td>9</td><td>10</td></tr><tr><td>Masamati et al. [<xref ref-type="bibr" rid="CR58">58</xref>]</td><td>2000</td><td>Malawi</td><td>Cross-sectional</td><td>25,562</td><td>24</td><td>6</td></tr><tr><td>Venter et al. [<xref ref-type="bibr" rid="CR59">59</xref>]</td><td>1995</td><td>South Africa</td><td>Prospective</td><td>10,380</td><td>40</td><td>36</td></tr><tr><td>Buccimazzaetal [<xref ref-type="bibr" rid="CR60">60</xref>].</td><td>1994</td><td>South Africa</td><td>Cross-sectional</td><td>516,252</td><td>240</td><td>12</td></tr><tr><td>Kinasha et al. [<xref ref-type="bibr" rid="CR61">61</xref>]</td><td>2003</td><td>Tanzania</td><td>Cross-sectional</td><td>34,000</td><td>24</td><td>30</td></tr><tr><td>Elsheikh et al. [<xref ref-type="bibr" rid="CR62">62</xref>]</td><td>2009</td><td>Sudan</td><td>Prospective</td><td>18,378</td><td>12</td><td>35</td></tr><tr><td>Krzesinski etal [<xref ref-type="bibr" rid="CR63">63</xref>].</td><td>2019</td><td>South Africa</td><td>Cross-sectional</td><td>93,609</td><td>72</td><td>7</td></tr><tr><td>Anyebuno et al. [<xref ref-type="bibr" rid="CR57">57</xref>]</td><td>1993</td><td>Ghana</td><td>Cross-sectional</td><td>19,094</td><td>24</td><td>12</td></tr><tr><td>Adetiloye et al. [<xref ref-type="bibr" rid="CR66">66</xref>]</td><td>1993</td><td>Nigeria</td><td>Cross-sectional</td><td>23, 438</td><td>120</td><td>5</td></tr><tr><td>Sorri et al. [<xref ref-type="bibr" rid="CR64">64</xref>]</td><td>2015</td><td>Ethiopia</td><td>Cross-sectional</td><td>28, 961</td><td>36</td><td>54</td></tr><tr><td>Ugwo et al. [<xref ref-type="bibr" rid="CR65">65</xref>]</td><td>2007</td><td>Nigeria</td><td>Cross-sectional</td><td>2, 891</td><td>48</td><td>128</td></tr><tr><td>Cornell et al. [<xref ref-type="bibr" rid="CR67">67</xref>]</td><td>1983</td><td>South Africa</td><td>Cross-sectional</td><td>116, 859</td><td>60</td><td>9</td></tr><tr><td>Kromberg et al. [<xref ref-type="bibr" rid="CR68">68</xref>]</td><td>1982</td><td>South Africa</td><td>Cross-sectional</td><td>29, 633</td><td>–</td><td>8</td></tr></tbody></table></table-wrap><table-wrap id="Tab2"><label>Table 2</label><caption><p>The study period, setting, birth outcome, and quality of included studies in the systematic review and meta-analysis, 2020</p></caption><table frame="hsides" rules="groups"><thead><tr><th>First author</th><th>Birth outcome</th><th>Prevalence period</th><th>Study setting</th><th>Study quality</th></tr></thead><tbody><tr><td>Gedefaw et al. [<xref ref-type="bibr" rid="CR2">2</xref>]</td><td>LB + SB</td><td>2016</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR3">3</xref>]</td><td>LB + SB</td><td>1991–2011</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Adane et al. [<xref ref-type="bibr" rid="CR5">5</xref>]</td><td>LB + SB</td><td>2015–2017</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Anyanwu et al. [<xref ref-type="bibr" rid="CR6">6</xref>]</td><td>LB</td><td>2013</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Houchar et al. [<xref ref-type="bibr" rid="CR7">7</xref>]</td><td>LB + SB</td><td>2004–2006</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Berihu et al. [<xref ref-type="bibr" rid="CR9">9</xref>]</td><td>LB + SB</td><td>2016–2017</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Taye et al. [<xref ref-type="bibr" rid="CR10">10</xref>]</td><td>LB</td><td>2015</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Abebe et al. [<xref ref-type="bibr" rid="CR11">11</xref>]</td><td>LB + SB</td><td>2011–2015</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Nnadi et al. [<xref ref-type="bibr" rid="CR12">12</xref>]</td><td>LB + SB</td><td>2011–2013</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Githuku et al. [<xref ref-type="bibr" rid="CR13">13</xref>]</td><td>LB</td><td>2005–2010</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Estifanos et al. [<xref ref-type="bibr" rid="CR14">14</xref>]</td><td>LB + SB</td><td>2007–2011</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Toma et al. [<xref ref-type="bibr" rid="CR15">15</xref>]</td><td>LB + SB</td><td>2013–2016</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Audu et al. [<xref ref-type="bibr" rid="CR16">16</xref>]</td><td>LB</td><td>2000–2003</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Legesse et al. [<xref ref-type="bibr" rid="CR17">17</xref>]</td><td>LB + SB</td><td>2018–2019</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR8">8</xref>]</td><td>LB + SB</td><td>2008–2011</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Ahuka et al. [<xref ref-type="bibr" rid="CR47">47</xref>]</td><td>LB</td><td>1993–2001</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Oumer et al. [<xref ref-type="bibr" rid="CR48">48</xref>]</td><td>LB + SB</td><td>2014–2015</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Alhassan et al. [<xref ref-type="bibr" rid="CR49">49</xref>]</td><td>LB + SB</td><td>2010–2014</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Alrede et al. [<xref ref-type="bibr" rid="CR50">50</xref>]</td><td>LB + SB</td><td>1987–1990</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Ekanem et al. [<xref ref-type="bibr" rid="CR51">51</xref>]</td><td>LB + SB</td><td>1980–2003</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Singh et al. [<xref ref-type="bibr" rid="CR52">52</xref>]</td><td>LB + SB</td><td>1995–1996</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Mohammed et al. [<xref ref-type="bibr" rid="CR53">53</xref>]</td><td>LB</td><td>2007</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Njamnshi et al. [<xref ref-type="bibr" rid="CR54">54</xref>]</td><td>LB + SB</td><td>1997–2006</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Sayed et al. [<xref ref-type="bibr" rid="CR55">55</xref>]</td><td>LB + SB</td><td>2004–2005</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Masamati et al. [<xref ref-type="bibr" rid="CR58">58</xref>]</td><td>LB + SB</td><td>1998–1999</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Venter et al. [<xref ref-type="bibr" rid="CR59">59</xref>]</td><td>LB</td><td>1989–1992</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Buccimazza etal [<xref ref-type="bibr" rid="CR60">60</xref>].</td><td>LB + SB</td><td>1973–1992</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Kinasha et al. [<xref ref-type="bibr" rid="CR61">61</xref>]</td><td>LB</td><td>2000–2002</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Elsheikh et al. [<xref ref-type="bibr" rid="CR62">62</xref>]</td><td>LB + SB</td><td>2003–2004</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Krzesinski et al. [<xref ref-type="bibr" rid="CR63">63</xref>]</td><td>LB + SB</td><td>2003–2013</td><td>Institution-based</td><td>Low risk</td></tr><tr><td>Anyebuno et al. [<xref ref-type="bibr" rid="CR57">57</xref>]</td><td>LB + SB</td><td>1991–1992</td><td>Institution-based</td><td>High risk</td></tr><tr><td>Adetiloye et al. [<xref ref-type="bibr" rid="CR66">66</xref>]</td><td>LB + SB</td><td>1982–1992</td><td>Institution-based</td><td>High risk</td></tr><tr><td>Sorri et al. [<xref ref-type="bibr" rid="CR64">64</xref>]</td><td>LB + SB</td><td>2009–2012</td><td>Institution-based</td><td>–</td></tr><tr><td>Ugwo et al. [<xref ref-type="bibr" rid="CR65">65</xref>]</td><td>LB + SB</td><td>2002–2005</td><td>Institution-based</td><td>–</td></tr><tr><td>Cornell et al. [<xref ref-type="bibr" rid="CR67">67</xref>]</td><td>LB + SB</td><td>1975–1980</td><td>Institution-based</td><td>–</td></tr><tr><td>Kromberg et al. [<xref ref-type="bibr" rid="CR68">68</xref>]</td><td>LB + SB</td><td>–</td><td>Institution-based</td><td>–</td></tr></tbody></table><table-wrap-foot><p>Key: <italic>LB</italic> Live births, <italic>SB</italic> Stillbirths</p></table-wrap-foot></table-wrap></p><p id="Par30">The pooled birth prevalence of neural tube defects in the present meta-analysis was 21.42 (95% CI: 19.29, 23.56) per 10,000 births. A forest plot showed that there was significant heterogeneity across the studies (<italic>P</italic>-value < 0.001, I<sup>2</sup> = 98.5%). Therefore, a random-effect model was applied to pool the overall prevalence [<xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR5">5</xref>–<xref ref-type="bibr" rid="CR17">17</xref>, <xref ref-type="bibr" rid="CR47">47</xref>–<xref ref-type="bibr" rid="CR55">55</xref>, <xref ref-type="bibr" rid="CR57">57</xref>–<xref ref-type="bibr" rid="CR68">68</xref>] (Fig. <xref rid="Fig2" ref-type="fig">2</xref>). For thirty-six studies, the median value of neural tube defects was 24.5 and the inter-quartile range was between 8.5 and 53 per 10, 000 births. The minimum and maximum values were 2 and 250 per 10, 000 births.
<fig id="Fig2"><label>Fig. 2</label><caption><p>Forest plot showing the pooled prevalence of neural tube defects in Africa, 2020</p></caption><graphic xlink:href="12887_2021_2653_Fig2_HTML" id="MO2"></graphic></fig></p><p id="Par31">Subgroup analyses based on the period prevalence, region/country, the birth outcome, and design was performed. The highest and the lowest prevalence rate was found in Algeria (75.0, 95% CI: 64.98, 85.02) and in Tunisia (2.0, 95% CI: 1.87, 2.13, per 10,000 births) (Supplementary file <xref rid="MOESM4" ref-type="media">4</xref>). Based on the birth outcome (I<sup>2</sup> = 98.5%), the prevalence for live births only was 26.85 (95% CI: 13.43, 40.27) and for both live birth and stillbirths was 19.76 (95% CI: 17.49, 22.03) per 10,000 births. Concerning the study designs (I<sup>2</sup> = 98.5%), the prevalence for the cross-sectional (21.01, 95% CI: 18.74, 23.27) was lower than the prospective cohort study designs (28.35, 95% CI: 17.53, 39.17, per 10, 000 births). Based on the period prevalence (I<sup>2</sup> = 98.5%), the burden of neural tube defects for the period after 2010 was 49.55 (95% CI: 36.50, 62.61), 2001–2010 was 29.48 (95% CI: 22.10, 36.87), 1991–2011 was 2.0 (95% CI: 1.86, 2.14), 1991–2000 was 12.42 (95% CI: 6.46, 18.38), 1980–2003 was 5.0 (95% CI: 3.77, 6.22), and before 1990 was 10.65 (95% CI: 6.52, 14.77) per 10,000 births.</p><p id="Par32">Sample size (<italic>P</italic>-value = 0.78), year of publication (<italic>P</italic>-value = 0.37), duration of the study in months (<italic>P</italic>-value = 0.74), study quality score (<italic>P</italic>-value = 0.69), study country (<italic>P</italic>-value = 0.03), study design (<italic>P</italic>-value = 0.84), birth outcome (<italic>P</italic>-value = 0.63), and period prevalence (<italic>P</italic>-value = 0.47) were analyzed for the source of heterogeneity and only study country was found statistically significant.</p><p id="Par33">In the current systematic review and meta-analysis, except for two Tunisian studies (years 2014 and 2015), the influence of studies on the overall estimates was uniform (Fig. <xref rid="Fig3" ref-type="fig">3</xref>). Meta-influence estimates were analyzed by removing one article at a time and the uniform influence was displayed and the prevalence after removing only the 2014 Tunisia study was 26.64 (95% CI: 23.0, 30.28), and after removing only the 2015 Tunisia study was 26.56 (95% CI: 22.96, 30.16) (Fig. <xref rid="Fig3" ref-type="fig">3</xref>). If both studies are omitted together, the prevalence was 28.24 (95% CI: 24.22, 32.27) with uniform influence. Even if the whole analysis was repeated after omitting the two studies, the heterogeneity across studies was not decreased (97.5%, only 1% reduction). We looked at the effect of low-quality studies on the overall estimates by limiting those studies included in a meta-analysis. The meta-analysis estimate was found by including studies that only scored greater than or equal to five, high-quality studies; therefore, its pooled estimate was 22.31 per 10,000 births.
<fig id="Fig3"><label>Fig. 3</label><caption><p>Sensitivity analysis showed the influence of each individual study in overall estimates in Africa, 2020</p></caption><graphic xlink:href="12887_2021_2653_Fig3_HTML" id="MO3"></graphic></fig></p><p id="Par34">The relationship between the burden of neural tube defects and the study publication years from 1982 (8.0) to 2020 (41 per 10,000 births) was visualized using the time trend analyses. Besides, the pattern of effects on the time, from the year 1982 (8.0) to the year 2020 (21.42 per 10,000 births), was displayed using the meta-cumulative analyses and the cumulative effects of all studies were significant (Fig. <xref rid="Fig4" ref-type="fig">4</xref>).
<fig id="Fig4"><label>Fig. 4</label><caption><p>Meta-cumulative analysis showing cumulative effect of neural tube defects in relation to time in Africa, 2020</p></caption><graphic xlink:href="12887_2021_2653_Fig4_HTML" id="MO4"></graphic></fig></p><p id="Par35">In estimating the birth prevalence, a significant publication bias was identified by Egger’s tests (<italic>P</italic>-value < 0.001) and its plot (Fig. <xref rid="Fig5" ref-type="fig">5</xref>). We conducted the trim and fill meta-analyses to adjust this bias. We analyzed fifty-five studies (19 articles were filled in the 36 studies) in the fill meta-analyses. As a result, the birth prevalence of neural tube defects using the random-effect model was 5.14 (95% CI: 2.90, 7.38) per 10,000 births. This adjusted estimate suggested a lower risk of bias than the original analysis. However, publication bias is still significant after fill and trim analyses have been done.
<fig id="Fig5"><label>Fig. 5</label><caption><p>Egger’s publication bias plot, 2020</p></caption><graphic xlink:href="12887_2021_2653_Fig5_HTML" id="MO5"></graphic></fig></p><p id="Par36">In this meta-analysis, folic acid supplementation during early pregnancy, consanguineous marriage, male newborn, and substance abuse during pregnancy (smoking, alcohol, especially) were the variables analyzed for association with neural tube defects. In estimating the association of all factors, there was no statistically significant publication bias among studies. Similarly, the Galbraith plot visualized that there was no heterogeneity among the studies. The summary of studies (odds ratio, confidence interval, etc.) included in the meta-analyses for an association was explained in Table <xref rid="Tab3" ref-type="table">3</xref>.
<table-wrap id="Tab3"><label>Table 3</label><caption><p>Summary of studies included in the meta-analysis for association with neural tube defects, 2020</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="2">First author</th><th rowspan="2">Year</th><th rowspan="2">Country</th><th>Associated factors</th><th rowspan="2">Odds ratio</th><th colspan="2">95% confidence interval</th></tr><tr><th>Folic acid</th><th>UCI</th><th>LCI</th></tr></thead><tbody><tr><td>Gedefaw et al. [<xref ref-type="bibr" rid="CR2">2</xref>]</td><td>2018</td><td>Ethiopia</td><td></td><td>0.47</td><td>0.95</td><td>0.23</td></tr><tr><td>Bourouba et al. [<xref ref-type="bibr" rid="CR4">4</xref>]</td><td>2018</td><td>Algeria</td><td></td><td>0.24</td><td>1.15</td><td>0.03</td></tr><tr><td>Anyanwu et al. [<xref ref-type="bibr" rid="CR6">6</xref>]</td><td>2015</td><td>Nigeria</td><td></td><td>0.36</td><td>19.27</td><td>0.03</td></tr><tr><td>Atlaw et al. [<xref ref-type="bibr" rid="CR18">18</xref>]</td><td>2019</td><td>Ethiopia</td><td></td><td>0.095</td><td>0.29</td><td>0.001</td></tr><tr><td>Berihu et al. [<xref ref-type="bibr" rid="CR19">19</xref>]</td><td>2019</td><td>Ethiopia</td><td></td><td>0.48</td><td>1.04</td><td>0.2</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR21">21</xref>]</td><td>2015</td><td>Tunisia</td><td></td><td>1.19</td><td>2.44</td><td>0.58</td></tr><tr><td>Nasri et al. [<xref ref-type="bibr" rid="CR23">23</xref>]</td><td>2016</td><td>Tunisia</td><td></td><td>0.15</td><td>0.44</td><td>0.04</td></tr><tr><td colspan="4"><bold>Pooled/net odds ratio</bold></td><td><bold>0.51</bold></td><td><bold>2.29</bold></td><td><bold>0.11</bold></td></tr><tr><td colspan="7"><bold>Consanguineous marriage</bold></td></tr><tr><td> Atlaw et al. [<xref ref-type="bibr" rid="CR18">18</xref>]</td><td>2019</td><td>Ethiopia</td><td></td><td>5.54</td><td>20.9</td><td>1.47</td></tr><tr><td> Nasri et al. [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR21">21</xref>]</td><td>2015</td><td>Tunisia</td><td></td><td>2.09</td><td>6.1</td><td>0.76</td></tr><tr><td> Kitova et al. [<xref ref-type="bibr" rid="CR22">22</xref>]</td><td>2013</td><td>Tunisia</td><td></td><td>2.46</td><td>6.37</td><td>0.95</td></tr><tr><td> Nasri et al. [<xref ref-type="bibr" rid="CR23">23</xref>]</td><td>2016</td><td>Tunisia</td><td></td><td>2.59</td><td>11.9</td><td>0.69</td></tr><tr><td> Nasri et al. [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR21">21</xref>]</td><td>2015</td><td>Tunisia</td><td></td><td>1.27</td><td>4.59</td><td>0.35</td></tr><tr><td colspan="4"><bold>Pooled/net odds ratio</bold></td><td><bold>2.41</bold></td><td><bold>18.47</bold></td><td><bold>0.31</bold></td></tr><tr><td colspan="7"><bold>Male newborn</bold></td></tr><tr><td> Gedefaw et al. [<xref ref-type="bibr" rid="CR2">2</xref>]</td><td>2018</td><td>Ethiopia</td><td></td><td>0.56</td><td>0.94</td><td>0.33</td></tr><tr><td> Nasri et al. [<xref ref-type="bibr" rid="CR3">3</xref>]</td><td>2014</td><td>Tunisia</td><td></td><td>0.68</td><td>0.79</td><td>0.59</td></tr><tr><td> Anyanwu et al. [<xref ref-type="bibr" rid="CR6">6</xref>]</td><td>2015</td><td>Nigeria</td><td></td><td>0.92</td><td>12.77</td><td>0.07</td></tr><tr><td> Houchar et al. [<xref ref-type="bibr" rid="CR7">7</xref>]</td><td>2008</td><td>Algeria</td><td></td><td>0.7</td><td>0.92</td><td>0.52</td></tr><tr><td> Atlaw et al. [<xref ref-type="bibr" rid="CR18">18</xref>]</td><td>2019</td><td>Ethiopia</td><td></td><td>0.72</td><td>1.37</td><td>0.38</td></tr><tr><td> Aynalem et al. [<xref ref-type="bibr" rid="CR20">20</xref>]</td><td>2018</td><td>Ethiopia</td><td></td><td>0.58</td><td>1.14</td><td>0.3</td></tr><tr><td> Nasri et al. [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR21">21</xref>]</td><td>2015</td><td>Tunisia</td><td></td><td>0.49</td><td>1.27</td><td>0.19</td></tr><tr><td colspan="4"><bold>Pooled/net odds ratio</bold></td><td><bold>0.67</bold></td><td><bold>1.06</bold></td><td><bold>0.42</bold></td></tr><tr><td colspan="7"><bold>Substance abuse during pregnancy</bold></td></tr><tr><td> Atlaw et al. [<xref ref-type="bibr" rid="CR18">18</xref>]</td><td>2019</td><td>Ethiopia</td><td></td><td>11.08</td><td>62.7</td><td>1.96</td></tr><tr><td> Berihu et al. [<xref ref-type="bibr" rid="CR19">19</xref>]</td><td>2019</td><td>Ethiopia</td><td></td><td>10.3</td><td>88.5</td><td>1.19</td></tr><tr><td> Aynalem et al. [<xref ref-type="bibr" rid="CR20">20</xref>]</td><td>2018</td><td>Ethiopia</td><td></td><td>0.56</td><td>1.5</td><td>0.21</td></tr><tr><td colspan="4"><bold>Pooled/net odds ratio</bold></td><td><bold>1.52</bold></td><td><bold>33.28</bold></td><td><bold>0.07</bold></td></tr></tbody></table><table-wrap-foot><p>Key: The different numbers of articles in different analysis/variables is due to a lack of similarity in studies reporting the risk factors</p></table-wrap-foot></table-wrap></p><p id="Par37">Taking folic acid during early pregnancy (Pooled OR (Odds Ratio) = 0.51, 95% CI: 0.11, 2.29), consanguineous marriage (Pooled OR = 2.41, 95% CI: 0.31, 18.47), male sex (Pooled OR = 0.67, 95% CI: 0.42, 1.06), and substance abuse during pregnancy (Pooled OR = 1.52, 95% CI: 0.07, 33.28) were assessed and none of them was statistically significant (Supplementary file <xref rid="MOESM4" ref-type="media">4</xref>).</p></sec><sec id="Sec11"><title>Discussion</title><p id="Par38">The present systematic review and meta-analysis were conducted to assess the pooled birth prevalence of neural tube defects and to identify the risk factors associated with the occurrence of neural tube defects. This review revealed the pooled birth prevalence in Africa and it evaluated the risk factors (folic acid uptake, consanguineous marriage, male newborn, and substance abuse during pregnancy) for association with neural tube defects. The hidden burden of neural tube defects is very high in Africa. The primary data research and systematic review/meta-analysis that show this burden are scarce. However, the effects of the defects are related to substantial mortality, disability, and psychological costs and it is an important public health problem [<xref ref-type="bibr" rid="CR24">24</xref>, <xref ref-type="bibr" rid="CR69">69</xref>–<xref ref-type="bibr" rid="CR73">73</xref>].</p><p id="Par39">The pooled birth prevalence of the neural tube defects in the present meta-analysis was found 21.42 per 10,000 births with a range of 19.29–23.56. Different prevalence rates have been reported by the review conducted in Indian [<xref ref-type="bibr" rid="CR74">74</xref>], Latin America [<xref ref-type="bibr" rid="CR75">75</xref>], and worldwide [<xref ref-type="bibr" rid="CR24">24</xref>]. Variation in estimates was also observed in reviews reported elsewhere [<xref ref-type="bibr" rid="CR69">69</xref>, <xref ref-type="bibr" rid="CR70">70</xref>, <xref ref-type="bibr" rid="CR74">74</xref>, <xref ref-type="bibr" rid="CR75">75</xref>]. The prevalence of the defect remains high in less-developed countries of Africa, Latin America, Asia, and the Far East [<xref ref-type="bibr" rid="CR1">1</xref>, <xref ref-type="bibr" rid="CR71">71</xref>–<xref ref-type="bibr" rid="CR73">73</xref>]. The variation in estimates may be due to the difference in countries’ health policy, income levels, and the institution of folic acid fortification [<xref ref-type="bibr" rid="CR24">24</xref>, <xref ref-type="bibr" rid="CR72">72</xref>]. The findings have stressed the need for more surveillance efforts, particularly in low-income countries [<xref ref-type="bibr" rid="CR69">69</xref>]. In the current review, a relatively high-pooled birth prevalence of neural tube defects was detected in Algeria, Ethiopia, Eritrea, and Nigeria. Of all, the highest and lowest rates were detected in Algeria (75) and Tunisia (2), respectively. The magnitude of the defect among African countries showed geographic variations as other previous reviews have shown in various regions of the world [<xref ref-type="bibr" rid="CR24">24</xref>, <xref ref-type="bibr" rid="CR69">69</xref>–<xref ref-type="bibr" rid="CR75">75</xref>]. Thus, the variation detected across studies in estimating the pooled prevalence of neural tube defects was due to differences in study countries, period prevalence, study design, and birth outcome. The variation of estimates across countries may be also due to the difference in the folic acid supplementation/fortification, prenatal care/antenatal screening, and countries’ health policy.</p><p id="Par40">The increment of prevalence over time may be due to a change in detection methods, an increment of the practices in documenting and reporting cases, an increase of the demands for fetal pathological examinations over these years, or a real increase in disease. Besides, it may be due to an increment of practice changes that could lead to increased detections, for instance, nowadays more children are born in hospitals and more women are became tested/screened.</p><p id="Par41">Taking folic acid during early pregnancy had a non-significant association with the incidence of neural tube defects. However, this finding is not supported by different previous literature [<xref ref-type="bibr" rid="CR24">24</xref>, <xref ref-type="bibr" rid="CR25">25</xref>, <xref ref-type="bibr" rid="CR29">29</xref>, <xref ref-type="bibr" rid="CR32">32</xref>]. Although folic acid has been revealed to decrease the risk of neural tube defects in previous studies [<xref ref-type="bibr" rid="CR36">36</xref>, <xref ref-type="bibr" rid="CR37">37</xref>, <xref ref-type="bibr" rid="CR39">39</xref>, <xref ref-type="bibr" rid="CR76">76</xref>], the potential of folic acid to decrease the occurrence of the defect has not been yet examined in most African countries and preventable neural tube defects continue to occur [<xref ref-type="bibr" rid="CR25">25</xref>]. Furthermore, the utilization is affected by the persistence of socioeconomic and educational issues in the consumption of folic acid, ethnic disparities, and the existence of age-based variation of supplement use [<xref ref-type="bibr" rid="CR25">25</xref>]. Despite there are folate supplements, there is a low utilization, it is difficult to attain the recommended daily intake of folate for different reasons (relatively poor availability of folate in natural foods, easy destruction during cooking, for instance) [<xref ref-type="bibr" rid="CR77">77</xref>]. May be the lack of significance is due to the inclusion of a small number of studies (and may be these are low folic acid utilized countries, non-mandatory folic acid users) in the analyses.</p><sec id="Sec12"><title>Strength and limitations of the review</title><p id="Par42">The present systematic review and meta-analysis gave cumulative and up-to-date evidence on neural tube defects and associated risk factors in Africa. The review finding is estimated from the pooled estimate of forty-three studies in Africa and it provides valuable information to the policymakers, and this should be the ultimate contribution of this review to the field.</p><p id="Par43">The findings of the current review should be interpreted based on some limitations. The estimate did not consider the terminated pregnancies of the defect and this may reduce the pooled prevalence estimates. Moreover, the presence of significant variation across countries may underestimate the overall burden of neural tube defects in Africa. Underestimation of the burden of neural tube defects should be considered due to the missing of many stillbirths and home births that are delivered in the community setting. Furthermore, the variability of the sample size in the included studies might influence the pooled birth prevalence estimates. The risk factors are harder to assess given the limitations on that data. All studies in this review were institution-based studies. Although moderate publication bias was detected in prevalence estimates, we adjusted the bias using the trim and fill analysis.</p></sec></sec><sec id="Sec13"><title>Conclusions</title><p id="Par44">The pooled birth prevalence of neural tube defects in Africa was found high. A high-pooled prevalence of neural tube defects was detected in Algeria, Ethiopia, Eritrea, and Nigeria. The risk factors evaluated were not found significant.</p><p id="Par45">We would like to inform policymakers that the pooled birth prevalence estimates are may be underestimated due to different mentioned factors and the pooled estimate should not impact policy decisions on prevention efforts negatively in Africa where policymakers may feel that this is not a big problem to prioritize the prevention funds. Strong prevention and control measures should be the priority. Moreover, limited available data on neural tube defects inform the need for additional primary, wide scope research that would improve the true burden of the defects and facilitate preventive policies on preventive factors in Africa.</p></sec><sec sec-type="supplementary-material"><title>Supplementary Information</title><sec id="Sec14"><p><supplementary-material content-type="local-data" id="MOESM1"><media xlink:href="12887_2021_2653_MOESM1_ESM.doc"><caption><p><bold>Additional file 1: Supplementary file 1</bold>. PRISMA reporting checklist</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM2"><media xlink:href="12887_2021_2653_MOESM2_ESM.docx"><caption><p><bold>Additional file 2: Supplementary file 2</bold>. PubMed Searching methods</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM3"><media xlink:href="12887_2021_2653_MOESM3_ESM.docx"><caption><p><bold>Additional file 3: Supplementary file 3</bold>. JBI critical appraisal checklists for all designs</p></caption></media></supplementary-material><supplementary-material content-type="local-data" id="MOESM4"><media xlink:href="12887_2021_2653_MOESM4_ESM.docx"><caption><p><bold>Additional file 4: Supplementary file 4</bold>. Additional Table and Figures</p></caption></media></supplementary-material></p></sec></sec></body><back><glossary><title>Abbreviations</title><def-list><def-item><term>CI</term><def><p id="Par5">Confidence Interval</p></def></def-item><def-item><term>DR</term><def><p id="Par6">Democratic Republic</p></def></def-item><def-item><term>I<sup>2</sup></term><def><p id="Par7">I-Squared</p></def></def-item><def-item><term>JBI</term><def><p id="Par8">Joanna Briggs Institute</p></def></def-item><def-item><term>MeSH</term><def><p id="Par9">Medical Subject Heading</p></def></def-item><def-item><term>OR</term><def><p id="Par10">Odds Ratio</p></def></def-item><def-item><term>PROSPERO</term><def><p id="Par11">Prospective Register of a Systematic Review</p></def></def-item><def-item><term>PRISMA</term><def><p id="Par12">Preferred Reporting Items for Systematic Reviews and Meta-Analysis</p></def></def-item></def-list></glossary><fn-group><fn><p><bold>Publisher’s Note</bold></p><p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p></fn></fn-group><ack><p>Not applicable.</p></ack><notes notes-type="author-contribution"><title>Authors’ contributions</title><p>MO, AT, and MS participated in the conceptualization of the review protocol, formal analysis, methodology or study design, writing-original draft, interpretation, writing-review and editing, and approving the final draft. MO, MS, and AT: Quality assessment, data extraction, and literature review. All authors read and approved the manuscript.</p></notes><notes notes-type="funding-information"><title>Funding</title><p>No funding sources for this review.</p></notes><notes notes-type="data-availability"><title>Availability of data and materials</title><p>The data sets used and/or analyzed during the current systematic review and meta-analysis are included in the review and available from the corresponding author on reasonable request.</p></notes><notes><title>Declarations</title><notes id="FPar1"><title>Ethics approval and consent to participate</title><p id="Par46">Not applicable.</p></notes><notes id="FPar2"><title>Consent for publication</title><p id="Par47">Not applicable.</p></notes><notes id="FPar3" notes-type="COI-statement"><title>Competing interests</title><p id="Par48">The authors declare that they have no competing interests.</p></notes></notes><ref-list id="Bib1"><title>References</title><ref id="CR1"><label>1.</label><mixed-citation publication-type="other">Moore KL, Persaud TVN. 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