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Cited by 59Antibiotic Resistance in BacteriaUrinary Tract Infections ManagementAntibiotic Use and Resistance

Maternal colonization or infection with extended-spectrum beta-lactamase-producing Enterobacteriaceae in Africa: A systematic review and meta-analysis

Open access
Bulabula, Andre N.H., Dramowski, Angela, Mehtar, Shaheen·2017·International Journal of Infectious Diseases
DOI 10.1016/j.ijid.2017.08.015
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Abstract

OBJECTIVE: To summarize published studies on the prevalence of and risk factors for maternal bacterial colonization and/or infection with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) in pregnant and/or post-partum women in Africa. METHODS: A systematic review was conducted using the PubMed, Scopus, and Google Scholar databases. Bibliographies of included eligible studies were manually searched to identify additional relevant articles. No language restriction was applied. The timeframe of the search included all records from electronic database inception to July 15, 2017. A random-effects meta-analysis was performed to summarize the prevalence and the 95% confidence intervals (CI) of ESBL-E colonization or infection in pregnant or post-partum women in Africa. The meta-analysis was conducted using STATA IC 13.1 software and the metaprop function/plugin. RESULTS: Ten studies (seven on pregnant women and three on post-partum women) were included, documenting a 17% prevalence of maternal colonization with ESBL-E in Africa (95% CI 10-23%). The prevalence of ESBL-E in community isolates exceeded that in isolates from the hospital setting (22% vs. 14%). The most frequently reported ESBL-encoding gene was CTX-M (cefotaxime hydrolyzing capabilities). Data on risk factors for maternal ESBL-E colonization and infection are very limited. CONCLUSIONS: The prevalence of colonization and/or infection with ESBL-E in pregnant and post-partum women in Africa exceeds that reported from high- and middle-income settings, representing a risk for subsequent neonatal colonization and/or infection with ESBL-E.

AI snapshot

Written from the paper’s full text.

TL;DR

This systematic review and meta-analysis found that 17% (95% CI 10–23%) of pregnant and post-partum women in Africa were colonized or infected with extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E). The authors conclude this exceeds rates reported from high- and middle-income settings and represents a risk for subsequent neonatal colonization and/or infection.

Key findings

  • Pooled ESBL-E prevalence was 17% (95% CI 10–23%) across 10 included observational studies, with high heterogeneity (I² = 93.6%, p < 0.001).
  • Pooled prevalence was higher in pregnant women (22%, 95% CI 12–31%) than post-partum women (7%, 95% CI 2–12%), and higher in community settings (22%, 95% CI 9–34%) than hospital settings (14%, 95% CI 5–23%).
  • Colonization prevalence (19%, 95% CI 10–27%) exceeded infection prevalence (13%, 95% CI −1–27%).
  • CTX-M was the most frequently reported ESBL-encoding gene; risk-factor data were limited, with three studies reporting independent factors including private indoor drinking water access (OR 3.8, 95% CI 1.2–11.6), living in an individual house (OR 2.2, 95% CI 1.0–4.8), antimicrobial activity in stool (OR 5.4, 95% CI 2.0–14.7), single marital status (OR 2.6, 95% CI 1.1–6.1), CD4+ count <200/ml (OR 2.9, 95% CI 1.1–7.7), and current UTI symptoms (OR 2.5, 95% CI 1.1–6.0).

Methods

  • Systematic review and random-effects meta-analysis of observational studies reporting ESBL-E colonization and/or infection in pregnant or post-partum women in Africa, searching PubMed, Scopus, and Google Scholar from database inception to July 15, 2017, with no language restriction.
  • Ten studies were included (from Nigeria, Tanzania, Madagascar, South Africa, Mozambique, Uganda, and Cameroon); 1,304 participants were pooled (927 pregnant women and 377 post-partum women).
  • Proportions were pooled using the Freeman-Tukey arcsine methodology in STATA IC 13.1 with the metaprop function/plugin; heterogeneity was assessed with the I² statistic, and risk of bias was assessed with an adapted Newcastle-Ottawa Scale.

Limitations

  • The authors state that the number of eligible studies was small, showing a lack of research in this population, and that findings may not be generalizable to all pregnant and/or post-partum women in Africa.
  • The authors note that all included studies were observational, a design prone to selection and information biases.
  • The paper reports high heterogeneity (I² = 93.6%, p < 0.001), and the text contains an internal inconsistency in study counts: the abstract states seven studies on pregnant women and three on post-partum women, while the Results section states six and four, respectively.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.ijid.2017.08.015

Cites

64 of 64 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

13 of 33 cited sources checked · 2 supported · 0 flagged · accuracy not yet measured

  • Findingcitation

    Chereau et al. (2015) identified living in an individual house (OR 2.2, 95% CI 1.0-4.8) as an independent risk factor for ESBL-E colonization among Malagasy women.

    “Chereau et al. (2015) identified private indoor access to drinking water (odds ratio (OR) 3.8, 95% CI 1.2-11.6)and living in an individual house (OR 2.2, 95% CI 1.0-4.8)as independent risk factors for ESBL-E colonization among Malagasy women (after adjusting for”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Chereau et al. (2015) source

      Table 2 reports the stated multivariate odds ratio for living in an individual house among pregnant women in Madagascar (OR 2.2, 95% CI 1.0–4.8). But its P value is 0.06, above the paper’s 0.05 significance threshold, so calling it an independent risk factor overstates the statistical evidence. The paper also cautions that risk factors should be interpreted carefully because the study was cross-sectional. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
  • Premisecitation

    Several studies have confirmed the role of maternal colonization in the subsequent development of neonatal sepsis, particularly for group B Streptococcus but also for ESBL-E.

    “Several studies have confirmed the role of maternal colonization in the subsequent development of neonatal sepsis (particularly for group B Streptococcus, but also for ESBL-E) (Chan et al., 2013;Kaba et al., 2016;Denkel et al., 2014;Rettedal et al., 2015).”
    Quote in the paperNot a substantial claim2 of 3 sources checked
    • cites Chan et al., 2013 source

      The Results (Meta-analyses; page not specified) report higher odds of neonatal infection among newborns of mothers colonized with group B Streptococcus, supporting that part of the claim. The passages on other pathogens discuss E. coli colonization but do not identify ESBL-E or establish an association between maternal ESBL-E colonization and neonatal sepsis. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
    • cites Kaba et al., 2016 source

      The Results (section labeled “2 ∙ M.P. Nicol”; page not given) report ESBL-producing bacterial carriage in mothers and infants and clonally related isolates in one mother–infant pair. This supports a possible link in colonization, but the study of apparently healthy infants does not report neonatal sepsis or establish that maternal colonization led to it. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites Denkel et al., 2014 source
  • Interpretationcitation

    The molecular epidemiology of ESBL-E enzymes identified in the Madagascar, Nigeria, Cameroon, and Mozambique studies was in keeping with the global predominance of the CTX-M clone.

    “The molecular epidemiology of the ESBL-E enzymes identified in the Madagascar (Chereau et al., 2015), Nigeria (Fortini et al., 2015), Cameroon (Djuikoue et al., 2016b), and Mozambique (Sáez-lópez et al., 2016) studies was in keeping with the global predominance of the CTX-M clone, which is also widely reported in community-acquired UTI (Pitout et al., 2005;Peirano and Pitout, 2010;Pallecchi et al.”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Pitout et al., 2005 source
    • cites Peirano and Pitout, 2010 source
    • cites Pallecchi et al., 2004 source

      The Abstract (page unavailable) says CTX-M-type enzymes have been reported in clinical isolates from community-acquired infections, and the Discussion describes them as important emerging ESBLs worldwide. But the passage does not identify those infections as UTIs or establish that CTX-M is widely reported specifically in community-acquired UTI. The cited paper studied fecal isolates from healthy children, not UTI cases. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Findingcitation

    Drinking water supply from a spring or a well was not significantly associated with ESBL-E colonization/infection.

    “The following elements were not found to be significantly associated with ESBL-E colonization/infection in these three studies: being employed or being a housewife (Tito et al. 2017), drinking water supply from a spring or a well (Chereau et al., 2015), and hospitalization in the last 3 months (Djuikoue et al. 2016a,b).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Chereau et al., 2015 source
  • Findingcitation

    Bebell et al. (2017) identified low CD4+ count of <200/ml (OR 2.9, 95% CI 1.1-7.7, p=0.031) as an independent predictor of ESBL-E infection.

    “Bebell et al. ( 2017)) identified single marital status (OR 2.6, 95% CI 1.1-6.1,p = 0.026), low CD4+ count of <200/ml (OR 2.9, 95% CI 1.1-7.7,p = 0.031), and current UTI symptoms (OR 2.5, 95% CI 1.1-6.0,p = 0.03) as independent predictors of ESBL-E infection.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Bebell et al. (2017) source

      The Results (Enrollment and demographics, Table 1; page unavailable) compare CD4 categories between women with and without confirmed infection, not ESBL-E infection. The Methods (Data entry and statistical analysis; page unavailable) describe group comparisons, and the Results (Urinary tract infections; page unavailable) report ESBL prevalence. Searches for the stated odds ratio, confidence interval, p-value, and independent-predictor analysis found no passage reporting the claimed association. (LLM, conf=0.78)

      Experimental — accuracy not yet measured
  • Classified as probably not a substantial claim. 16
  • May combine two claims. 3

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The Freeman-Tukey arcsine methodology was applied to ensure proportionate weight distribution to studies presenting extreme prevalence.

    “To ensure proportionate weight distribution to studies presenting extreme prevalence (near 0 or 1), the Freeman-Tukey arcsine methodology was applied (Nyaga et al., 2014).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Nyaga et al., 2014 source

      The Results (Example two; page not provided) use the Freeman–Tukey transformation when some proportions are at or near 1, explaining that studies at 1 would otherwise be excluded and bias the pooled estimate. The Methods describe a weighted pooled estimate after transformation, but do not say the method ensures proportionate weight distribution to studies with extreme prevalence. (LLM, conf=0.84)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Interpretationcitation

    Because ESBL-E stool carriage persists for a variable length of time, the study population may have acquired ESBL-E during pregnancy that then persisted up to delivery and the post-partum period, reflecting community-acquired antimicrobial resistance genes rather than healthcare-associated acquisition.

    “Because ESBL-E stool carriage persists for a variable length of time (Ahmed et al., 2014), the study population may have acquired ESBL-E during pregnancy that then persisted up to delivery and the post-partum period, reflecting community-acquired antimicrobial resistance genes rather than healthcare-associated acquisition.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites Ahmed et al., 2014 source

      Split into 2 atoms — 1 confirmed, 0 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S4 (based).

    Findingnone given

    This appears to be the first systematic review and meta-analysis on ESBL-E colonization and/or infection focusing on pregnant and post-partum women in Africa.

    “This appears to be the first systematic review and meta-analysis on ESBL-E colonization and/or infection focusing on pregnant and post-partum women in Africa.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    Research on determinants of maternal colonization in Africa is scarce.

    “However, the scarcity of research on determinants of maternal colonization in Africa is worrisome.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductown data

    A random-effects meta-analysis was performed to summarize the proportions and 95% confidence intervals of ESBL-E in pregnant or post-partum women in Africa.

    “A random-effects meta-analysis was performed to summarize the proportions and the 95% confidence intervals (CI) of ESBL-E in pregnant or post-partum women in Africa.”
    Quote in the paperSubstantial claim
    • The authors state this as an assumption: Studies reporting on the magnitude of ESBL-E in pregnant and post-partum women used different laboratory methods, were conducted in different settings (hospital and community), or had other unknown factors influencing the magnitude of ESBL-E in pregnant and post-partum women in Africa.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    A comprehensive search of several electronic databases was performed, in addition to manual searches and attempts to contact authors of relevant studies to obtain specific details.

    “A comprehensive search of several electronic databases was performed, in addition to manual searches and attempts to contact authors of relevant studies to obtain specific details.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    This meta-analysis of observational studies is reported in compliance with the MOOSE statement and checklist.

    “This meta-analysis of observational studies is reported in compliance with the MOOSE statement and checklist (Stroup et al., 2000) (Meta-analysis of Observational Studies in Epidemiology).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Stroup et al., 2000 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The between-study heterogeneity was assessed using the I2 statistic.

    “The between-study heterogeneity was assessed using the I 2 statistic (which quantifies the percentage of variation across studies due to heterogeneity rather than to chance): I 2 <75% was considered as moderate heterogeneity (Higgins and Thompson, 2002) and >75% reflected high heterogeneity, in which case subset analyses were performed.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Higgins and Thompson, 2002 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductreasoning

    The authors made an effort to search the grey literature by using Google Scholar.

    “The authors made an effort to search the 'grey literature' by using Google Scholar, as many African publications are not listed in PubMed or Scopus.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The Newcastle-Ottawa Scale adapted for cross-sectional studies was used to assess the risk of bias for each selected study.

    “The Newcastle-Ottawa Scale (Herzog et al., 2013) adapted for cross-sectional studies (see below) was used to assess the risk of bias for each selected study.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Herzog et al., 2013

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Studies with a minimum score of 3 were considered of acceptable methodological quality for inclusion in the meta-analysis.

    “Studies with a minimum score of 3 were considered of acceptable methodological quality for inclusion in the meta-analysis (Table 2).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    The difference in ESBL-E proportions between pregnant and post-partum women may be explained by a greater probability of UTIs with ESBL-E during pregnancy than in the post-partum period.

    “This difference may be explained by a greater probability of UTIs with ESBL-E during pregnancy than in the post-partum period (Sáezlópez et al., 2016).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Sáezlópez et al., 2016

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Study design and conductnone given

    Each study was thoroughly assessed for risk of bias.

    “Each study was thoroughly assessed for risk of bias.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    Lack of trained healthcare workers and weak laboratory and infection control capacity may contribute to healthcare-associated transmission of ESBL-E to pregnant and post-partum women.

    “Another possible explanation is that the lack of trained healthcare workers (Kimang'a, 2012) and weak laboratory and infection control capacity (Petti et al., 2006) may contribute to healthcare-associated transmission of ESBL-E to pregnant and post-partum women.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Kimang'a, 2012
    • cites Petti et al., 2006 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Observational studies are prone to many biases, including selection and information biases.

    “The publications retrieved and included in the meta-analysis were all observational studies, a study type that is prone to many biases, including selection and information biases (Archer and Horn, 2006).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Archer and Horn, 2006

      Couldn’t be matched to a paper in Crossref, so it can’t be checked.

  • Probably not a substantial claim: may not pass S4 (based). May combine two claims.

    Interpretationnone given

    Maternal ESBL-E colonization/infection represents a risk for mother-to-child pathogen transmission with the potential for subsequent neonatal colonization and/or infection.

    “Maternal ESBL-E colonization/infection represents a risk for mother to child pathogen transmission with the potential for subsequent neonatal colonization and/or infection.”
    Quote in the paperNot a substantial claim
16 of 16

  • The authors state this as an assumption.

    Studies reporting on the magnitude of ESBL-E in pregnant and post-partum women used different laboratory methods, were conducted in different settings (hospital and community), or had other unknown factors influencing the magnitude of ESBL-E in pregnant and post-partum women in Africa.

    “The randomeffects model was chosen based on the anticipated assumption that studies reporting on the magnitude of ESBL-E in pregnant and post-partum women used different laboratory methods, were conducted in different settings (hospital and community), or had other unknown factors influencing the magnitude of ESBL-E in pregnant and post-partum women in Africa.”

  • The paper relies on this without support.

    The relationship between factors contributing to antimicrobial resistance in Africa and maternal colonization or infection with ESBL-E is unclear and requires investigation.

    “The relationship between these factors and maternal colonization or infection with ESBL-E is unclear and requires investigation.”
2 of 2

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Conflicting counts of pregnant and post-partum studies

    Minor

    The abstract assigns seven studies to pregnant women and three to post-partum women, while the Results section assigns six and four, respectively.

  • Infection confidence-interval lower bound differs from Figure 4

    Minor

    The text gives 0.01 as the lower bound for the pooled infection estimate, but Figure 4 gives -0.01.

  • Colonization confidence-interval lower bound differs from Figure 4

    Minor

    The text gives 0.01 as the lower bound for the pooled colonization estimate, but Figure 4 gives 0.10.

3 of 3

Cites

Flagged first, then by citations

Research works printed but not linked: 4

  1. Aljabri, 2010, Original article, Ann Saudi Med, 30, 10
  2. Archer, 2006, Perspectives in practice publishing nutrition research: a review of 2006, J Am Diet Assoc, 4, 89
  3. Frieden, 2013, Antibiotic resistance threats, CDC, 22
  4. Lincetto, 2006, Antenatal care, Lancet, 51

Cited by

Sorted by citations

Related

Authors
Bulabula, A. N. H., Dramowski, A., & Mehtar, S.
Affiliations
Stellenbosch University (ZA)
Corresponding author
Bulabula, Andre N.H.
ORCID
Venue
International Journal of Infectious Diseases
Publisher
Elsevier BV
Published
2017-11
Volume
64
Pages
58-66
ISSN
1201-9712 (ISSN-L)
DOI
10.1016/j.ijid.2017.08.015
OpenAlex
W2751088626
Semantic Scholar
5afb9650df73b038019bfb8b54a85210149cab6b
Cited by
59
References
64
Citations by year
2026: 5 · 2025: 8 · 2024: 8 · 2023: 8 · 2022: 8 · 2021: 9 · 2020: 3 · 2019: 9 · 2018: 1
FWCI
0.42
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Infectious Diseases (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • SUNScholar (Stellenbosch University) (submittedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Health Sciences › Medicine › Epidemiology › Urinary Tract Infections Management
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
Keywords
extended-spectrum beta-lactamase, ESBL-producing Enterobacteriaceae, maternal colonization, maternal infection, pregnancy, postpartum women, prevalence, risk factors, CTX-M, community-acquired infections, neonatal colonization, antimicrobial resistance, Africa
MeSH terms
Africa, beta-Lactamases, Cefotaxime, Enterobacteriaceae, Enterobacteriaceae Infections, Female, Humans, Pregnancy, Pregnancy Complications, Infectious, Risk Factors, Prevalence, Postpartum Period

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