Abstract
The Coronavirus Disease 2019 (COVID-19) pandemic disrupted maternity care, highlighting the need for rapid, high-quality clinical practice guidelines (CPGs) to ensure safe care for pregnant women. We assessed the quality and recommendations of CPGs related to COVID-19 in pregnancy. Following prospective registration (PROSPERO number: CRD42022346031) we searched Medline, Web of Science, and UpToDate from inception until July 2024. The methodological quality was appraised using the Appraisal of Guidelines for Research and Evaluation II (AGREE II). A total of 27 CPGs were included. High scores were achieved in scope and purpose (21/27, 78%) and clarity (17/27, 63%). The most poorly addressed domains were rigour of development and applicability to clinical practice (18/27, 67% and 19/27, 70% scored low quality, respectively). Overall, only four (15%) guidelines were recommended. Most CPGs (25/27, 93%) addressed COVID-19 screening and transmission prevention, but few covered psychological care (3/27, 11%) or maternal delivery preferences (4/21, 19%). Consensus was found on timing and mode of delivery (16/17, 94%), but there was disagreement on delayed cord clamping and virus transmission interventions. Evidence-based practice requires health care providers, patients and stakeholders to be aware of variations in both the quality and recommendations of CPGs, especially during times of uncertainty.
Introduction
The recent Coronavirus Disease 2019 (COVID-19) global pandemic caused major disruptions in health care service worldwide leading to increased morbidity with a rise in both direct and indirect mortality [1, 2], resulting in decreased access to and delivery of care [3, 4], and adversely affecting perinatal care and pregnancy outcomes [5–7]. Offering effective and safe maternity care requires consistent, safe access to health services, a very difficult task to maintain during the pandemic, particularly in situations where resources are scarce [4, 8–11].
Facing this worldwide health challenge, rapid synthesis of evidence and development of clinic guideline is an essential step to re-adjust health care services and adopt new care pathways in response to this new challenge. As such, clinical practice guidelines (CPGs) need to be produced rapidly to a high quality and standard that meet the local population needs. While a lengthy and laborious process, producing quality guidelines is now more streamlined using internationally agreed upon standards [12].
Still, maintaining good quality of standards, inclusivity and relevance may be hard when faced with rapid production of guideline in times of crisis. This is especially relevant to pregnant women (PW) as a special vulnerable group where evidence sought from the general population may not be directly applicable in pregnancy.
This review aims to investigate CPGs on the management of COVID-19 in pregnancy during the pandemic to assess their quality using a validated tool (AGREE II) and highlight differences and variations in practice worldwide.
Methods
We undertook a systematic review of published guidance for the delivery of health care services and clinical management of women with COVID-19 infection, produced during the pandemic (PROSPERO number: CRD42022346031). We reported our findings in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [13].
We defined guidance as any set of systematically developed criteria with recommendations on the care or nonpharmacological treatment of women with confirmed or suspected COVID-19. For inclusion in our review, guidance had to make specific recommendations on the management of COVID-19 in pregnancy and delivery, for example, provision of fluids, oxygen therapy and management of labour. We did not include guidance which only reported on infection prevention or the diagnosis of COVID-19, pharmacological treatment of COVID-19, pregnancies with specific conditions such as chronic diseases, pre-eclampsia, eclampsia, gestational diabetes, hypothyroidism, hypertension, among others.
We included guidance produced from international and national scientific and health care organizations but excluded local and regional guidance. We included the latest version of any guidance until July 2024, to better reflect the level of evidence given the rapid progress in this field.
Literature search and selection
We searched the electronic databases Medline/PubMed and Web of Science, and UpToDate, from inception until July 2024. We combined the following MeSH terms using the Boolean operators to screen for relevant studies: (‘COVID’, ‘Corona Virus’, ‘SARS-CoV-2’, ‘clinical management’, ‘guidance’, ‘guideline’, ‘decision tool’, ‘consensus statement’, ‘position statement’, ‘protocol’, ‘obstetrics’, ‘pregnancy’, ‘women’ and ‘woman’), outlined in Supplementary Material S1.
All references were exported to Endnote X9 (Clarivate Analytics), and duplicates were removed using the ‘find duplicates’ software tool and by manual checking. Three independent reviewers (C.A.P., L.G.V., M.G.V.) completed the study selection and inclusion process in two stages. Titles of identified studies were screened to identify relevant citations, following which the full text was reviewed of those which met out search criteria.
Data extraction
Data were extracted in duplicate (C.A.P., L.G.V.) using an electronic data collection tool (Excel spreadsheet) including country, issuing health authority, named authors, year of publication, peer review, methodology for establishing consensus among authors, inclusion/exclusion criteria, evidence synthesis, disease domains addressed, intended population, recommendations, grading system used for each recommendation, implementation tools provided and number of recommendations.
Three authors (C.A.P., L.G.V., M.G.V.) mapped out each recommendation in the guidelines and classified accordingly into three categories depending on whether they were regarding care of PW, recommendations to the health care providers (HCPs) or surveillance measures. Disagreements in all stages were resolved with a third reviewer (B.W.).
Assessment of risk of bias
Quality of identified studies was assessed using the AGREE II instrument [12]. The AGREE II is a validated tool providing a framework to assess the quality of clinical guidance reporting on six domains that were assessed through 23 individual items and scored independently by three assessors (C.A.P., L.G.V., M.G.V.). Domain scores were calculated by summing up all the scores of each item in a domain and by scaling the total as a percentage of the maximum possible score for that domain [12]. We considered all domain scores and created a threshold across all six domain scores as suggested in AGREE II user’s manual guidance. Those domains with scores from 100% to 70% were categorized as high-quality; 70%–40%, medium quality; and below 40%, low quality [14].
Once completing the 23 items, two overall assessments of each guideline were provided. First, an overall score of each guideline, considering the criteria used in the assessment process. Second, a decision about whether a guideline would be recommended, with or without modifications, or not recommended was based on the overall quality of the CPG. Thus, those CPGs scoring under 40%, in the overall quality score, were not recommended; 40%–70% were recommended with modifications and those scoring above 70% were recommended.
Statistical analysis
Descriptive data, such as characteristics of included CPGs, domains covered in the recommendations and quality domain scores, were reported as normal frequencies, and number of recommendations as median and interquartile range. The statistical analysis was performed using the software IBM SPSS Statistics for Windows version 28 (IBM Corp., Armonk, NY, USA).
Ethics approval
This study is not based upon clinical study or patient data.
Results
The completed search yielded 625 records that were transferred to Endnote, duplicates removed and 589 titles were screened for eligibility based on their title and abstract. A total of six multinational [15–20] and 21 national [21–41] guidelines met the inclusion criteria and were included in the systematic review (n = 27) (Fig. 1).
Figure 1.
Flow of included guidelines for the systematic review on the quality of evidence-based clinical guidelines on the COVID-19 management in pregnancy from Page et al. [42].
Characteristics of the guidelines are presented in Table 1. Only five CPGs were reported as formally peer-reviewed (6/27, 22%) [18, 20, 25, 26, 29, 33]. Whatever the methodology used to establish consensus, it was not recorded in 21 CPGs (Table 1). Only four CPGs detailed the search strategy (4/27, 15%) and reported a clear evidence grading system when making recommendations, using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) [20, 29, 33] and the Scottish Intercollegiate Guidelines Network Grading System (SIGN) [28]. Implementation tools for evidence into clinical practice were provided by 18 CPGs (Table 1).
Table 1.
Characteristics of included clinical practice guideline on the COVID-19 management in pregnancy
| Issuing health authority | Publication year | Country | Peer reviewed | Consensus methodology | Search strategy | Inclusion/exclusion criteria | Evidence grading system | Tools implemented | Number of recommendations |
|---|---|---|---|---|---|---|---|---|---|
| FIGO [15] | 2021 | Multinational | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Not mentioned | No | 3 |
| FIGO [16] | 2020 | Multinational | Not mentioned | Not mentioned | Not fully described | Not mentioned | Not mentioned | Yes | 19 |
| ICM [17] | 2020 | Multinational | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Not mentioned | No | 7 |
| WAPM [18] | 2020 | Multinational | Yes | Not mentioned (peer review literature and expert opinion) | Joint database from perinatal centers around the world | Not mentioned | Not mentioned | No | 7 |
| ISIDOG [19] | 2020 | Multinational | Not mentioned | Not mentioned | Based on an extensive literature review (strategy not detailed) | Published/in-press peer reviewed and on the CDC, RCOG, ANZICS guidelines. | Not mentioned | Yes | 25 |
| WHO [20] | 2023 | Multinational | Yes | Not mentioned (peer review literature) | Fully described | Fully described | GRADE | Yes | 9 |
| SMFM, SOAP [21] | 2020 | USA | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Not mentioned | No | 10 |
| SMFM [22] | 2021 | USA | Not mentioned | Not mentioned | Not mentioned | Examples of current practices from some centers that have seen a relatively higher volume of cases | Not mentioned | Yes | >30 |
| NIH [23] | 2024 | USA | Not mentioned | Expert Panel (peer review literature and expert opinion) | Not mentioned | Not mentioned | A, B, C: Indicating the strengh of the recommendation; I, IIa, IIb, III: Indicating the quality of the evidence | No | 8 |
| UTHealth [24] | 2020 | USA | Not mentioned | Not mentioned (expert opinion) | Input from experts across the country and a review of current literature (strategy not detailed) | Not mentioned | Not mentioned | Yes | 13 |
| Peer-reviewed Journal [25] | 2020 | USA | Yes | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Yes | 13 |
| Peer-reviewed Journal [26] | 2020 | USA, Italy | Yes | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Yes | >18 |
| SG [27] | 2021 | UK | Not mentioned | Not mentioned (expert opinion) | Not mentioned | Pregnant women with respiratory symptoms, pregnant women in critical care during the pandemic | Not mentioned | Yes | 6 |
| RCOG [28] | 2022 | UK | Not formally peer-reviewed | Committee consensus opinion | RCOG Library team: ‘pregnancy’, ‘coronavirus’, ‘SARS’, ‘severe acute respiratory syndrome’, ‘infant’, ‘new-born’ ‘breastfeeding’. Also ‘grey’ literature and non-peer reviewed content. | Pregnant women recently given birth, partners, neonates and studies of other populations. | SIGN grading system | Yes | >42 |
| National COVID-19 Clinical Evidence Taskforce [29] | 2023 | Australia | Yes | Not mentioned, but they mentioned consensus | Detailed in Supplementary Table S1 (technical report and search methods documents). They used alerts in PubMed | Primary research articles or systematic reviews relevant to the PICO question and undertaken in patients with a diagnosis or clinical suspicion of COVID-19. | GRADE | No | 7 |
| SOGC [30] | 2021 | Canada | Not mentioned | Committee consensus opinion | Not mentioned | Not mentioned | Not mentioned | No | >18 |
| MoHFW [31] | 2021 | India | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Yes | >36 |
| FOGSI [32] | 2020 | India | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Yes | 12 |
| FOGSI, NNF, IAP [33] | 2022 | India | Yes | Not mentioned | PubMed, international and national organizations websites. The Cochrane Gynaecology and Fertility group. Guidelines published by Pediatric and Obstetric Societies and bibliographies of relevant articles. Search updated till 20 May 2021 | Search strategy and data bases used are mentioned | GRADE | Yes | 7 |
| ICMR, NIRRH [34] | 2020 | India | Not mentioned | Not mentioned | International agencies like CDC, ACOG, RCOG, FOGSI and Lancet publications. | Not mentioned | Not mentioned | Yes | 43 |
| Journal [35] | 2020 | Singapore | Not mentioned | Committee consensus opinion | Not mentioned | Not mentioned | Not mentioned | Yes | 14 |
| Journal [36] | 2020 | Singapore | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Not mentioned | Yes | 11 |
| FEBRASGO [37] | 2020 | Brazil | Not mentioned | Not mentioned (expert opinion) | Not mentioned | Not mentioned | Not mentioned | No | 15 |
| CNGOF [38] | 2020 | France | Not mentioned | Not mentioned (expert opinions and national recommendations of the General direction of Public Health in France) | Not mentioned | Not mentioned | Not mentioned | Yes | 8 |
| HAS [39] | 2020 | France | Not mentioned | Panel discussion | French and International scientific societies, WHO guidelines, recommendations from international health agencies (NICE, INESS). | Not mentioned | Not mentioned | No | 10 |
| COGA [40] | 2020 | China | Not mentioned | Committee consensus opinion | N/A | Not mentioned | Not mentioned | Yes | 2 |
| COCG [41] | 2020 | Spain | Not mentioned | Not mentioned | Based on scientific evidence and international recommendations (Strategy not detailed) | Not mentioned | Not mentioned | Yes | 21 |
ACOG, American College of Obstetricians and Gynecologists; ANZICS, Australian and New Zealand Intensive Care Society; CDC, Centers for Disease Control and Prevention; CNGOF, French Societies of gynaecology-obstetrics, infectious diseases and neonatalogy; COGA, Chinese Obstetricians and Gynecologists Association; COCG, COVID Collaborative Group. Barcelona. Centre for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu); CMS, Centers for Medicare & Medicaid Services; FIGO, International Federation of Gynecology and Obstetrics; FOGSI, Federation of Obstetrics and Gyneacological Societies of India; HAS, The French National Authority for Health; IAP, Indian Academy of Pediatrics; ICM, International Confederation of Midwives; ICMR, Indian Council of Medical Research; ISIDOG, International Society for Infectious Diseases in Obstetrics and Gynaecology; MoHFW, Ministry of Health and Family Welfare; NIH, National Institutes of Health; NIRRH, National Institute for Research in Reproductive Health; NNF, National Neonatology Forum of India; RCOG, Royal College of Obstetrics and Gynaecology; SG, Scottish Government; SMFM, Society for Maternal-Fetal Medicine; SOAP, Society for Obstetric Anesthesia and Perinatology; UTHealth, University of Texas Health Science Center at Houston (Department of Obstetrics, Gynecology, and Reproductive Sciences); WAPM, World Association of Perinatal Medicine; N/A, Not applied.
The median number of recommendations made per guideline that met the inclusion criteria was 12 (interquartile range 12).
AGREE II scores
The quality domain scores are presented in Fig. 2, and the two global rating items are in Table 2. Most of the guidelines offered a high-quality score in the scope and purpose domain (21/27, 78%) as well as in the clarity and presentation domain (17/27, 63%). Rigour of development and applicability to clinical practice were the most poorly addressed domains (18/27, 67%; 19/27, 70%, respectively). Only three guidelines scored high in applicability (3/27, 11%) [20, 29, 33] (Fig. 2).
Figure 2.
Quality of included CPGs on the management of COVID-19 in pregnancy and labour using AGREE II [12]. CPGs were evaluated thorough 23 items grouped into six domains. Each item is scored according to the AGREE II user’s manual guidance and criteria suggested for each item. Each domain score is obtained by summing up all the items in that domain and by scaling the total as a percentage of the maximum possible score for that domain. We considered domain scores under 40% to indicate low quality; 40%–70% medium quality and 70%–100% high quality of guideline development [14].
Table 2.
Summary of the domains identified in the recommendations in COVID-19 clinical practice guidelines and overall assessment with AGREE II tool
| Guideline | Pregnancy management | Labour management | Health care providers recommendations | Surveillance measures | Overall quality score (%) | Recommended guideline |
|---|---|---|---|---|---|---|
| FIGO [15] | ✓ | X | X | ✓ | 42.03 | Recommended with modifications |
| FIGO [16] | ✓ | ✓ | ✓ | ✓ | 48.55 | Recommended with modifications |
| ICM [17] | ✓ | ✓ | X | ✓ | 20.29 | Not recommended |
| WAPM [18] | X | ✓ | ✓ | ✓ | 60.14 | Recommended with modifications |
| ISIDOG [19] | ✓ | ✓ | ✓ | ✓ | 65.94 | Recommended with modifications |
| WHO [20] | X | ✓ | X | ✓ | 89.96 | Recommended |
| SMFM, SOAP [21] | X | X | ✓ | ✓ | 29.71 | Not recommended |
| SMFM [22] | ✓ | ✓ | X | ✓ | 56.52 | Recommended with modifications |
| NIH [23] | ✓ | ✓ | ✓ | ✓ | 57.97 | Recommended with modifications |
| UTHealth [24] | ✓ | ✓ | ✓ | ✓ | 44.20 | Recommended with modifications |
| Peer-reviewed Journal [25] | ✓ | ✓ | ✓ | ✓ | 31.88 | Recommended with modifications |
| Peer-reviewed Journal [26] | ✓ | ✓ | ✓ | ✓ | 55.07 | Recommended with modifications |
| SG [27] | ✓ | X | X | ✓ | 42.03 | Recommended with modifications |
| RCOG [28] | ✓ | ✓ | ✓ | ✓ | 73.91 | Recommended |
| National COVID-19 Clinical Evidence Taskforce [29] | X | ✓ | X | ✓ | 96.38 | Recommended |
| SOGC [30] | ✓ | ✓ | ✓ | ✓ | 50.72 | Recommended with modifications |
| MoHFW [31] | ✓ | ✓ | X | ✓ | 25.36 | Not recommended |
| FOGSI [32] | ✓ | ✓ | ✓ | ✓ | 56.52 | Recommended with modifications |
| FOGSI, NNF, IAP [33] | ✓ | ✓ | X | ✓ | 77.54 | Recommended |
| ICMR, NIRRH [34] | ✓ | ✓ | ✓ | ✓ | 20.29 | Not recommended |
| Journal [35] | X | ✓ | ✓ | ✓ | 50.72 | Recommended with modifications |
| Journal [36] | X | ✓ | ✓ | ✓ | 31.16 | Recommended with modifications |
| FEBRASGO [37] | ✓ | ✓ | ✓ | ✓ | 28.26 | Not recommended |
| CNGOF [38] | X | X | ✓ | ✓ | 38.41 | Recommended with modifications |
| HAS [39] | X | X | X | ✓ | 63.04 | Recommended with modifications |
| COGA [40] | X | X | ✓ | ✓ | 50.00 | Recommended with modifications |
| COCG [41] | ✓ | ✓ | ✓ | ✓ | 53.62 | Recommended with modifications |
✓, Covered; X, Not covered.
ACOG, American College of Obstetricians and Gynecologists; ANZICS, Australian and New Zealand Intensive Care Society; CDC, Centers for Disease Control and Prevention; CNGOF, French Societies of gynecology-obstetrics, infectious diseases and neonatalogy; COGA, Chinese Obstetricians and Gynecologists Association; COCG, COVID Collaborative Group. Barcelona. Centre for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu); CMS, Centers for Medicare & Medicaid Services; FIGO, International Federation of Gynecology and Obstetrics; FOGSI, Federation of Obstetrics and Gyneacological Societies of India; HAS, The French National Authority for Health; IAP, Indian Academy of Pediatrics; ICM, International Confederation of Midwives; ICMR, Indian Council of Medical Research; ISIDOG, International Society for Infectious Diseases in Obstetrics and Gynaecology; MoHFW, Ministry of Health and Family Welfare; NIH, National Institutes of Health; NIRRH, National Institute for Research in Reproductive Health; NNF, National Neonatology Forum of India; RCOG, Royal College of Obstetrics and Gynaecology; SG, Scottish Government; SMFM, Society for Maternal-Fetal Medicine; SOAP, Society for Obstetric Anesthesia and Perinatology; UTHealth, University of Texas Health Science Center at Houston (Department of Obstetrics, Gynecology, and Reproductive Sciences); WAPM, World Association of Perinatal Medicine.
The domain scores of each guideline are outlined in Supplementary Table S2. Only four CPGs scored above 70% in the overall quality score (4/27, 15%) and were recommended [20, 28, 29, 33] (Table 2).
Summary of recommendations
Specific recommendations identified in each of the included guidelines are detailed in Supplementary Table S3. All guidelines appraised covered issues regarding surveillance measures (27/27, 100%), most of CPGs focused on labour management (21/27, 78%), 18 CPGs on pregnancy management and 18 CPGs on recommendations to the HCPs (18/27, 67%) (Table 2).
Recommendations to pregnant women
Home isolation [31] and self-monitoring of temperature, heart rate and oxygen saturation assessment [19, 22, 31], rest and adequate hydration [41] are recommended for infected PW. Instructions to monitor foetal movements are also advised [19, 30]. Recommendation to seek medical assistance promptly once they develop symptoms was found in eight CPGs [15, 16, 19, 20, 22, 27, 30, 41]. Only two guidelines addressed the need for monitorization of the patient’s psychological and emotional state [20, 32, 39] and the violence risk [32, 39]. For the follow-up visits, some guidelines encouraged the use of telemedicine [21, 22, 30–32, 35, 39, 41] depending on the obstetric risks and circumstances.
Recommendations to health care providers
Infection control measures are advisable for those caregivers in contact with infected PW [16, 18, 19, 21, 24–26, 28, 30, 32, 34–37, 41]. One guideline recommended chemoprophylaxis for HCPs with known contact of COVID-19-positive patients [32].
Surveillance measures
Antenatal management
There was consensus in the management of PW with mild COVID-19 and no comorbidities at home [18–20, 30, 33, 38, 41]. Symptomatic COVID-19-infected PW should be given oxygen therapy [19, 22, 25, 27, 28, 31, 34, 37, 41]. Fluid restriction with a fluid balance close to zero [19] and the use of intravenous fluids conservatively unless cardiovascular instability [25] has been also recommended.
Mode and timing of delivery
Mode and timing of delivery should be individualized depending on the clinical status of the patient, gestational age and foetal condition [16, 18–20, 22, 24–26, 31, 34, 37, 41]. Only four from 21 CPGs, considering delivery, included maternal wishes and preferences as a factor to consider in relation to delivery decisions [17, 20, 25, 28].
Negative pressure isolation rooms
Delivery, including caesarean delivery for positive PW [16, 18, 35, 40] or hospitalization [16, 25, 28, 41], should be carried out in negative pressure isolation rooms. However, one guideline stated that this measure is not required [26].
Birthing pools
Birth in water is not recommended to reduce transmission to the baby [17, 28, 37] and needs to be revised to limit the potential spread of infection [36].
Delayed umbilical cord clamping
There was disagreement between guidelines as to whether to offer delayed cord clamping. Four guidelines suggested that delayed cord clamping should be avoided until more information is available regarding COVID-19 vertical transmission [24, 35, 36, 41]. Others suggested that delayed cord clamping should be offered in line with usual practice [20, 28–30, 37], and recommended since early clamping does not decrease the risk of vertical transmission [31].
Policies on visitors and support persons
There was a consensus about the number of visitors for PW in hospital to be reduced [16, 17, 21, 25, 26, 28, 31, 32, 34, 41]. There was also consensus regarding limiting the frequency and duration of room visits by the caregivers and visitors [24, 28, 31, 34] and the number of staff at delivery [19]. One guideline advised that no companion person should be allowed at PW’s check-up appointments [38].
Discussion
Summary of findings
Those guidelines that scored higher in the AGREE II overall assessment were produced more recently. This suggests that the speed in the development of the guidelines works against quality, even though we have considered their updates. Most of the CPGs had methodological weaknesses. Globally, declarations of interest were poorly documented, and this is paramount when evidence is lacking. Some practices in the management of labour, such as delayed cord clamping, were controversial, and others differed from practices before the pandemic due to the implementation of interventions for virus transmission control.
What is already known on this subject
PW, especially during the third trimester, are more vulnerable to adverse effects produced by COVID-19 [6, 43, 44]. In response to this heightened risk, 72 CPGs have been developed and updated during the pandemic, to provide insight and guidance on the management of pregnancy, labour and postpartum in different settings. However, many of these guidelines on maternal COVID-19 management emerged rapidly during the pandemic, often lacking the necessary rigour. The availability of quality, evidence-based guidelines is of utmost importance for providing clinicians, health care services, and policymakers with the best choices when delivering medical care and formulating health policies, especially during periods of uncertainty, such as the COVID-19 pandemic, when scientific evidence may be scarce in some respects. The lack of consensus between guidelines can create confusion among guideline users, which is concerning. In the past, recommendations were commonly based on clinical judgments and experience, making them more likely to be biased and more susceptible to self-interest in decision-making. A scoping review of the impact of the COVID-19 pandemic on maternal and perinatal health emphasizes the lack of consistency in guidelines for labour, delivery and breastfeeding for COVID-19-positive women, leading to confusion and potentially unnecessary harm [7].
In response to emerging and ongoing epidemic threats, a recent study protocol was published with the aim of developing a core set of outcomes for maternal and perinatal health research and surveillance [45].
What this study adds
This systematic review contributes to the existing body of knowledge by appraising the quality of available and updated CPGs on COVID-19 management during pregnancy and delivery, generated because of the emergency pandemic response, using a validated instrument (AGREE II) and summarizes recommendations across guidelines worldwide, highlighting disagreements and consensus in their practice.
Notably, eight of the evaluated guidelines acknowledge that their recommendations were solely based on expert opinion [18, 24, 27, 28, 30, 37, 38, 40], allowing readers to make their own judgment in regard to the validity of the given recommendations when making decisions, signalling the need for more rigorous evidence-based approaches. One specific inconsistency involves early cord clamping; a systematic review and meta-analysis revealed that many neonates born to SARS-CoV-2-positive mothers had their umbilical cords clamped early, often due to concerns about virus transmission from mother to child, even though most guidelines recommended delayed clamping [46]. Importantly, the timing of cord clamping was found to have no effect on mother-to-neonate transmission of SARS-CoV-2 [46, 47], raising concerns, particularly in low-resources settings where delayed clamping may provide significant benefits [8]. Evidence regarding virus transmission in specific scenarios, such as water births, also remains limited [28], indicating the need for guidelines to include sections on future research areas [48].
Developing high-quality guidelines requires adequate human and financial resources, both of which are often scarce during crisis. Guideline developers must consider the cost effectiveness and utility of recommendations, as this is crucial for resource allocation in times of limited health resources. Some CPGs effectively accounted for local resource availability and maximized the use of telehealth to address these constraints [22, 31, 32, 34, 35].
The scarcity of resources during crisis directly impacts the quality of guidelines [49]. Developers must consider these constraints and work to ensure that guidelines remain practical and applicable under varying conditions. The domains of rigour of development and applicability to clinical practice were the most insufficiently addressed, consistent with findings from a rapid review that aimed to assess the availability, quality and inclusivity of clinical guidelines produced in the early stage of the COVID-19 pandemic [50]. This review also highlighted poor overall quality, particularly in stakeholder involvement, applicability and editorial independence [50]. Similarly, a recent study that assessed health systems guidance from the World Health Organization (WHO), European Centre for Disease Prevention and Control (ECDC) and Centers for Disease Control and Prevention for the H1N1 Influenza A virus and COVID-19 pandemics, using the Appraisal of Guidelines Research & Evaluation-Health Systems (AGREE-HS) tool, also pointed to incomplete reporting in key areas such as methodology, participant involvement, conflicts of interest and implementability [51]. These deficiencies in guideline development and applicability may have significant implications for maternal and perinatal health outcomes. Guidelines that lack a rigorous development process, including systematic evidence synthesis, consideration of health benefits, side effects and risks, may lead to inconsistent or suboptimal recommendations. For example, one harmful effect on the neonate is the recommendation in some guidelines of early umbilical cord clamping, as previously mentioned. Likewise, limited consideration of applicability could hinder the effective implementation of these guidelines in clinical settings, reducing their impact on patient care. These shortcomings may contribute to variability in clinical practice, potentially affecting the quality of care provided to PW with COVID-19.
Furthermore, guidelines should undergo external review to ensure validity, clarity, applicability, and usefulness in clinical practice. However, most of the reviewed guidelines did not mention this process.
The concept of ‘living guidelines’ is essential for keeping recommendations up to date by continuously integrating the latest evidence, and it has been demonstrated that this approach is feasible even during crisis like the COVID-19 pandemic [52]. Living guidelines help ensure that health care practices remain up-to-date, enhancing patient care and improving outcomes. This study included three living guidelines [20, 28, 29].
Strengths and limitations
To our knowledge, this is the first systematic review to appraise the quality of the available evidence-based CPGs on the management of COVID-19 in PW using the AGREE II tool [12]. We reviewed 27 guidelines from different organizations and agencies around the world that meet the inclusion criteria. We closely monitored and checked for updates to guidelines and were able to identify topics of disagreement and uncertainty.
We encountered limitations in our study. The exclusion of local or regional guidelines may affect the global representativeness of our findings, particularly from low- and middle-income countries. This could introduce publication bias, as some guidelines may not be widely disseminated or indexed. Future research should consider including a broader range of guidelines to enhance comprehensiveness. Additionally, despite the existence of validated systems for making recommendations, such as GRADE [53], most of the guidelines identified were produced without a formal guideline development process, lacking evidence synthesis, due to its rapid production. This limitation makes it difficult to compare recommendations across guidelines. Furthermore, our study focused on assessing the quality of the guidelines rather than evaluating their impact on clinical practice or maternal and perinatal outcomes, which limits the conclusions that can be drawn about their real-world effectiveness. Another limitation of our review is the fact that the AGREE II tool does not supply a threshold for distinguishing between high- and low-quality CPGs. Instead, appraisers must establish a threshold by prior consensus before the assessment, as we did previously [14]. Therefore, scores of an AGREE II evaluation must be interpreted cautiously and restricted to a specific situation.
Conclusion
Current CPGs on the management of COVID-19 in pregnancy have been rapidly produced and vary in their quality, developed methodology and recommendations. Our review identified 27 guidelines from 24 organizations and agencies related to antenatal and intrapartum care of women with COVID-19. Rigour of development and applicability were the worst-rated domains. Only four guidelines were identified as high quality according to the AGREE II overall assessment and thus recommended. This review provides an overview of the quality of the available CPGs worldwide from the onset of the pandemic and summarizes and compares recommendations across guidelines identified to help guide HCPs and health services as well as guideline developers.
Supplementary Material
Contributor Information
Luz García-Valdés, Department of Preventive Medicine and Public Health, University of Granada, Granada, Spain.
Bassel H Al Wattar, Beginnings Assisted Conception Unit, Epsom and St Helier University Hospitals, London, United Kingdom; Clinical Trials Unit, Anglia Ruskin University, Chelmsford, United Kingdom.
Mar García-Valdés, Servicio de Farmacia Hospitalaria, Hospital Virgen de las Nieves, Granada, Spain.
Carmen Amezcua-Prieto, Department of Preventive Medicine and Public Health, University of Granada, Granada, Spain; Consortium for Biomedical Research in Epidemiology and Public Health (CIBERESP), Madrid, Spain; Instituto de Investigación Biosanitaria (ibs.Granada), Granada, Spain.
Supplementary data
Supplementary data are available at EURPUB online.
Conflict of interest: None declared.
Funding
The authors did not receive funding to carry out this research.
Data availability
The data underlying this article are available in the article and in its online supplementary material.
Key points.
Rapidly developed clinical guidelines often lack methodological rigour, leading to variability in recommendations, which can affect the consistency of care during health emergencies.
Implementing standardized, evidence-based processes in guideline development is essential for enhancing their reliability and supporting public health responses in future crises.
Addressing the psychological and emotional well-being of vulnerable populations, such as pregnant women, is a critical gap that must be prioritized in public health strategies.
High-quality guidelines are crucial not only for guiding health care providers but also for shaping effective public health policies and improving outcomes in times of crisis.
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Data Availability Statement
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Key points.
Rapidly developed clinical guidelines often lack methodological rigour, leading to variability in recommendations, which can affect the consistency of care during health emergencies.
Implementing standardized, evidence-based processes in guideline development is essential for enhancing their reliability and supporting public health responses in future crises.
Addressing the psychological and emotional well-being of vulnerable populations, such as pregnant women, is a critical gap that must be prioritized in public health strategies.
High-quality guidelines are crucial not only for guiding health care providers but also for shaping effective public health policies and improving outcomes in times of crisis.