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Colorectal
Original research
Standards for the provision of antenatal care for patients with inflammatory bowel disease: guidance endorsed by the British Society of Gastroenterology and the British Maternal and Fetal Medicine Society
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  1. Christian Selinger1,
  2. Nicola Carey1,
  3. Shelley Cassere2,
  4. Catherine Nelson-Piercy3,
  5. Aileen Fraser4,
  6. Veronica Hall5,
  7. Kate Harding6,
  8. Jimmy Limdi7,8,
  9. Lyn Smith9,
  10. Marie Smith10,
  11. Melanie Catherine Gunn11,
  12. Aarthi Mohan12,
  13. Khasia Mulgabal13,
  14. Alexandra Kent14,
  15. Klaartje Bel Kok15,
  16. Tracey Glanville2
  1. 1 Leeds Gastroenterology Institute, Leeds Teaching Hospitals NHS Trust, Leeds, UK
  2. 2 Obstetrics, Leeds Teaching Hospitals NHS Trust, Leeds, UK
  3. 3 Obstetric Medicine, Guy’s and Saint Thomas’ Hospitals NHS Trust, London, UK
  4. 4 Gastroenterology, United Hospitals Bristol, Bristol, UK
  5. 5 Gastroenterology, Royal Bolton Foundation NHS Trust, Bolton, UK
  6. 6 Obstetrics, Guy’s and Saint Thomas’ Hospitals NHS Trust, London, UK
  7. 7 Section of IBD—Division of Gastroenterology, The Pennine Acute Hospitals NHS Trust, Manchester, UK
  8. 8 Gastroenterology, Manchester Academic Health Science Centre, Manchester, UK
  9. 9 Gastroenterology, NHS Greater Glasgow and Clyde North Glasgow University Hospitals Division, Glasgow, UK
  10. 10 Obstetrics, Newcastle Upon Tyne Hospitals NHS Foundation Trust, Newcastle Upon Tyne, UK
  11. 11 Gastroenterology, Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle upon Tyne, UK
  12. 12 Obstetrics, United Hospitals Bristol, Bristol, UK
  13. 13 Obstetrics, Royal Bolton Foundation NHS Trust, Bolton, UK
  14. 14 Gastroenterology, King’s College Hospital NHS Foundation Trust, London, UK
  15. 15 Gastroenterology, Barts and The London NHS Trust, London, UK
  1. Correspondence to Dr Christian Selinger, Leeds Gastroenterology Institute, Leeds Teaching Hospitals NHS Trust, Leeds LS9 7TF, UK; christian.selinger{at}web.de

Abstract

Background Pregnant women with inflammatory bowel disease (IBD) are at increased risk of adverse pregnancy outcomes. Comprehensive guidelines on medical management have been published; yet, there is limited guidance on service set-up and minimum standards of care for pregnant women with IBD.

Aim To develop a position statement on service set-up and minimum standards of care in the UK.

Methods A working group consisting of 16 gastroenterologists, obstetricians, obstetric physician, IBD specialist nurses and midwives was assembled. Initial draft statements were produced and a modified Delphi process with two rounds of voting applied. Statements were modified according to voters’ feedback after each round. Statements with ≥80% agreement were accepted.

Results All 15 statements met criteria for inclusion. To facilitate optimal care, regular and effective communication between IBD and obstetric teams is required. There should be nominated link clinicians for IBD in obstetric units and for pregnancy in IBD units. Preconception counselling should be available for all women with IBD. All pregnant women should be advised on the safety of IBD medication during pregnancy and breast feeding, the optimal mode of delivery, the management of biologics (where applicable) and safety of childhood vaccinations. Regular audit of pregnancy outcomes and documentation of advice given is recommended.

Conclusion Position statements have been developed that advise on the importance of joined-up multidisciplinary care, proactive decision-making with clear documentation and communication to the woman and other healthcare practitioners.

  • ulcerative colitis
  • Crohn's disease
  • inflammatory bowel disease

Data availability statement

No data are available. There are no data beyond the published data in the manuscript.

https://doi.org/10.1136/flgastro-2020-101459

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    Summary box

    What is already known about this subject?

    • Inflammatory bowel disease (IBD) affects pregnancy outcomes and requires complex decision-making.

    • Excellent international guidelines provide advice on medical management.

    What are the new findings?

    • This position statement provides IBD and obstetric services with guidance on service set-up and delivery.

    • Minimum standards of care have been developed to guide clinicians.

    How might it impact on clinical practice in the foreseeable future?

    • IBD and obstetric services should review current practice to ensure that standards of care are being met.

    • Regular audits using the proposed standards can be performed to guide quality improvement.

    Background

    Inflammatory bowel disease (IBD) affects many women of childbearing age, who often have poor knowledge of pregnancy-related issues in IBD,1 views adverse to medical guidelines2 and higher levels of voluntary childlessness.3 4 Women with IBD are at increased risk of adverse pregnancy outcomes including preterm birth, small for gestational age birth weight, gestational diabetes, stillbirth and are more likely to have a caesarean section.5 Over the past two decades, the management of women with IBD during the reproductive period has evolved and comprehensive guidelines have been published by the European Crohns and Colitis Organisation,6 7 the Canadian Society of Gastroenterology (Toronto consensus)8 and the American Gastroenterology Association.9 These guidelines address most aspects of care including advice on medication, vaccinations, investigations and mode of delivery.

    There is however limited guidance for clinicians on how to set up services to deliver safe and effective care for pregnant women with IBD. Women with IBD may encounter a multitude of healthcare professionals from different professional backgrounds including general practitioners, midwives, obstetricians, IBD specialist nurses and gastroenterologists during their pregnancy. Knowledge of IBD-related pregnancy care varies between different medical specialties increasing the risk of divergent advice being offered by practioners.10 Furthermore, obstetric and IBD care occurs not infrequently across different healthcare organisations increasing the difficulties in providing coordinated care. Uncoordinated care could increase women’s anxiety about the correct management and risk inappropriate cessation of IBD therapy. Poor communication between healthcare professionals could lead to delays in treating flares, delays in closely monitoring fetal health during flares, decisions on mode of delivery not taking IBD into account, reduced uptake of breast feeding and risk of inappropriate live vaccinations in infants exposed to biologics in utero.

    Effective guidance on service set-up, clear standards on communication and responsibilities in providing advice could help improve the safe provision of antenatal care for women with IBD. This position statement aims to provide guidance for clinicians involved in the care of pregnant patients with IBD. The focus of the position statement is on service set-up and minimum standards of care as well as audit recommendations.

    Methods

    British Society of Gastroenterology (BSG)-endorsed guidance statements are significant and influential brief statements addressing novel, topical or controversial subjects where it is felt that the society needs to clarify its position and give clear advice where possible to the membership.11 BSG-endorsed guidance statements are often limited to an expert opinion based on the latest best available evidence.11 This endorsed guidance statement was produced to address questions on service set-up, responsibilities of clinicians, minimum standards of care and suggestions for audit standards. While many aspects may be applicable to the wider IBD community, the endorsed guidance statement was developed to specifically address care in the National Health Service for women living in Great Britain and Northern Ireland.

    A modified Delphi process with a consensus meeting followed by two rounds of online voting and subsequent statement modification was applied. A working group was formed under the auspices of the BSG and expert clinicians in the field were identified and invited by two of the authors (CS and TG). The final working group consisted of six IBD expert gastroenterologists, five obstetricians, one obstetric physician, three IBD specialist nurses and one midwife. While the majority worked in academic teaching hospitals, three working group members came from District General Hospitals providing views of services outside of large academic centres. Themes of care provision were identified by the working group members through a narrative literature review and a face-to-face meeting in London in October 2018. The endorsed guidance statement was drafted in accordance with the guidance of the BSG on endorsed guidance statements, which in contrast to full guidelines advocates a less stringent approach without full systematic literature review and without grading of statements.11 Working group members rated their agreement on 5-point Likert scales from (1) totally disagree, (2) mostly disagree, (3) neutral, (4) mostly agree to (5) totally agree. Statements were included when ≥80% voted agree or totally agree. The final endorsed guidance statement was first reviewed and approved by the BSG clinical services and standards committee and then reviewed and endorsed by the council of the British Maternal and Fetal Medicine Society.

    Results

    The face-to-face meeting was attended by 14 working group members and voting rounds were closed after the minimum of 10 votes was reached for each round. All 15 statements reached the ≥80% agreement threshold and were included in the endorsed guidance statement.

    Domain 1: set-up of services

    Traditionally, pregnant patients with IBD were likely to have received separate care from IBD and obstetric services with great variation in care and service set-up. Due to the complexity of caring for pregnant patients with IBD, the care needs to be coordinated between services and provision by staff with relevant experience and expertise of IBD and pregnancy is highly desirable. Specific IBD antenatal services can facilitate coordinated high-quality care with subsequent good maternal and fetal outcomes.12 Joint consultations may not be feasible for all services but can provide the best model of care for communication between teams, providing unified patient advice and can reduce the number of total appointments required during a pregnancy. This may be out of the scope of some units where the number of pregnant women with IBD is insufficient to make the provision of joint clinics feasible.

    Statement 1:

    To facilitate optimal care and joint decision-making, regular and effective communication between IBD and obstetric teams is required. As a minimum there should be a nominated link clinician for IBD in every obstetric unit and a nominated link clinician for pregnancy in every IBD unit. [0% mostly, 90% totally agree]

    Statement 2:

    Specially set-up IBD pregnancy clinics can provide optimal specialised care. This is best facilitated by a joint clinic with an obstetric clinician and an IBD clinician present during the consultation. [30% mostly, 70% totally agree]

    Domain 2: minimum standards of care

    Many patients have poor knowledge of IBD-related issues in pregnancy1 and hold attitudes contrary to medical guidelines.2 13 These may in turn lead to poor adherence14 and an increased risk of flaring disease during pregnancy. As active disease is associated with adverse pregnancy outcomes, patients should be medically optimised prior to pregnancy, advised on the importance of maintaining remission from IBD and be given general advice on preconception health (smoking; alcohol, folic acid, etc). Patients who received IBD-specific prepregnancy counselling experienced better disease control during pregnancy and better pregnancy outcomes.12

    Statement 3:

    Pre-conception counselling should be available to all women with IBD to optimize preconception health. Poor patient knowledge on reproductive issues is associated with voluntary childlessness and adverse pregnancy related outcomes. Pro-active approaches to pre-conception counseling are considered the gold-standard. [0% mostly, 100% totally agree]

    Medical management of IBD during pregnancy requires weighing of potential risks of medication versus the usually higher risk of active disease. The IBD team is best placed to measure disease activity and take disease and treatment history into account. Advice on medication issues should be provided by the team with the best experience and knowledge. Gastroenterologists and IBD nurses have excellent IBD-related pregnancy knowledge.1 15 For most women with IBD, the IBD service can provide prepregnancy counselling but for women with other health issues or significant problems during previous pregnancies further advice from a maternal medicine obstetrician or an obstetric physician should be sought. Up to 40% of pregnancies are not planned and ideally all women with IBD of childbearing age should receive at least basic information about IBD, contraception and pregnancy.

    Statement 4:

    The IBD team must advise all patients with IBD who are pregnant or considering pregnancy on drug safety during conception, pregnancy and the importance of maintaining remission. [0% mostly, 100% totally agree]

    Women with IBD are at increased risk of adverse pregnancy outcomes and therefore have in general above average risk pregnancies.5 A consultant-led clinic should review the patient and assess for IBD and non-IBD risk factors to facilitate the most appropriate care and follow-up during pregnancy. The initial antenatal assessment should be delivered in a consultant-led antenatal clinic. The visit should be used to stratify disease and pregnancy risk and provide a detailed plan for the antenatal care including as a minimum the timing, setting and modality for maternal and fetal surveillance. Routine antenatal care should be provided by midwives and obstretricians in line with current national obstetric guidelines.

    Statement 5:

    Pregnant women with IBD should be offered consultant led obstetric care. Following initial clinic assessment care in different clinical settings may be appropriate. [40% mostly, 60% totally agree]

    Statement 6:

    All pregnant women with IBD should be offered IBD specialist care by a consultant or IBD nurse with experience in IBD pregnancy care. [0% mostly, 100% totally agree]

    Statement 7:

    The frequency of IBD, obstetric and or joint clinic follow-up should be determined by IBD disease activity in the absence of other obstetric concerns. Patients with mild disease can be monitored remotely (via “telephone” or “virtual” clinics) but moderate to severe disease requires follow-up by IBD, obstetric and/or joint clinics. [20% mostly agree, 80% totally agree]

    Management of biologics during pregnancy requires complex decision-making to ensure optimal patient outcomes. European and North American guidance differ on the question of continuation during the third trimester.7–9 Discontinuation of anti-tumour necrosis factor (TNF) at the end of the second trimester leads to lower drug levels in cord blood,16 which was thought to reduce the risk of serious infections in the infant.16 A large French study has however shown that women who discontinued anti-TNF experienced more flares while no differences in infant infection rates were seen between those exposed to third trimester anti-TNF and those not exposed.17 Women with IBD need to be advised on risks and benefits of continuing biologics during the third trimester on an individual basis taking into account their disease and treatment history.

    Statement 8:

    All pregnant women receiving biological therapy for IBD need to receive individual advice on whether to continue or stop therapy during the third trimester and when to restart therapy postpartum.

    • This discussion and the decision need to be clearly documented.

    • All women on biologics need to be counselled on safety aspects for the infant including vaccinations and advice on infection-related complications. [0% mostly, 100% totally agree]

    While the majority of women with IBD can have a vaginal delivery, choosing caesarean sections is crucial for the subset of women with active perianal disease.7 Women with ileo-anal pouches have borderline continence and may therefore benefit from caesarean sections to reduce the risk of sphincter injury.7 Women with IBD have caesarean sections significantly more often than than general population.5 Obstetricians should be advised by IBD teams whether an IBD indication for caesarean section is present or whether obstetric concerns alone in conjunction with patient wishes should guide the mode of delivery decision. Discussion with the surgical team may influence both timing and mode of delivery with early elective delivery (38 weeks) being preferable to emergency surgical delivery in some women with previous complex surgery. If early delivery is required, antenatal corticosteroids may need to be considered, to improve fetal lung maturity.

    Statement 9:

    All pregnant women with IBD should be advised on whether their IBD influences the mode of delivery

    • A clear recommendation on optimum mode of delivery should be made well in advance of the expected delivery date. Considerations need to be made in regard to absolute contra-indications for a vaginal delivery. Gold standard is a joint IBD-obstetric decision.

    • For patients with IPAA or perianal disease a joint approach that may include surgical input is required. [0% mostly, 100% totally agree]

    Breast feeding conveys many benefits to the infant including optimal nutrition, beneficial effects on the immune system and a potential reduction in the risk of developing IBD.7 18 The amount of biological agent found in breast milk is likely to be small and unlikely to be significantly systemically absorbed by the infant. Therefore, breast feeding should normally be encouraged.8 Patients require individual advice on the risks and benefits to make informed decisions on the choice of infant nutrition.

    Statement 10:

    All pregnant women with IBD should be counselled on the benefits of breast feeding with specific advice on the suitability of their medical treatment on breast feeding well in advance of the expected delivery date and the decision should be documented. [0% mostly, 100% totally agree]

    Childhood vaccinations are important for the infant’s health and the appropriate use of vaccinations needs to be based on medical advice. Only biological agents require an adjustment from the routine vaccination schedule as live vaccinations carry potential risks and should therefore be delayed.

    Statement 11:

    All pregnant women with IBD should be counselled on the safety of vaccinations for the newborn. Women on relevant biological drugs should be advised that the infant should avoid the rota virus vaccination and that the BCG vaccination should be delayed. This should be documented. [0% mostly, 100% totally agree]

    Pregnant women with IBD have an increased risk of preterm labour and small for gestation birth weight.5 This risk is largely from active inflammation and seems to be much lower in women having achieved remission from IBD.5 19 Fetal growth scanning can help obstetricians identify and/or monitor high-risk patients. Growth scans at 28 and 34 weeks gestation may be useful in women with active disease but the benefit of routine scanning in the third trimester in women with mild disease or in clinical remission from IBD is unclear.

    Statement 12:

    Additional growth scans in the 3rd trimester should be considered for patients with active IBD and/or other comorbidities as determined by the supervising obstetrician. [10% mostly, 90% totally agree]

    Patients with IBD are at increased risk of venous thromboembolism (VTE) during flares and this risk is further increased during pregnancy.20 For women with active IBD, thromboprophylaxis with low molecular weight heparin should be considered. The Royal College of Obstetrics and Gynaecology (RCOG) guidelines provide helpful advice that includes all known risk factors for VTE.21

    Statement 13:

    In patients with active IBD prophylaxis against venous thromboembolism should be considered taking into account other risk factors using the RCOG VTE guidelines. [0% mostly, 100% totally agree]

    Continuity of care postdelivery is important for all women with IBD. This particularly busy period for new mothers can be challenging. Clear advice on when and how to contact the IBD service is vitally important to allow for swift follow-up where needed without burdening new mothers with routine appointments when in remission. Some women with ulcerative colitis experience a higher risk of postpartum flares8 and should be advised on how to manage this. Furthermore, women who discontinued biologics need to be advised when to restart these.

    Statement 14:

    Prior to delivery women should be advised on the plan for follow-up post partum and given contact details for the IBD service. [0% mostly, 100% totally agree]

    Domain 3: audit of services

    Routine capture of pregnancy outcome is advised to help services review their results and allow for quality improvement programmes. We have proposed four audit standards on decision-making and documentation that are vital to ensure safe high-quality care. We suggest that services audit their IBD antenatal care to ensuring minimum standards of care are met.

    Statement 15:

    Pregnancy related outcome data should be captured regularly where possible and should include: delivery date, mode of delivery, complications and breast feeding status.

    Services should aim to achieve a 90% target for:

    • Documented decision on biological therapy during pregnancy

    • Documented advice on delivery method

    • Documented advice on vaccination for the newborn

    • Documented advice on breast feeding [20% mostly agree, 80% totally agree]

    Discussion

    The management of IBD during pregnancy requires complex decision-making incorporating consideration of maternal and fetal health. For the vast majority of patients, the risk of active IBD poses a risk that far outweighs any medication risk (except for methotrexate or tofacitinib) and continuation of maintenance therapy is vital to ensure well-controlled IBD which in turn is associated with better pregnancy outcomes.5 7 12 22 Patients however often harbour concerns and fears over IBD medications during pregnancy, which increases the risk of non-adherence.13 23

    Clinician knowledge varies according to specialty, and advice by clinicians not versed in the management of pregnant patients with IBD may lead to inappropriate (usually overcautious) medical advice.10 Furthermore, uncoordinated care between obstetric and IBD units may increase the risk of the patient perceiving medical advice from the respective units to be conflicting. Opportunities to optimise care and instigate tighter monitoring of the pregnancy may be missed, which in turn could lead to adverse pregnancy outcomes. In light of this, the IBD antenatal working group was formed to provide this endorsed guidance statement on service standards for the care of pregnant women with IBD. The standards are often based on expert opinion as evidence for high-quality care was sometimes lacking. This endorsed guidance statement does not aim to replicate the excellent medical guidance offered by European and North American detailed guidelines,7–9 but aims to provide practical advice for clinicians in the UK on how to organise services and what should be seen as minimum standards of care.

    Collaborative working between obstetric and IBD units is, in the view of the working group, key to providing high-quality care. A dedicated IBD pregnancy clinic in the Netherlands has shown that coordinated care and prepregnancy counselling are associated with better maternal and fetal outcomes.12 While such specially set-up clinics are models for high-quality care, they are resource intensive and may not be justified in smaller IBD units where the patient numbers do not justify this set-up. Coordinated working can also occur via nominated link clinicians and routine communication after every clinical encounter. This is especially important in Trusts where different electronic systems for health records are used in maternity and gastroenterology.

    To avoid confusion for patients and general practitioners advice on safety of medications during pregnancy, breast feeding and childhood vaccinations should be provided to all pregnant women with IBD and clearly documented and communicated. Decisions on mode of delivery should be informed by advice from the IBD unit whether there is an IBD indication for a mode of delivery.

    In summary, this endorsed guidance statement provides advice on how to organise services for pregnant women with IBD and sets minimum standards of care. Further work including potentially a nationwide audit is required to assess quality of care for pregnant women with IBD. Qualitative research into how women perceive their care would also be important.

    Data availability statement

    No data are available. There are no data beyond the published data in the manuscript.

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    Footnotes

    • Contributors All authors developed the guidance statements by contributing to face-to-face discussion on the guidance statement, formulating the statements and voting on the statements. The draft article was written by CS. NC, SC, CN-P, AF, VH, KH, JL, LS, MS, MCG, AM, KM, AK, KBK and TG critically reviewed the article.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

    • Competing interests CS has received unrestricted research grants from Warner Chilcott, Janssen and AbbVie, has provided consultancy to Warner Chilcott, Dr Falk, AbbVie, Takeda, Fresenius Kabi and Janssen, and had speaker arrangements with Warner Chilcott, Dr Falk, AbbVie, MSD, Pfizer and Takeda. CN-P had speaker arrangements with Dr Falk, UCB, Sanofi, Alliance and Alexion. KBK has provided consultancy to Amgen and PredictImmune, and had speaker arrangements with Janssen and Takeda. AK has provided consultancy to Abbvie, and had speaker arrangements with Pfizer, Janssen and Takeda. JL has received research grants from Takeda, consultancy and speaker fees from Abbvie, Janssen, MSD, Pfizer and Takeda. All other authors do not declare any conflict of interest. No funding was received for this work.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    Linked Articles

    • UpFront
      Highlights from this issue
      R Mark Beattie
      Frontline Gastroenterology 2021; 12 167-168 Published Online First: 07 Apr 2021. doi: 10.1136/flgastro-2021-101849