The management of post-Caesarean infection is widely perceived as the responsibility of secondary care but, because most women are discharged within one to two days, infections are rarely seen in the hospital setting. The provision of care therefore falls to community services. It is important that NHS Trusts, Clinical Commissioning Groups (CCGs) and Health Boards agree a common management pathway that optimises patient care and minimises administrative and financial burdens.
At a symposium sponsored by Smith & Nephew, held at the Royal College of Obstetricians and Gynaecologists in London on 23 June 2014, a multidisciplinary Advisory Board was convened to interpret recent evidence on the management of post-Caesarean infection in the light of clinical experience. In workshop groups, participants reviewed their practice and discussed which areas could be improved to support closer collaboration between acute surgical units and community services. These discussions are intended to form the basis of a practice guideline for primary and secondary care to prevent post-Caesarean infection.
Caesarean section (CS) is probably the most common major operation performed on women in the world.1 In England, the proportion of births by CS has risen substantially over the past 30 years, from 9% in 1980 to 25.5% in 2012/13.2,3 There are many possible ways of performing the procedure, and operative techniques vary widely depending on many factors, including the clinical situation and the preferences of the operator.1 Surgical site infection or incision dehiscence is one of a number of possible complications of a CS and while most CS-related wound infections are superficial, this represents a substantial burden to the health system given the high number of women undergoing the procedure.2
Developing a UK national guideline for preventing a post-Caesarean infection
Discussion at the symposium was stimulated by results from a prospective study of 4107 women undergoing CS in 14 NHS hospitals in England by the Health Protection Agency (HPA), which found that the incidence of surgical site infection within 30 days was 9.6% (Box 1).2 Few independent risk factors were identified, but the strongest relationship was associated with increasing body mass index (BMI; Figure 1). The rate of infection in obese women was approximately 20%. However, anecdotal experience has long suggested that the risk of infection is also increased by many other factors, such as emergency CS and prolonged second-stage labour.
This disagreement between published evidence and the perceptions of health professionals raises questions about awareness of the factors that contribute to post-CS infection and the impact of current clinical practice on risk. Almost all of the infections in the HPA study were diagnosed after the patient had been discharged from hospital, raising the possibility that surgeons underestimate the scale of the problem and do not recognise the possible causes. Conversely, care in the community may not be optimal.
The National Institute for Health and Care Excellence (NICE) guideline for CS includes recommendations for all women undergoing CS with no specific guidance for the management of women who are obese.4 Obstetric practice is very individual and, given that the preferences of the surgeon are major determinants of the choice of surgical procedures and materials for CS,it is important to raise awareness about the factors that increase the risk of infection.
Surgeons may be surprised by the high infection rate associated with CS among their overweight and obese patients. Because the length of stay is typically one to two days and most infections occur after the patient has left hospital, surgeons do not receive feedback about their perioperative care from the patient. They may believe that infections occurring in the community are not serious, but that is not always the case.
The Advisory Board noted a lack of expertise in wound management in the community. With the advent of direct entry to midwifery, some new midwives will lack the first-hand experience of wound care that is gained by their peers who progressed through general nursing. This is not tenable when a subgroup of women have a risk of infection of over 20%.
Reducing post-CS infection rates in women with BMI ≥35
Mr Sean Burns (Consultant Obstetrician, Wrightington, Wigan and Leigh NHS
Foundation Trust) described an evaluation of measures to reduce the risk of post-CS infection.5 Audit within the Trust had demonstrated an overall post-CS infection rate of 12%.6 However, there were three to four readmissions per month due to infection in women with a BMI >35. The average length of stay for each readmission was three days, giving an average direct cost per patient episode of £1050.
A thorough multidisciplinary review of the entire patient pathway revealed no significant deviation from recommended procedures, but staff and patients lacked education about wound care and it was evident that most infections were occurring after discharge. A review of wound care procedures showed that dressings were removed after one day, consistent with NICE guidance on CS,4 but conflicting with the generally accepted good clinical practice of covering the wound with an appropriate dressing for 48 hours.7
Following the review, in line with changing protocols to incorporate prolonged wound care, OPSITE◊ Post-Op Visible (Smith & Nephew) was used and left in
situ for at least seven days in uncomplicated, low-risk cases (ie BMI <35).6 In wounds with excessive exudate levels, the dressing was changed earlier. This dressing was chosen because it allows good visibility of the incision, as well as being soft and conformable.
Tissue viability and infection control nurses also selected negative pressure wound therapy (NPWT) for evaluation in obese women undergoing CS.6 NPWT has been shown to reduce infection rates and length of stay in orthopaedic surgery and has been used successfully in overweight and obese patients.8,9 Early dressing removal may interrupt the process of re-epithelialisation, so it was agreed that the dressing would be left in place for seven days.
PICO◊ (Smith & Nephew) was selected as the postoperative dressing (Figure 2) for the obese women. This is a canister-free, single-use NPWT system with an innovative dressing. Clinical experience showed that it has good adhesiveness in obese women. The implementation included the following:
- Staff were educated about wound assessment, recognising infection and appropriate swabbing.
- Patients were given written information to help them recognise infection and instruct them how to respond. They were advised to use underwear that did not rub on the dressing.
- Patients were followed up for 30 days, and received telephone contact and one home visit.
- Surgical site infection was defined as two clinical signs supported by a positive swab.
Subsequently, between February 2012 and January 2014, 1289 CSs were carried out in the Wrightington, Wigan and Leigh NHS Foundation Trust, including 206 women with BMI ≥35, of whom 79 had a BMI ≥40 (these data build upon a prior 138-patient analysis presented at the 23rd European Congress of Obstetrics and Gynaecology in May 201410). The data showed the following:
- The infection rate during this period was 3.6% (2.6% within the last 12 months).
- There were no readmissions.
- Patient feedback was positive.
- Based on an historical comparison, it is estimated that post-CS NPWT saved the Trust approximately £59 000 over two years.
Women are currently assessed for factors that may increase the risk of CS and complications, including the following:
- Preoperative assessment of risk factors, such as maternal age >45, obesity and previous CS, informs subsequent management and helps to provide information that is individually relevant when counselling about CS.
- In-labour risk factors include prolonged membrane rupture, temperature >38°C, chorioamnionitis and prolonged second-stage labour.
- Postoperative factors include haemoglobin <8g/dL and a surgery duration of >60 minutes.
The HPA study did not find clear evidence that these traditional risk factors were in fact relevant. Obesity was the single most important factor for developing infection.2 The consideration of the Advisory Board was that all women having a CS should be assessed and managed in the same manner with regard to infection prevention, but specific measures may be required in the obese. Why the obese are at particular risk remains uncertain. It is of note that the risk increases with increasing BMI.
Obesity is a significant risk factor for post-Caesarean infection2
The HPA study identified that the organisms are primarily skin and faecal, suggesting entry into the wound from the skin, and the delayed onset of infection in relation to the date of surgery points to wound hygiene as an area of concern.2 The pannus in obese women produces a moist warm environment that reduces the effectiveness of personal hygiene and promotes transdermal spread of skin organisms into the surgical incision.
Because most post-CS infections occur in the community, women should also be risk assessed at the time of discharge. Those with evidence-based risk factors for post-CS infection (ie a high BMI, diabetes) should be flagged because these criteria can be used to guide the choice and duration of use of postoperative dressing. Referral to the tissue viability team should be considered for women with BMI ≥35. Cosmetic surgeons may leave sutures in place for up to 14 days to improve the cosmetic outcome, but it is not known whether this would be a useful strategy after CS. An additional factor is that the prophylactic antibiotics may be less effective in the obese, whether due to reduced tissue penetration or even that a standard dose is actually too low for an obese woman. In children, it is normal practice to titrate the dose of an antibiotic against the weight of the child. This is not done in adults, and Falagas et al suggest that this reduces the effectiveness of antibiotics in the obese.11
Almost all post-Caesarean infections develop after discharge from hospital2
Obstetric units differ in their intraoperative procedures and there is no evidence that demonstrates the superiority of a specific approach. Each unit should develop its own standards of practice and work to improve the competence of all staff.
Obstetricians should adopt a consensus approach to intraoperative management within the unit. Examples include standardisation on the choice of antibiotic therapy, skin preparation, skin closure and suture material, and protocols for the theatre such as access during surgery and temperature control.
Choosing between options for intraoperative management should take into account published evidence. The NICE guideline on CS includes recommendations on operative technique and recommends pre-incision antibiotic prophylaxis with an agent other than co-amoxiclav.4 One trial has shown that subcuticular skin closure was associated with better short-term cosmetic outcomes and less skin closure time than interrupted skin closure in obese non-diabetic women, although there was a slightly higher risk of superficial incisional surgical site infection and significantly more postoperative pain.12 NICE states that the evidence is inconclusive on the relative merits of different suture materials for skin closure.4
A 1998 meta-analysis of 25 trials involving a total of 12 249 patients with abdominal wound closures concluded that continuous closures with non-absorbable suture should be used for most wounds, but interrupted absorbable sutures are preferred if infection or distension is anticipated.13 Monofilament is associated with a lower risk of infection than braided sutures.14 Trials have shown advantages for other methods of closure, such as skin closure with Steri-StripsTM, over subcuticular closure with sutures for abdominal procedures.15 Steri-StripsTM offer the practical advantage of deterring the patient from touching the wound, but they cannot be used with dressings such as PICO◊. There appears to be no difference in the complication rate associated with interrupted or continuous slowly absorbable sutures for closure of primary elective midline abdominal incisions.16
There was a consensus among members of the Advisory Board that monofilament should replace braided sutures for all closures, although opinion was divided on the choice of absorbable or non-absorbable sutures for skin closure. Given the lack of definitive evidence, there is no single solution that is appropriate for all units. The Board recommended that units should standardise the choice of suture and skin closure because this should increase staff expertise and facilitate the provision of consistent patient information.
Staff should receive training in the use of the dressings selected by the unit. The
precise time for which a dressing is left in place is less important than it being of sufficient duration – that is, five to seven days rather than 24 hours. The experience at Wrightington, Wigan and Leigh NHS Foundation Trust provides evidence that NPWT is effective in reducing the risk of post-CS infection in obese women (reducing post-CS infection rate to 3.6% from 12% and saving the Trust around £59 000 over two years); a cost-effectiveness analysis is now needed.
A transverse Joel-Cohen incision is recommended for CS.4 Some Board members noted that a low vertical incision may be suitable for very obese women, but experience is limited.
Superficial wound drains should not be used in CS.4 They are associated with an increased incidence of pain, longer healing, a greater risk of adhesions and an increased risk of infection.
There is a lack of evidence to guide antibiotic dosing for obese women who, by virtue of their greater body mass, may be considered for higher or more frequent doses. The dose of antibiotics with a narrow therapeutic ratio, such as gentamicin, is calculated on the basis of body weight. Some surgeons use this approach for safer antibiotics such as co-amoxiclav and the cephalosporins when calculating the appropriate dose for women weighing over 80kg. The surgical unit should liaise with local clinical microbiologists and clinical pharmacologists to agree the best approach.
An infection can have a profound effect on a patient’s ability to support the family by imposing a burden of outpatient appointments and transport costs
Women should be advised that hair should be clipped. Shaving and waxing are associated with localised trauma and altered local flora that may increase the risk of infection. However, these changes do not persist and women who shave or wax at least 48 hours before admission are not necessarily at increased risk.
Chlorhexidine is normally the disinfectant of choice for skin preparation. Care should be taken to avoid pooling of alcoholic preparations when using procedures such as diathermy. Chlorhexidine is available in different formulations. Chloraprep® (2% chlorhexidine in 70% isopropyl alcohol) is supplied with an applicator that avoids pooling. The solution should be allowed to air dry on the skin.
In the immediate postoperative period, patients should be taught about wound hygiene and the signs of infection, and advised on how to look after their dressing and how they can bathe. Verbal advice should be supported by written information and must be consistent; health professionals should avoid offering conflicting advice. Information should include a list of recommended websites providing quality information and a telephone number to contact the midwifery service. Written information should be provided in a simple format, such as a card, and the midwife should go through this with the patient at the time of discharge.
The dressing should normally be left in place for five to seven days. There is no evidence to guide practice after this period, but longer duration of use should be considered for women at increased risk of complications. The consensus view of the Board is that the wound should be assessed on Day 7. Given the concerns about increased risk of late-onset infection in obese individuals, the recommendation is to consider applying a new occlusive dressing in those identified women for a further period of four to seven days. This should be supported with appropriate education for the woman to be empowered to manage and assess her own wound and to have easy access for advice to a named professional.
Health professionals, particularly nurses and midwives, should be offered education about wound management that includes correct procedures for swabbing a wound and clear criteria for diagnosing a wound infection. There is no evidence to show that it is essential to view a wound and therefore to use a transparent dressing. While this is one factor that may be taken into account, it should not override other clinical considerations when selecting a dressing.
NICE recommends that ‘women should be offered early discharge (after 24 hours) from hospital and follow-up at home.’4 This means that the surgeon is likely to lose contact with the patient and will not be aware of wound infection unless the patient is readmitted.
Communication between health professionals in primary and secondary care is often unsatisfactory. Contributory factors include the absence of GP involvement during the pregnancy and a lack of secondary care input after discharge. It is therefore important to develop a single patient pathway that is led by a midwife who has responsibility for co-ordinating care and signposting women to appropriate sources of support. This pathway should empower women to take some responsibility for the care of their wound.
It is important to assess and improve the entire patient pathway, not simply change one or two interventions
It is essential to monitor women’s progress after discharge. Infection control should be promoted by a local champion who can be the primary point of contact
within the community midwife team and who can liaise with the tissue viability service both clinically and to encourage education about wound care.
Different trusts and Health Boards will develop service models and funding streams best suited to their own needs. Patients discharged to a catchment area outside of the trust may therefore receive different treatments and health professionals should work to minimise disruption to their care.
NHS Trusts and Health Boards have a nominated individual responsible for oversight of governance; this person should monitor the implementation of and adherence to the pathway to ensure effective collaboration between primary and secondary care. Ideally, this would not impose an additional administrative burden on practitioners.
Importance should be placed on developing a single patient pathway that empowers women to take some responsibility for the care of their wound
It should be recognised that the cost of post-CS wound care falls mainly on the
primary care sector (except for readmission within 30 days). CCGs are aware that wound care is potentially expensive and will fund a pathway that is of demonstrable benefit in reducing the risk of complications and offers the prospect of lowering spending. The pathway must show how primary and secondary care are working together to rationalise treatment and minimise service duplication, recognising that decisions made by one sector have implications for the other. CCGs are more likely to fund a pathway that has been endorsed by the relevant professional bodies. NHS Trusts and Health Boards may care for patients from several CCGs, in which case CCGs should be encouraged to form a representative group that can negotiate for them all.
- Anderson ER, Gates S. Techniques and materials for closure of the abdominal wall in caesarean section. Cochrane Database Syst Rev 2004;(4):CD004663.
- Wloch C, Wilson J, Lamagni T, et al. Risk factors for surgical site infection following caesarean section in England: results from a multicentre cohort study. BJOG 2012;119:1324–33.
- NHS Health and Social Care Information Centre. Hospital Episode Statistics: NHS Maternity Statistics – 2012–13 (www.hscic.gov.uk/catalogue/PUB12744/nhs-mate-eng-2012-13-summ-repo-rep.pdf; accessed 4 July 2014).
- National Institute for Health and Care Excellence. Caesarean section. Clinical Guideline 132. August 2012 (www.nice.org.uk/guidance/cg132; accessed 7 July 2014).
- Bullough L, Wilkinson D, Burns S, Wan L. Changing wound care protocols to reduce post-operative caesarean section infection and readmission. Wounds UK 2014;10:72–6.
- Bullough L, Wilkinson D. Changing wound care protocols to reduce post-operative caesarean section complications. Wounds UK Conference, Harrogate, UK, 12–14 November 2012.
- National Collaborating Centre for Women’s and Children’s Health. Surgical site infection prevention and treatment of surgical site infection. October 2008 (www.nice.org.uk/guidance/cg74/resources/cg74-surgical-site-infection-full-guideline2; accessed 15 August 2014).
- Grauhan O, Navasardyan A, Hofmann M, et al. Prevention of poststernotomy wound infections in obese patients by negative pressure wound therapy. J Thorac Cardiovasc Surg 2013;145:1387–92.
- Grauhan O, Navasardyan A, Tutkun B, et al. Effect of surgical incision management on wound infections in a poststernotomy patient population. Int Wound J 2014;11 (Suppl 1):6–9.
- Bullough L, Burns S and Wilkinson D. Reducing infection rates in Caesarean section patients with BMI of 35 or more: a 138 patient evaluation. 23rd European Congress of Obstetrics and Gynaecology (EBCOG), Glasgow, UK, 7–10 May 2014.
- Falagas ME, Karageorgopoulos DE. Adjustment of dosing of antimicrobial agents for bodyweight in adults. Lancet 2010;375:248–51.
- Ibrahim MI, Moustafa GF, Al-Hamid AS, et al. Superficial incisional surgical site infection rate after cesarean section in obese women: a randomized controlled trial of subcuticular versus interrupted skin suturing. Arch Gynecol Obstet 2014;289:981–6.
- Weiland DE, Bay RC, Del Sordi S. Choosing the best abdominal closure by meta-analysis. Am J Surg 1998;176:666–70.
- Hochberg J, Meyer KM, Marion MD. Suture choice and other methods of skin closure. Surg Clin North Am 2009;89:627–41.
- Kerrigan CL, Homa K. Evaluation of a new wound closure device for linear surgical incisions: 3M Steri-Strip S Surgical Skin Closure versus subcuticular closure. Plast Reconstr Surg 2010;125:186–94.
- Seiler CM, Bruckner T, Diener MK, et al. Interrupted or continuous slowly absorbable sutures for closure of primary elective midline abdominal incisions: a multicenter randomized trial (INSECT: ISRCTN24023541). Ann Surg 2009;249:576–82.