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Instituting Surveillance Guidelines and Adverse Outcomes in Preeclampsia

Menzies, Jennifer BSc1,5; Magee, Laura A. MD, FRCPC1,2,3,4; Li, Jing MSS4; MacNab, Ying C. PhD2,4; Yin, Ruihua MSc5; Stuart, Heather BSc1; Baraty, Brandon BSc1; Lam, Elaine BSc1; Hamilton, Trevor BSc6; Lee, Shoo K. MBBS, PhD7; von Dadelszen, Peter MBChB, DPhil for the Preeclampsia Integrated Estimate of RiSk (PIERS) Study Group

doi: 10.1097/01.AOG.0000266977.26311.f0
Original Research

OBJECTIVE: To assess the incidence of combined adverse maternal and perinatal outcomes in women with preeclampsia before and after introducing standardized assessment and surveillance.

METHODS: This study was a preintervention (retrospective) compared with a postintervention (prospective) cohort comparison in a single-tertiary, perinatal unit that included women admitted to hospital with preeclampsia. We interrogated an existing retrospective 24-month database and then introduced the guidelines, assessing the incidence of the combined adverse maternal and perinatal outcomes for 41 months (September 2003 through February 2007). Tests of organ (dys)function were performed at least as often as on the day of admission, admission day +1, every Monday and Thursday, day of delivery, and delivery day +1. All data were checked for errors. The combined maternal outcome was maternal death or one or more of hepatic failure, hematoma, or rupture, Glasgow coma score of less than 13, stroke, at least two seizures, cortical blindness, need for positive inotrope support, myocardial infarction, infusion of any third antihypertensive, renal dialysis, renal transplantation, at least 50% FIO2 for greater than 1 hour, intubation, or transfusion of at least 10 units of blood products. The combined perinatal outcome was perinatal or infant mortality, bronchopulmonary dysplasia, necrotizing enterocolitis, grade III/IV intraventricular hemorrhage, cystic periventricular leukomalacia, or stage 3–5 retinopathy of prematurity.

RESULTS: Two hundred ninety-five and 405 women were in the preintervention and postintervention cohorts, respectively. The incidence of adverse maternal outcome fell (5.1% to 0.7%; Fisher P<.001; odds ratio 0.14, 95% confidence interval 0.04–0.49). Perinatal outcomes did not change.

CONCLUSION: Standardized surveillance of women with preeclampsia was associated with reduced maternal risk.


Introducing standardized surveillance of women with preeclampsia is associated with reduced maternal risk.

From the Departments of 1Obstetrics and Gynaecology, 2Health Care and Epidemiology, and 3Medicine, and the 4CFRI Centre for Healthcare Innovation and Improvement, University of British Columbia, Vancouver, British Columbia; 5Department of Ambulatory Care and Prevention, Harvard Medical School, Cambridge, Massachusetts; 6Faculty of Medicine, Dalhousie University, Halifax, Nova Scotia; and 7Department of Paediatrics and iCARE, University of Alberta, Alberta, Canada.

* For members of the PIERS Study Group, see the Appendix.

Funded by grants from the Canadian Institutes for Health Research (operating grants to P.v.D. and S.K.L. and salary awards to P.v.D., S.K.L., and J.M. [STIRRHS award]), the Michael Smith Foundation for Health Research (operating grant to S.K.L. and salary awards to P.v.D. and L.A.M.), and the Child and Family Research Institute (salary award to P.v.D.).

The authors thank Pamela Lutley, Jonathan Lam, and Kelly Richardson for their research assistance.

Corresponding author: Dr. Peter von Dadelszen, University of British Columbia, Department of Obstetrics and Gynecology, 2H30-4500 Oak Street, Vancouver, BC V6H 3N1, Canada; e-mail:

Financial Disclosure The authors have no potential conflicts of interest to disclose.

Preeclampsia remains a leading cause of maternal mortality in North America, and we have found that the surveillance of women with suspected or confirmed preeclampsia is variable between practitioners.1 The mainstays of the management of severe preeclampsia include “full assessment of the mother and the baby, and delivery on the best day in the best way.”2

It has been observed that standardizing care is associated with reduced adverse health outcomes across a range of disciplines and medical conditions.3–14 Failure to standardize care has been associated with poorer outcomes.14

We have previously undertaken a multicenter retrospective study of 2 years of preeclampsia cases in three tertiary level units.15 In that study, we tested a number of predictors of adverse maternal outcomes against a combined adverse maternal outcome derived by international Delphic consensus.16,17 This combined adverse outcome reflects the systemic inflammatory nature of the maternal syndrome18,19 and assesses all vulnerable organ systems.19 In an era of generally adequate blood pressure control, maternal mortality associated with preeclampsia is largely due to the complications of systemic inflammation.18

Since the time of the retrospective study, we have developed guidelines for the assessment and ongoing evaluation of women admitted to our unit with a suspected or confirmed hypertensive disorder of pregnancy. Part of a continuous quality improvement initiative at British Columbia Women’s Hospital and Health Centre (BC Women’s), these guidelines were designed to evaluate comprehensively vulnerable organ function and to reflect both the variable presentation and the systemic nature of preeclampsia (gestational hypertension with either proteinuria or adverse conditions) and the other hypertensive disorders of pregnancy. They were derived from the pattern of investigation used in other centers of excellence, and in response to international guidelines,20–22 to current practice across Canada1 and preliminary evidence that it may be possible to identify those women most at risk of doing poorly.15 In this paper we describe the incidence and pattern of adverse maternal and perinatal outcomes before and since introducing the guidelines.

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From the previous retrospective study,15 we identified those patients who had been cared for at BC Women’s, from January 2000 to December 2001. The criteria for inclusion in that study were admitted women with preeclampsia, the hemolysis, elevated liver enzymes, low platelets (HELLP) syndrome, or eclampsia. The same criteria were used for the prospective part of the study published here, although the guidelines cover all women with either hypertension in pregnancy or gestational proteinuria or both.

In this context, preeclampsia was defined as at least two of the following: 1) hypertension (systolic blood pressure of 140 mm Hg or greater and/or diastolic blood pressure of 90 mm Hg or greater, taken twice more than 4 hours apart) after 20 weeks of gestation, 2) proteinuria defined as 0.3 g/d or more or 2+ or more dipstick proteinuria after 20 weeks of gestation, 3) nonhypertensive and nonproteinuric HELLP syndrome, using Sibai’s criteria,23 or 4) an isolated eclamptic seizure without preceding hypertension or proteinuria, using the British Eclampsia Survey Team criteria to define eclampsia.24

These guidelines were developed as a minimum standard. The timing of the investigations was at least as frequently as the day of admission, admission day +1, every Monday/Thursday (ante- and postpartum), day of delivery, and delivery day +1. Additional clinical, laboratory, and ultrasound evaluations were performed whenever considered necessary or prudent by providers. There is no policy of mandatory subspecialty consultation.

In addition to routine measurement of maternal blood pressure, the investigations included the following:

  1. Hematology: full blood screen, international normalized ratio (INR), activated partial thromboplastin time (APTT), and fibrinogen.
  2. Renal: urea, creatinine, electrolytes, uric acid, and dipstick. While other testing occurred twice weekly, urine was also assessed by 24-hour urine for protein and creatinine clearance (on admission and once weekly thereafter [every Sunday/Monday]).
  3. Hepatic: aspartate transaminase (AST), alanine transaminase (ALT), lactate dehydrogenase (LDH), bilirubin, albumin (plasma), and random glucose.
  4. Respiratory: pulse oximetry.
  5. Fetal surveillance (antenatally only): cardiotocography (CTG; daily), ultrasound for assessment of fetal weight (every 14 days), and amniotic fluid volume and umbilical artery Doppler (twice weekly).

These guidelines were introduced into practice in September 2003 through the North American practice of standing orders. Standing orders are preprinted forms used to standardize management to improve outcomes. The use of the standing orders was monitored each weekday by two of us (J.M. and B.B.), and those practitioners not using the orders were contacted to request their use. Using a pre-/postintervention study design, we examined the influence of introducing the guidelines on the incidence of the combined adverse maternal outcome.

The combined outcome was maternal death or one or more of hepatic failure, hematoma, or rupture, Glasgow coma score less than 13, stroke, two or more seizures, cortical blindness, need for positive inotrope support, myocardial infarction, infusion of any third antihypertensive, renal dialysis, renal transplantation, 50% or more FIO2 for more than 1 hour, intubation, or transfusion of 10 or more units of blood products.15 We also assessed a combined adverse perinatal outcome (Delphic consensus): perinatal or infant mortality, bronchopulmonary dysplasia, necrotizing enterocolitis, grade III or IV intraventricular hemorrhage, cystic periventricular leukomalacia, or stage 3–5 retinopathy of prematurity.15

Specifically, comparisons were made based on the incidence among 295 women from the feasibility study of January 2000 to December 2001 (as preintervention) and 405 women with completed charts from the postintervention period of September 1, 2003, to February 28, 2007. Because the incidence was uncommon (particularly in the postintervention period), statistical analysis of rates and ratios were carried out by assessing Fisher exact test and odds ratio, using Prism 4.0 (GraphPad, San Diego, CA). For continuous variables (demographics), Student t test was used, unless otherwise stated. Significance was set at P<.05. The study was approved by the University of British Columbia Clinical Research Ethics Board and Children’s and Women’s Health Centre of British Columbia Research Review Committee.

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Of the 594 women included in the retrospective study,15 295 were cared for at BC Women’s; of these, 15 women (5.1%) developed the outcome. The postintervention cohort includes data from 405 women, of whom one was a postpartum transfer accompanying an infant admitted for neonatal intensive care.

Table 1 presents the clinical characteristics of the women in both cohorts. Initially, use of the standing orders for eligible antepartum women was 42%. For the final 15 months of the study period, the use remained consistently above 92% for antepartum women. Of the 404 women admitted antepartum for whom the orders were used, the minimum frequency of surveillance set by the standing orders was not met in 37 (9.2%) women, with 158 (39.1%) and 209 (51.7%) receiving surveillance either matching or exceeding the minimum frequency, respectively.

Table 1

Table 1

At all time periods, postpartum orders use remained about 10% lower than for the antepartum orders. The women in the postintervention cohort were at least as unwell with preeclampsia (in terms of objective blood pressure and renal and hepatic markers of disease severity) as the women in the preintervention cohort. Women in the postintervention cohort were also admitted at an earlier gestational age, were more likely to carry a multiple pregnancy, and more likely to receive antihypertensive medications than women in the preintervention cohort. Expectant management was more commonly used postintervention, as reflected in the increased admission-to-delivery interval for the whole postintervention cohort.

For women admitted before 34+0 weeks of gestation (when expectant management could be anticipated), the median admission-to-delivery interval was 2 days greater for the postintervention (128 of 405) than for the preintervention (99 of 295) cohort (4 days, interquartile range 2–9, compared with 2 days, interquartile range 1–3, respectively; Mann-Whitney U, P<.001).

Since the introduction of the standing orders, the incidence of the combined adverse maternal outcome fell from 5.1% (15 of 295) to 0.7% (3 of 405); Fisher exact test, P<.001; odds ratio 0.14 (95% confidence interval 0.04–0.49), with a power of 0.89 (Table 2). The combined adverse perinatal outcome did not differ between cohorts, but there was a trend to improved outcomes in the postintervention period (Table 3).

Table 2

Table 2

Table 3

Table 3

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Introducing standing orders was associated with a reduced incidence of adverse maternal outcomes. This effect was greater than we had anticipated and than could have been expected from the experience of others.6 The women in the postintervention cohort were certainly not at lower risk than were those in the preintervention cohort; they had higher admission blood pressure, heavier admission dipstick proteinuria, and earlier-onset disease.15 Twenty-four hour urines were collected in less than 60% of both cohorts; therefore, we cannot comment on the comparability of fully assessed proteinuria. We believe that the failure to routinely complete 24-hour collections was due to the fact that most cases of preeclampsia arise at term, and because those women are generally admitted for delivery, 24-hour urine collection is generally not practicable under those circumstances, even in a tertiary health sciences center. The maternal age differences and rising rates of multiple births (primarily through assisted reproductive techniques) observed between the cohorts reflect the changing maternity demographics seen in British Columbia.25

We recognize that combined adverse outcomes always reflect a spectrum of adversity.26 For example, is the decision to use a third antihypertensive equivalent to the occurrence of stroke? This combined adverse maternal outcome was agreed upon by a Delphic consensus of internationally recognized experts in the field.15 We believe that it is unusual for women to receive three parenteral antihypertensives (indeed, only 3 [0.43%] of the total 700 women did so). In this institution, this would reflect perceived clinical failure by the treating physicians (obstetrician, obstetric internist, and/or obstetric anesthesiologist) of both intravenous labetalol and hydralazine, precipitating the use of nitroprusside. We were not prescriptive of clinical practice, and no set guidelines were in place to guide the timing of the use of a third parenteral agent.

The improvements in outcome came during a phase of increasing institutional acceptance of expectant management of preeclampsia remote from term.27 It might have been anticipated that increasing use of expectant management would be associated with increases, rather than decreases, in maternal morbidity,28 because most practitioners await deteriorating maternal condition to precipitate the decision to deliver. We identified that women in the postintervention cohort admitted at less than 34+0 weeks of gestation had longer admission-to-delivery intervals than did those in the preintervention cohort, confirming our impression that local practice had changed. There was no change in adverse perinatal outcomes in the postintervention cohort (indeed the incidence of necrotizing enterocolitis was lower). Although there is the potential for a type II error, the trend toward a decrease in adverse perinatal outcome occurred in the postintervention cohort in which there was a lower gestational age at which the women were both admitted and delivered.

We were fortunate that the process of introducing a standardized pattern of assessment and surveillance for women admitted to a tertiary perinatal unit with either suspected or confirmed preeclampsia had the full support of the hospital administration and occurred through a stepwise process of feasibility study,15 education (of medical, nursing, administration, and clerical colleagues), ongoing surveillance of implementation, and review of outcomes.

It is possible that the apparent success of introducing the standing orders may have accrued from the fact that they were not accompanied by management guidelines from the outset; a group of competent providers, when asked to collect data did not feel intimidated but did intervene more appropriately when presented with a standardized data set. In comparison with the findings of Foy et al,6 who found that the introduction of a complex set of guidelines was not effective in either altering practice or standardizing care, we chose to address a single element of the management of women admitted with the hypertensive disorders of pregnancy, namely their laboratory assessment and ongoing surveillance. The Yorkshire guidelines, which were introduced to guide the management of, rather than surveillance of, women with severe preeclampsia, have also been associated with reduced levels of maternal morbidity and rates of both between-hospital transfers and intensive care admissions.29 Our experience with the standing orders is complementary to that of the Yorkshire group because our center is currently introducing management guidelines to the province of British Columbia in the context of a funded health services research project that will assess the manner of guideline introduction and the impact of those guidelines on outcomes across the province. These guidelines are based on those developed and introduced so successfully in Yorkshire and the standing orders. We believe that taking iterative steps will advance the quality of care more effectively than would trying to address all issues with a single large, and overwhelming, document addressing all aspects of care.

It is unclear what elements of the standing orders may have contributed to the fall in adverse maternal outcomes, although some have been identified through the retrospective study15 and by others.30 Certainly, before the introduction of the standing orders, the frequency and complexity of investigations varied between clinicians, as was predicted by our national review of practice.1 We recognize that the number of tests in the current regimen is greater than that which is standard in most units. The identification of those elements of this standardized approach that are truly predictive of adverse maternal outcomes is occurring through an international study to develop an outcome prediction model for women with preeclampsia, the PIERS (Preeclampsia Integrated Estimate of RiSk) model. Once the PIERS model has been established, then a reduced list of investigations will be suggested to replace the current list that we recognize is probably overly thorough and, therefore, expensive.

The pattern of investigations has standardized the approach within our unit. The choice of follow-up surveillance testing being on Mondays and Thursdays was made to improve the timing of the delivery of infants away from times of reduced pediatric staffing, especially for those remote from term.31 Of course, some or all of these investigations were performed at other additional times, at the discretion of the attending doctor or midwife; the influence of these “unscheduled” tests in the management of women with preeclampsia is a secondary outcome for the PIERS project.

A study limitation is that we do not have data on the eligible women who did not receive care using the standing orders during the postintervention phase of the study. In part, this is because we were aware of some women who were admitted with very severe preeclampsia and some end organ complications that evolved to become severe enough to fulfill the combined adverse maternal outcome. The physicians in these cases chose to write their own orders that almost matched the standing orders, but not fully. Therefore, we would have overly biased the analyses in favor of the standing orders.

In addition, we were underpowered to perform logistic regression analyses to determine the magnitude of any possible independent effect of the standing orders in influencing the change in outcomes. Although we have data on antihypertensive drug use in the retrospective cohort, we do not know the number of agents and duration of their use. Similarly, we do not have data on the rate of cesarean delivery in the preintervention cohort.

We recognize that the use of a preintervention and postintervention design is another significant limitation to this study. A better approach may have been to have randomized women to the use of guidelines or not. However, this methodology could not have been blinded, and we were concerned that the Hawthorne effect32 would have been profound because women not randomized to the guidelines may have received significantly more detailed care than did those women who received care in our unit before the introduction of the guidelines. We are also reassured through the knowledge that the women in the postintervention cohort were at a comparable, if not greater, baseline risk on admission and received a greater degree of expectant management (Table 1).

Therefore, we conclude that carefully introducing and implementing standardized initial assessment and ongoing surveillance of women admitted to our hospital with preeclampsia has been associated with a reduced incidence of adverse maternal outcomes.

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The other members of the PIERS (Preeclampsia Integrated Estimate of RiSk) Study Group are Joanne Douglas, Mark Ansermino, Keith Walley, James Russell, Jelena Maric, and Daniela Caprera (Vancouver, BC); Jean-Marie Moutquin and Annie Ouellet (Sherbrooke, Québec); Graeme Smith (Kingston, Ontario); Andrée Gruslin (Ottawa, Ontario); James Walker (Leeds, UK); Philippa Kyle and Peter Moore (Christchurch, NZ); and Barry Walters (Subiaco, Western Australia, Australia).

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© 2007 by The American College of Obstetricians and Gynecologists. Published by Wolters Kluwer Health, Inc. All rights reserved.