Influence of Patient Comorbidities on the Risk of Near-miss Maternal Morbidity or Mortality
Mhyre, Jill M. M.D.*; Bateman, Brian T. M.D.†; Leffert, Lisa R. M.D.†
Background: Maternal morbidity and mortality are increased in the United States compared with that of other developed countries. The objective of this investigation is to determine the extent to which it is possible to predict which patients will experience near-miss morbidity or mortality.
Methods: The authors defined near-miss morbidity as end-organ injury associated with length of stay greater than the 99th percentile or discharge to a second medical facility, and identified all cases of near-miss morbidity or death from admissions for delivery in the 2003–2006 Nationwide Inpatient Sample. Logistic regression was used to examine the effect of maternal characteristics on rates of near-miss morbidity/mortality.
Results: Approximately 1.3 per 1,000 hospitalizations for delivery was complicated by near-miss morbidity/mortality as defined in this study (95% CI 1.3–1.4). Most of these events (58.3%) occurred in 11.8% of the delivering population—in those women with important medical comorbidities or obstetric complications identified before admission for delivery. The highest rates were noted among women with pulmonary hypertension (98.0 cases per 1,000 deliveries), malignancy (23.4 per 1,000), and systemic lupus erythematosus (21.1 per 1,000).
Conclusions: Risk for near-miss morbidity or mortality is substantially increased among an identifiable subset of pregnant women. To the extent that antepartum multidisciplinary coordination and high-quality intrapartum care improve delivery outcomes for women with significant antepartum medical and obstetric disease, then public health investments to reduce the national burden of delivery-related near-miss morbidity and mortality will have the greatest effect by focusing resources on identifying and serving these high-risk groups.
What We Already Know about This Topic
* Maternal mortality is increasing in the United States, but the risk factors for maternal near-miss morbidity or mortality have not been well defined
What This Article Tells Us That Is New
* Using the 2003–2006 Nationwide Inpatient Sample, approximately 1.3 per 1,000 hospitalizations for delivery was complicated by near-miss morbidity or mortality
* Women with preexisting conditions or antenatal obstetric complications suffer the majority of these events
BOTH the Joint Commission and Amnesty International have recently called attention to the poor record of maternal patient safety in the United States.1
The maternal mortality ratio in the United States has been estimated to be as high as 17 deaths per 100,000 live births, and the rate of annual increase between 1998 and 2008 exceeded that of any other developed country.3
Multiple studies have suggested that nearly half of all pregnancy-related deaths are preventable with timely delivery of appropriate healthcare services.4–7
Although many maternal deaths are due to etiologies that are unpredictable, an increasing proportion of maternal deaths are attributed to preexisting disease.8
Both the extent to which maternal morbidity/mortality is concentrated in high-risk patients and the relative effect of specific preexisting conditions have not been well defined. This information is needed to evaluate the potential effect of public health investments to regionalize maternal health care, specifically to triage high-risk patients to regional centers with increased capacity to deliver intensive antepartum and peripartum care.
Even in the largest datasets, studies that focus on maternal mortality alone do not provide sufficient case numbers on which to conduct a detailed analysis of risks associated with preexisting conditions. We therefore chose to expand our analysis to include near-miss maternal morbidity as well as mortality. An obstetric “near-miss” occurs when a pregnant or recently postpartum woman survives a life-threatening event, either by chance or because of high-quality medical care.6
James Drife introduced this concept in 1993 when he called for an expansion of the United Kingdom Confidential Enquiry in Maternal Death to consider “near- miss” events to better elucidate the processes leading to adverse outcomes.10
Geller et al.
and Gregory et al.
incorporated this concept into their continuum of maternal delivery outcomes beginning with “ideal birth,” and progressing from some morbidity, to severe morbidity, to near-miss, and finally to maternal death.6
Definitions of near-miss morbidity have typically relied on either management-based criteria (e.g.
, intensive care unit admission,12–18
) or criteria available from chart review but not administrative data.9
Recently, the World Health Organization conducted a systematic review of studies of near-miss maternal morbidity and found that end-organ injury was a more specific and epidemiologically sound method to identify near-miss morbidity than were management-based criteria.21
Moreover, definitions based on chart review have limited utility in analyzing population-level predictors of near-miss maternal morbidity because this outcome is fortunately rare.
In our investigation, we develop an administrative data definition of near-miss maternal morbidity and define the extent to which preexisting maternal medical and obstetric conditions that are identifiable before the time of admission to the labor and delivery suite predict near-miss maternal morbidity or death.
Materials and Methods
Data were derived from the Nationwide Inpatient Sample (NIS), an administrative dataset that is maintained by the Agency for Healthcare Research and Quality as part of the Healthcare Cost and Utilization Project. The NIS is constructed to approximate a 20% stratified sample of non-Federal hospitals, and contains information on all acute care admissions from each of the sampled hospitals. Approximately 1,000 hospitals are selected for inclusion each year; sampling is based on five characteristics including ownership (e.g.
, investor owned, government, not-for-profit), bed size, teaching status, urban (vs.
rural) location, and geographic region, such that the sample is representative of all hospitalizations in the United States. Multiple data elements are included for each admission including patient age, race, admission source, assigned diagnosis-related group, disposition, and up to 15 diagnoses and procedures recorded using the International Classification of Diseases, Ninth Revision codes (ICD-9 CM).‡
Identification of Hospitalizations for Delivery
We queried all diagnosis, procedure, and diagnosis-related group fields using a modified version of the algorithm described by Kuklina et al
to identify all admissions for delivery in the NIS during 2003–2006. Hospitalizations were included if they had a diagnosis code or diagnosis-related groups indicating delivery or procedure codes related to delivery (e.g.
, forceps, breech extraction, vacuum extraction, version and extraction, manually assisted deliveries, episiotomy, hysterotomy, or cesarean delivery). Hospitalizations were excluded if they had diagnosis codes indicating hydatidiform mole, ectopic pregnancy, other abnormal products of conception, or procedure codes indicating abortion. We excluded hospitalizations in which the age of the patient was missing. The ICD-9 CM and diagnosis-related group codes used in selecting deliveries can be found in appendix 1.
Near-miss morbidity or death was the primary outcome of this analysis. We surveyed the literature23–25
and reviewed the ICD-9 CM manual to compile a list of severe, life-threatening complications representing end-organ injury that were relevant to an obstetric population. We then identified the presence of these complications in our cohort of delivering patients by querying all diagnosis fields using the appropriate ICD-9 CM codes (table 1
). The association of each of these complications with in-hospital death or discharge to a medical facility was then confirmed using univariate analysis (data not shown). One or more of each of these complications was present in 82.1% of in-hospital maternal deaths.
We defined near-miss morbidity as the presence of any of the complications listed in table 1
plus either a length of stay corresponding to the 99th
percentile for delivery-related hospitalization (i.e.
, greater than 7 days) or discharge to a facility other than home (i.e.
, short- term hospital, skilled nursing facility, intermediate care facility, or another type of healthcare facility).
From a survey of the published literature25–33
and clinical plausibility, we compiled a list of maternal medical and obstetric comorbidities that might act as risk factors for near-miss morbidity/mortality. We focused our analysis on preexisting conditions (comorbidities) rather than on complications of delivery and identified the presence of these conditions by querying all diagnosis fields using the ICD-9 CM codes listed in appendix 2.
Disposition after hospital discharge was missing in 213 records; these were assumed to be routine discharges to home, consistent with 97.3% of records. Length of stay was missing in 61 records; these were assumed to be less than 7 days, which is true of 99% of hospitalizations. Eleven states in 2003–2004 and nine states in 2005–2006 did not record or publically release data on patient race; race was coded as “Missing” when this data element was not available.
Bivariate analysis was initially completed with the entire dataset to detect an association between near-miss morbidity/mortality and the maternal characteristics shown in table 2
. Conditions that afflict 10 or fewer patients are not reported in accordance with the NIS Data Use Agreement, designed to prevent identification of individuals. Chronic congestive heart failure and history of pulmonary embolism were excluded from further analysis because the total number of patients was less than or equal to 10 in the delivering cohort. Categoric variables were compared using the chi-square test. The patient demographics and the preexisting condition variables shown in table 2
were then tested for collinearity. The variance inflation scores ranged from 1.0 to 1.25, with a mean of 1.03, and the maximum condition index was 3.78 and all variables were retained in subsequent analysis.
The dataset was then randomly split into an estimation dataset (70%) and a validation dataset (30%). Logistic regression analysis was then performed on the estimation dataset to identify independent predictors of near-miss morbidity/mortality. Initially all of the variables were included in the model. After the first step of model selection, variables with limited statistical significance (P > 0.1) or clinical significance (OR >0.9 and <1.1) were excluded and the model was refit. We did not consider interaction terms in the model. The model was tested for discrimination in both the estimation and validation dataset by calculating the area under the receiver operating curve.
Variable selection and univariate statistics were completed using SPSS version 17.0 (SPSS, Chicago, IL). Multivariate analysis was completed in Stata version 10.0, (Stata, College Station, TX).
Of the 3,463,327 maternal hospital admissions for delivery in the NIS for the years 2003–2006, we identified 4,550 hospitalizations (0.13%) that were complicated by a near-miss morbidity/mortality event. Of these, 3,996 patients (87.9%) remained in the hospital longer than 7 days, 775 (17.0%) were discharged or transferred to a medical facility, and 226 (5.8%) died during the delivery-hospitalization.
The most common complications, each occurring in approximately 20% of these patients, were disseminated intravascular coagulation/coagulopathy, acute liver disease, acute respiratory distress syndrome, and acute heart failure (table 1
). One or more of these complications was present in 68.4% (n = 3,112) of the patients.
shows the rates of various maternal demographic characteristics and comorbidities in the delivering cohort and the univariate association with near-miss morbidity/mortality. Women older than 34 yr and non-Hispanic black women are disproportionately represented among patients with near-miss morbidity/mortality. In addition, all tested conditions were significantly associated with this outcome, with the exception of spine abnormalities. Among women with near-miss morbidity/mortality, the most common comorbidities are hypertensive disorders of pregnancy (34.7%), previous cesarean delivery (15.7%), diabetes mellitus (10.5%), preexisting hypertension (10.2%), and multiple gestation (9.8%).
The rate of near-miss morbidity/mortality per 1,000 hospitalizations is increased with age older than 34 yr and nonwhite race (table 3
). Near-miss morbidity or mortality complicates close to 10% of deliveries in women with pulmonary hypertension and 2% or more deliveries in women with malignancy or systemic lupus erythematosus. This rate exceeds 1% for women with placenta previa, sickle cell disease, chronic renal disease, congenital heart disease, and human immunodeficiency virus.
All preexisting conditions listed in table 3
are independently associated with near-miss morbidity/mortality, with the exception of obesity and previous cesarean delivery.
Discrimination of the final logistic regression model was assessed in the estimation and validation samples by calculating the area under the receiver operating characteristic curve; this value was 0.79 and 0.78, respectively.
lists the discrimination characteristics for various thresholds to identify high-risk patients. An adjusted OR threshold of 3 has a sensitivity of 58.3%, meaning that most of all near-miss maternal morbidity or mortality events occurred in 11.8% of the delivering population—in those women who had least 1 of 15 conditions listed in table 3
with an adjusted OR of 3 or greater. Decreasing the adjusted OR threshold to 2 increases sensitivity to 69.4%, and encompasses an additional 10.2% of delivering women who were either ≥40 yr of age or of non-Hispanic black race, with no identifiable coexisting disease with an adjusted OR of 3 or greater. The remaining 78% of the delivering population did not have any of the identified risk factors with an adjusted OR of 2 or greater; these women experienced 30.6% of all near-miss maternal morbidity/mortality events, but individual risk was just 0.05% during each hospitalization for delivery.
Using the largest hospital discharge dataset available in the United States, we found that 1 in 760 hospitalizations for delivery is complicated by near-miss morbidity or mortality. We sought to determine the extent to which near-miss morbidity/mortality is concentrated in high-risk patients and found that most of these events occur in patients with high-risk conditions generally identifiable at the time of admission to the labor floor. This suggests a potential opportunity to improve maternal outcomes by triaging high-risk women to delivery centers with increased capacity to deliver intensive antepartum and peripartum care.
Previous population-level analyses have documented increased risk for severe maternal morbidity or mortality among those parturients admitted with malignancy,32
sickle cell disease,28
hypertensive disorders of pregnancy,31
chronic renal disease,25
chronic ischemic heart disease,25
congenital heart disease,25
systemic lupus erythematosus,25
human immunodeficiency virus,39
valvular heart disease,25
and diabetes mellitus.25
We used multivariate analysis to define the independent risk of near-miss morbidity/mortality associated with each of these conditions. High rates of substance abuse have been noted in inquiries of maternal death,47
and our analysis confirms a fourfold increased rate of near-miss morbidity/mortality among these women. Likewise, deaths attributed to asthma have been consistently identified by maternal mortality surveillance efforts,47
and asthma has been associated with other adverse obstetric outcomes including preeclampsia, chorioamnionitis, antepartum and postpartum hemorrhage, and cesarean delivery.48–51
Our study confirms an epidemiologic link between asthma and near-miss maternal morbidity or mortality.
In contrast with previous studies, neither obesity nor previous cesarean delivery predicted a near-miss maternal morbidity/mortality event in our multivariate analysis. Event rates were increased at least twofold among obese women; however, multivariate analysis suggests that coexisting medical disease rather than obesity per se
drives this relationship. Approximately 15% of the sample had a previous cesarean delivery, and while risk was increased approximately 10% in this group, the sample size was insufficient to confirm or refute an independent relationship in multivariate analysis. Nevertheless, previous cesarean delivery does increase risk for abnormal placentation,35
and placenta previa was a strong independent risk factor for near-miss morbidity/mortality.
Although smoking has been shown to increase a number of specific maternal risks, including myocardial infarction29
women who smoked had a slightly reduced risk of near-miss morbidity/mortality in the current study. Tobacco abuse has been shown to correlate with intrauterine growth restriction resulting in small head circumference for gestational age53
and with preterm birth, both of which may decrease probability of cesarean delivery and the increased risk of maternal complications that accompany it. In addition, smoking has been associated with reduced rates of preeclampsia in women younger than 30 yr without preexisting hypertension.54
Risk is increased among nonwhite women, but particularly among non-Hispanic black women. Multivariate adjustment for maternal age and preexisting conditions does little to attenuate this increase in risk. Although black race has been shown to predict a number of adverse maternal outcomes, including pregnancy-related death,8
the mechanism for this disparity is unknown and may involve maternal behavioral patterns, genetic predispositions, social circumstances, environmental exposures, and suboptimal medical care.57
Advancing maternal age is strongly associated with near-miss morbidity/mortality, consistent with previous reports.56
Compared with women age 20–34 yr, risk is increased twofold for women between 35 and 39 yr, and threefold for women aged 40 yr and older. Adjustment for all preexisting conditions considered in this analysis explains approximately 16% and 31% of this increased risk, respectively.
On the continuum of maternal delivery outcomes, near-miss lies between severe obstetric morbidity and maternal death.6
The delivery-related mortality rate in our study was 6.5 per 100,000 hospitalizations for delivery, comparable with rates recently reported elsewhere.5
This ratio is less than half of the maternal mortality ratio, which includes all deaths during any point in pregnancy or within 42 days of the end of pregnancy, and substantially less than the pregnancy-related maternal mortality ratio, which includes all deaths during any point in pregnancy or up to a full year after the termination of pregnancy.58
Severe obstetric morbidity includes a broader category of women who suffered major complications with delivery that were not necessarily associated with critical illness (e.g.
, blood transfusion). Previous analyses of population-level administrative data in the United States and Canada have used ICD-9 CM codes to identify those delivery-related hospitalizations that resulted in severe obstetric morbidity, and have reported incidences between 4.4 and 8.1 per 1,000 deliveries.23–25
Combining ICD-9 CM codes with a requirement for prolonged length of stay decreases the number of identified cases, presumably by improving specificity.23
Prolonged length of stay greater than the 90th
, length of stay more than 3 days) or discharge to a second health care facility has been used to enhance specificity to identify true cases with severe obstetric morbidity.23
Our current work builds on existing definitions of severe obstetric morbidity to capture near-miss maternal morbidity by requiring an ICD-9 CM code that designates end-organ injury, and by pairing this requirement with either a prolonged length of stay greater than the 99th percentile or discharge to a second medical facility. This new definition allowed us to query a dataset with close to 3.5 million hospitalization records, to identify a composite outcome of near-miss maternal morbidity or mortality, and to evaluate a long list of patient characteristics and comorbidities in a single multivariate model to predict these adverse outcomes as a whole.
Based on recent surveillance in the United States and the United Kingdom, complications of preexisting medical conditions appear to be the fastest rising category of maternal death.8
Our analysis confirms this observation; close to 60% of near-miss maternal morbidity or mortality events are concentrated in approximately 10% of women with medical or obstetric conditions known at the time of admission to the labor and delivery unit. As such, targeted regionalization, specifically, triaging high-risk patients to regional centers with increased capacity to deliver intensive antepartum and peripartum care, may be a viable public health strategy to improve maternal delivery outcomes in the United States.
Similarly, The American Congress of Obstetricians and Gynecologists and the National Institutes of Health have called for regional networks structured around referral centers that provide a safe environment for women to undertake a trial of labor after cesarean delivery.63
Centers with resources to support these trials of labor could be the same centers with enhanced capacity to care for women with significant preexisting disease. Services in these regional centers may already or could be expanded to include antepartum consultations to maternal-fetal medicine specialists, anesthesiologists, cardiologists, and other specialists as needed, multidisciplinary coordination to optimize the delivery plan, around-the-clock dedicated in-house obstetric and anesthesia and intensive care services, an on-site blood bank for women with conditions that increase risk for hemorrhage, and interventional radiology. Delivery in a regional center with a multidisciplinary care team has recently been shown to reduce morbidity among women with placenta accreta64
and morbidity and mortality among women who underwent peripartum hysterectomy.65
The list of high-risk conditions in table 3
and the risk thresholds in table 4
could be used as a triage tool for individual facilities. For example, nonhospital birth centers and small delivery centers with limited capacity to provide around-the-clock services might use thresholds to decide on their level of acceptable risk, and consequently the characteristics of the pregnant population they are safely able to serve. Obstetric health care providers working within the targeted regional centers could also use this tool, in this case to identify those patients who may benefit from closer antenatal scrutiny and referrals for multidisciplinary antepartum consultation and coordination.
Despite the significant potential applications, several limitations are inherent in this analysis. We were unable to confirm the severity of conditions by using medical records. The conditions listed in table 3
were considered to be preexisting, but the data are cross-sectional, and a present-on-admission flag is not available to confirm antepartum diagnosis. Specific ICD-9 CM codes do not exist for many conditions of interest, including placenta accreta and antepartum cesarean delivery. In addition, the NIS has insufficient power to evaluate certain rare conditions, such as cystic fibrosis and chronic congestive heart failure. Existing codes may not reliably be applied if the consequences for billing are minor, and therefore common conditions such as obesity are typically not well coded.
In conclusion, we found that risk for near-miss maternal morbidity or mortality is substantially increased among a subset of pregnant women who can be identified before admission for delivery. Existing clinical studies suggest that for many of these conditions, antepartum multidisciplinary coordination and careful delivery planning and implementation can improve outcomes for these high-risk patients. Future investigations are needed to define the extent of hospital-level variation in near-miss maternal morbidity/mortality and the potential effect of targeted regionalization to triage high-risk patients to facilities with the capacity to provide high acuity antepartum and peripartum care.
The authors thank the Health Care Utilization Project partners who contributed data to the Nationwide Inpatient Sample. The list is available at www.hcup-us.ahrq.gov/db/hcupdatapartners.jsp
(accessed July 6, 2011).
‡ Information on the dataset is available at http://www.hcup-us.ahrq.gov/nisoverview.jsp
. Accessed June 1, 2010. Cited Here...
1. Joint Commission on Accreditation of Healthcare Organizations: Preventing maternal death. Sentinel Event Alert 2010; 1–4
2. Deadly Delivery: The Maternal Health Care Crisis in the USA. London, UK: Amnesty International, 2010
3. Hogan MC, Foreman KJ, Naghavi M, Ahn SY, Wang M, Makela SM, Lopez AD, Lozano R, Murray CJ: Maternal mortality for 181 countries, 1980–2008: A systematic analysis of progress towards Millennium Development Goal 5. Lancet 2010; 375:1609–23
4. Berg CJ, Harper MA, Atkinson SM, Bell EA, Brown HL, Hage ML, Mitra AG, Moise KJ Jr, Callaghan WM: Preventability of pregnancy-related deaths: Results of a state-wide review. Obstet Gynecol 2005; 106:1228–34
5. Clark SL, Belfort MA, Dildy GA, Herbst MA, Meyers JA, Hankins GD: Maternal death in the 21st century: Causes, prevention, and relationship to cesarean delivery. Am J Obstet Gynecol 2008; 199:36.e1–5; discussion 91–2.e7–11
6. Geller SE, Rosenberg D, Cox SM, Brown ML, Simonson L, Driscoll CA, Kilpatrick SJ: The continuum of maternal morbidity and mortality: Factors associated with severity. Am J Obstet Gynecol 2004; 191:939–44
7. Kilpatrick SJ, Crabtree KE, Kemp A, Geller S: Preventability of maternal deaths: Comparison between Zambian and American referral hospitals. Obstet Gynecol 2002; 100:321–6
8. Berg CJ, Callaghan WM, Syverson C, Henderson Z: Pregnancy-related mortality in the United States, 1998 to 2005. Obstet Gynecol 2010; 116:1302–9
9. Mantel GD, Buchmann E, Rees H, Pattinson RC: Severe acute maternal morbidity: A pilot study of a definition for a near-miss. Br J Obstet Gynaecol 1998; 105:985–90
10. Drife JO: Maternal “near miss” reports? BMJ 1993; 307:1087–8
11. Gregory KD, Fridman M, Shah S, Korst LM: Global measures of quality- and patient safety-related childbirth outcomes: Should we monitor adverse or ideal rates? Am J Obstet Gynecol 2009; 200:681.e1–7
12. Baskett TF, Sternadel J: Maternal intensive care and near-miss mortality in obstetrics. Br J Obstet Gynaecol 1998; 105:981–4
13. Bouvier-Colle MH, Ould El Joud D, Varnoux N, Goffinet F, Alexander S, Bayoumeu F, Beaumont E, Fernandez H, Lansac J, Lvy G, Palot M: Evaluation of the quality of care for severe obstetrical haemorrhage in three French regions. BJOG 2001; 108:898–903
14. Bouvier-Colle MH, Salanave B, Ancel PY, Varnoux N, Fernandez H, Papiernik E, Brart G, Benhamou D, Boutroy P, Caillier I, Dumoulin M, Fournet P, Elhassani M, Puech F, Poutot C: Obstetric patients treated in intensive care units and maternal mortality. Eur J Obstet Gynecol Reprod Biol 1996; 65:121–5
15. Bouvier-Colle MH, Varnoux N, Brart G: Maternal deaths and substandard care: The results of a confidential survey in France. Medical Experts Committee. Eur J Obstet Gynecol Reprod Biol 1995; 58:3–7
16. Kilpatrick SJ, Matthay MA: Obstetric patients requiring critical care: A five-year review. Chest 1992; 101:1407–12
17. Mahutte NG, Murphy-Kaulbeck L, Le Q, Solomon J, Benjamin A, Boyd ME: Obstetric admissions to the intensive care unit. Obstet Gynecol 1999; 94:263–6
18. Wheatley E, Farkas A, Watson D: Obstetric admissions to an intensive therapy unit. Int J Obstet Anesth 1996; 5:221–4
19. Geller SE, Rosenberg D, Cox S, Brown M, Simonson L, Kilpatrick S: A scoring system identified near-miss maternal morbidity during pregnancy. J Clin Epidemiol 2004; 57:716–20
20. Reichenheim ME, Zylbersztajn F, Moraes CL, Lobato G: Severe acute obstetric morbidity (near-miss): A review of the relative use of its diagnostic indicators. Arch Gynecol Obstet 2009; 280:337–43
21. Say L, Pattinson RC, Gulmezoglu AM: WHO systematic review of maternal morbidity and mortality: The prevalence of severe acute maternal morbidity (near miss). Reprod Health 2004; 1:3
22. Kuklina EV, Whiteman MK, Hillis SD, Jamieson DJ, Meikle SF, Posner SF, Marchbanks PA: An enhanced method for identifying obstetric deliveries: Implications for estimating maternal morbidity. Matern Child Health J 2008; 12:469–77
23. Callaghan WM, Mackay AP, Berg CJ: Identification of severe maternal morbidity during delivery hospitalizations, United States, 1991–2003. Am J Obstet Gynecol 2008; 199:133.e1–8
24. Kuklina EV, Meikle SF, Jamieson DJ, Whiteman MK, Barfield WD, Hillis SD, Posner SF: Severe obstetric morbidity in the United States: 1998–2005. Obstet Gynecol 2009; 113:293–9
25. Wen SW, Huang L, Liston R, Heaman M, Baskett T, Rusen ID, Joseph KS, Kramer MS, Maternal Health Study Group, Canadian Perinatal Surveillance System: Severe maternal morbidity in Canada, 1991–2001. CMAJ 2005; 173:759–64
26. Berg CJ, Mackay AP, Qin C, Callaghan WM: Overview of maternal morbidity during hospitalization for labor and delivery in the United States: 1993–1997 and 2001–2005. Obstet Gynecol 2009; 113:1075–81
27. Clowse ME, Jamison M, Myers E, James AH: A national study of the complications of lupus in pregnancy. Am J Obstet Gynecol 2008; 199:127.e1–6
28. James AH, Bushnell CD, Jamison MG, Myers ER: Incidence and risk factors for stroke in pregnancy and the puerperium. Obstet Gynecol 2005; 106:509–16
29. James AH, Jamison MG, Biswas MS, Brancazio LR, Swamy GK, Myers ER: Acute myocardial infarction in pregnancy: A United States population-based study. Circulation 2006; 113:1564–71
30. James AH, Jamison MG, Brancazio LR, Myers ER: Venous thromboembolism during pregnancy and the postpartum period: Incidence, risk factors, and mortality. Am J Obstet Gynecol 2006; 194:1311–5
31. Kuklina EV, Ayala C, Callaghan WM: Hypertensive disorders and severe obstetric morbidity in the United States. Obstet Gynecol 2009; 113:1299–306
32. Smith LH, Dalrymple JL, Leiserowitz GS, Danielsen B, Gilbert WM: Obstetrical deliveries associated with maternal malignancy in California, 1992 through 1997. Am J Obstet Gynecol 2001; 184:1504–12; discussion 1512–3
33. Villers MS, Jamison MG, De Castro LM, James AH: Morbidity associated with sickle cell disease in pregnancy. Am J Obstet Gynecol 2008; 199:125.e1–5
34. Olive EC, Roberts CL, Algert CS, Morris JM: Placenta praevia: Maternal morbidity and place of birth. Aust N Z J Obstet Gynaecol 2005; 45:499–504
35. Rosenberg T, Pariente G, Sergienko R, Wiznitzer A, Sheiner E: Critical analysis of risk factors and outcome of placenta previa. Arch Gynecol Obstet 2011; 284:47–51
36. Silver RM, Landon MB, Rouse DJ, Leveno KJ, Spong CY, Thom EA, Moawad AH, Caritis SN, Harper M, Wapner RJ, Sorokin Y, Miodovnik M, Carpenter M, Peaceman AM, O'Sullivan MJ, Sibai B, Langer O, Thorp JM, Ramin SM, Mercer BM, National Institute of Child Health and Human Development Maternal-Fetal Medicine Units Network: Maternal morbidity associated with multiple repeat cesarean deliveries. Obstet Gynecol 2006; 107:1226–32
37. Zhang J, Meikle S, Trumble A: Severe maternal morbidity associated with hypertensive disorders in pregnancy in the United States. Hypertens Pregnancy 2003; 22:203–12
38. Kuklina E, Callaghan W: Chronic heart disease and severe obstetric morbidity among hospitalisations for pregnancy in the USA: 1995–2006. BJOG 2011; 118:345–52
39. Fiore S, Newell ML, Thorne C, European HIV in Obstetrics Group: Higher rates of post-partum complications in HIV-infected than in uninfected women irrespective of mode of delivery. AIDS 2004; 18:933–8
40. Louis J, Landon MB, Gersnoviez RJ, Leveno KJ, Spong CY, Rouse DJ, Moawad AH, Varner MW, Caritis SN, Harper M, Wapner RJ, Miodovnik M, Carpenter M, Peaceman AM, O'Sullivan MJ, Sibai BM, Langer O, Thorp JM, Ramin SM, Mercer BM, Maternal-Fetal Medicine Units Network, National Institute of Child Health and Human Development: Perioperative morbidity and mortality among human immunodeficiency virus infected women undergoing cesarean delivery. Obstet Gynecol 2007; 110:385–90
41. Conde-Agudelo A, Belizán JM, Lindmark G: Maternal morbidity and mortality associated with multiple gestations. Obstet Gynecol 2000; 95:899–904
42. Little CM: One consequence of infertility treatment: Multifetal pregnancy. MCN Am J Matern Nurs 2010; 35:150–5
43. Luke B, Brown MB: Maternal morbidity and infant death in twin versus
triplet and quadruplet pregnancies. Am J Obstet Gynecol 2008; 198:401.e1–10
44. MacKay AP, Berg CJ, King JC, Duran C, Chang J: Pregnancy-related mortality among women with multifetal pregnancies. Obstet Gynecol 2006; 107:563–8
45. Porreco RP, Barkey R: Peripartum intensive care. J Matern Fetal Neonatal Med 2010; 23:1136–8
46. Walker MC, Murphy KE, Pan S, Yang Q, Wen SW: Adverse maternal outcomes in multifetal pregnancies. BJOG 2004; 111:1294–6
47. Miles J: Substance misuse. In Lewis G, ed. The Confidential Enquiry into Maternal and Child Health (CEMACH). Saving mothers' lives: Reviewing maternal deaths to make motherhood safer—2003–2005. The Seventh Report on Confidential Enquiries into Maternal Deaths in the United Kingdom. London: CEMACH, 2007; 165–72
48. Demissie K, Breckenridge MB, Rhoads GG: Infant and maternal outcomes in the pregnancies of asthmatic women. Am J Respir Crit Care Med 1998; 158:1091–5
49. Enriquez R, Griffin MR, Carroll KN, Wu P, Cooper WO, Gebretsadik T, Dupont WD, Mitchel EF, Hartert TV: Effect of maternal asthma and asthma control on pregnancy and perinatal outcomes. J Allergy Clin Immunol 2007; 120:625–30
50. Liu S, Wen SW, Demissie K, Marcoux S, Kramer MS: Maternal asthma and pregnancy outcomes: A retrospective cohort study. Am J Obstet Gynecol 2001; 184:90–6
51. Wen SW, Demissie K, Liu S: Adverse outcomes in pregnancies of asthmatic women: Results from a Canadian population. Ann Epidemiol 2001; 11:7–12
52. Bauer ST, Bonanno C: Abnormal placentation. Semin Perinatol 2009; 33:88–96
53. Källén K: Maternal smoking during pregnancy and infant head circumference at birth. Early Hum Dev 2000; 58:197–204
54. Conde-Agudelo A, Althabe F, Belizn JM, Kafury-Goeta AC: Cigarette smoking during pregnancy and risk of preeclampsia: A systematic review. Am J Obstet Gynecol 1999; 181:1026–35
55. Engel SM, Janevic TM, Stein CR, Savitz DA: Maternal smoking, preeclampsia, and infant health outcomes in New York City, 1995–2003. Am J Epidemiol 2009; 169:33–40
56. Rosenberg D, Geller SE, Studee L, Cox SM: Disparities in mortality among high risk pregnant women in Illinois: A population based study. Ann Epidemiol 2006; 16:26–32
57. Bryant AS, Worjoloh A, Caughey AB, Washington AE: Racial/ethnic disparities in obstetric outcomes and care: Prevalence and determinants. Am J Obstet Gynecol 2010; 202:335–43
58. Main EK: Maternal mortality: New strategies for measurement and prevention. Curr Opin Obstet Gynecol 2010; 22:511–6
59. Callaghan WM, Berg CJ: Pregnancy-related mortality among women aged 35 years and older, United States, 1991–1997. Obstet Gynecol 2003; 102:1015–21
60. Luke B, Brown MB: Contemporary risks of maternal morbidity and adverse outcomes with increasing maternal age and plurality. Fertil Steril 2007; 88:283–93
61. Needleman J, Minnick AF: Anesthesia provider model, hospital resources, and maternal outcomes. Health Serv Res 2009; 44:464–82
62. Cantwell R, Clutton-Brock T, Cooper G, Dawson A, Drife J, Garrod D, Harper A, Hulbert D, Lucas S, McClure J, Millward-Sadler H, Neilson J, Nelson-Piercy C, Norman J, O'Herlihy C, Oates M, Shakespeare J, de Swiet M, Williamson C, Beale V, Knight M, Lennox C, Miller A, Parmar D, Rogers J, Springett A: Saving Mothers' Lives: Reviewing maternal deaths to make motherhood safer: 2006–08. The Eighth Report of the Confidential Enquiries into Maternal Deaths in the United Kingdom. BJOG 2011; 118 Suppl 1:1–203
63. National Institutes of Health Consensus Development Conference Panel: National Institutes of Health Consensus Development conference statement: Vaginal birth after cesarean: New insights March 8–10, 2010. Obstet Gynecol 2010; 115:1279–95
64. Eller AG, Bennett MA, Sharshiner M, Masheter C, Soisson AP, Dodson M, Silver RM: Maternal morbidity in cases of placenta accreta managed by a multidisciplinary care team compared with standard obstetric care. Obstet Gynecol 2011; 117:331–7
65. Wright JD, Herzog TJ, Shah M, Bonanno C, Lewin SN, Cleary K, Simpson LL, Gaddipati S, Sun X, D'Alton ME, Devine P: Regionalization of care for obstetric hemorrhage and its effect on maternal mortality. Obstet Gynecol 2010; 115:1194–200
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