Abstract
Background:
Postpartum hemorrhage (PPH) is the leading preventable cause of maternal mortality. Most PPH cases are caused by uterine atony, which is inconsistently defined in clinical care. The electronic health record was used to prompt communication between the anesthesia and obstetric care teams about uterine tone using a validated 11-point numeric rating scale (NRS) at 0, 5, and 10 min after placental delivery for all cesarean deliveries at our institution. The primary hypothesis was that lower uterine tone NRS would be strongly associated with progression to major PPH.
Methods:
This was a single-center, prospective observational study conducted over a 1-yr period. The primary predictor was the 0 to 10 uterine tone NRS recorded 10 min after placental delivery, and the primary outcome was major PPH, defined as quantitative blood loss greater than or equal to 1,500 ml. Area under the receiver operating characteristic curves were created, and the relative risk of major PPH for each 1-point change in the tone score was estimated. Key secondary outcomes analyzed included associations between tone scores, PPH, and blood transfusion.
Results:
A total of 1,599 consecutive cesarean deliveries were performed by obstetricians from academic (39.3%), county public health (21.1%), and private practice (38.8%) services. Major PPH complicated 9.9% and transfusion 6.7% of cesarean deliveries. Uterine tone NRS was documented at 0 min after placental delivery in 91.6%, 5 min in 97.4%, and 10 min in 97.0% of cesarean deliveries. The 10-min NRS was a strong predictor of major PPH, with an area under the receiver operating characteristic of 0.78 (95% CI, 0.73 to 0.82). Each 1-point decrease in NRS increased the risk of major PPH by 71% (95% CI, 0.58 to 0.86). A 10-min uterine tone NRS less than or equal to 6 had high positive predictive value for major PPH (32.9%), as well as PPH (64.2%) and transfusion (20.6%).
Conclusions:
Standardized uterine tone assessments on a 0 to 10 scale are feasible to implement and strongly associated with progression to major PPH and blood transfusion. Future studies should investigate whether implementation of PPH interventions based on uterine tone NRS can reduce major PPH and hemorrhage-associated morbidity.
Standardized assessments of uterine tone on a 0 to 10 scale are feasible and easy to implement using electronic anesthesia record–triggered alert. The dynamic interactions between the obstetric and anesthesia teams allow the care team to assess and document uterine tone promptly and reliably. The uterine tone scores are strongly associated with the progression to postpartum hemorrhage and the need for blood transfusion.
Editor’s Perspective
What We Already Know about This Topic
Postpartum hemorrhage is the leading preventable cause of maternal mortality, and the majority of all postpartum hemorrhage results from uterine atony.
Existing risk stratification tools for postpartum hemorrhage focus on clinical risk factors but have not been validated.
The 0 to 10 numeric rating scale for uterine tone has been developed with good to excellent inter-rater reliability. However, its clinical implications and performance have not yet been validated.
What This Article Tells Us That Is New
Standardized assessments of uterine tone on a 0 to 10 scale are feasible and easy to implement using electronic anesthesia record–triggered alert.
The dynamic interactions between the obstetric and anesthesia teams allow the care team to assess and document uterine tone promptly and reliably.
The uterine tone scores are strongly associated with the progression to postpartum hemorrhage and the need for blood transfusion.
Postpartum hemorrhage (PPH) is the leading preventable cause of maternal mortality worldwide.1,2 The majority (79%) of all PPH results from uterine atony, defined as inadequate uterine contraction to compress bleeding from the placental bed after delivery.3 At term, the normal rate of blood flow to the uterus is approximately 600 to 700 ml/min; as such, unrecognized or untreated uterine atony can lead to rapid PPH.4,5 Risk stratification tools for PPH from organizations such as the California Maternal Quality Care Collaborative (CMQCC) and the Association of Women’s Health, Obstetric and Neonatal Nurses focus on clinical risk factors; however, most patients who hemorrhage due to uterine atony lack clinically identifiable risk factors.3,6–9 Additionally, few studies have assessed the degree of uterine atony; most instead categorize atony as a binary yes or no. Given the limitations of current PPH risk stratification, high vigilance and early recognition of uterine atony are essential for all patients.
Uterine atony lacks a standardized clinical assessment tool. During cesarean deliveries, the management of uterine atony requires close communication between the obstetrician performing delivery and the anesthesia care team. Several qualitative and quantitative tools have been used in clinical research to report uterine tone during cesarean delivery including 0 to 10 scales, “unsatisfactory” versus “satisfactory,” “A” to “F” grading scales, and 0 to 100 scales.10–17 Recently, Cole et al.18 demonstrated the validity of the 0 to 10 numeric rating scale (NRS) for uterine tone, in which the obstetrician palpates the fundus of the uterus and rates the adequacy of uterine contraction tone from 0 (flaccid and atonic) to 10 (optimal) during cesarean delivery. The scale had high interrater agreement and reliability; however, the relationship between uterine NRS scores and clinically relevant PPH outcomes have not yet been defined.
To fill this knowledge gap and address delayed recognition of uterine atony, we implemented the 0 to 10 NRS assessment for all cesarean deliveries at our institution as a quality improvement initiative. We leveraged the electronic health record (EHR) to prompt the anesthesiologist to discuss tone with the obstetrician and record a uterine tone NRS score at three time points (0, 5, and 10 min after placental delivery). We prospectively studied whether the uterine tone NRS served as an early indicator of hemorrhage. Our primary hypothesis was that lower uterine tone NRS by 10 min after placental delivery would be strongly associated with major PPH, defined as quantitative blood loss (QBL) greater than or equal to 1,500 ml. Our secondary aim was to identify an optimal uterine tone cut-point NRS score with high positive predictive value for major PPH. We also explored the relationship between tone scores and PPH defined as QBL greater than or equal to 1,000 ml, blood transfusion, and uterine atony treatments and interventions.
Materials and Methods
This single-center, prospective observational study included all cesarean deliveries performed in the labor and delivery unit of Lucile Packard Children’s Hospital Stanford, a tertiary care academic center, over a 1-yr timespan. This study included scheduled, urgent, and emergent cesarean deliveries conducted under neuraxial or general anesthesia during the study period with no exclusions. The study protocol was reviewed by Stanford University’s institutional review board and granted a waiver of informed consent (institutional review board approval no. 62584, approved September 23, 2021). The predefined primary clinical outcome was major PPH with QBL greater than or equal to 1,500 ml.
Uterine Tone NRS
Beginning February 1, 2022, as a quality improvement initiative to address delayed recognition of poor uterine tone contributing to PPH, the obstetric anesthesia team implemented standardized assessments of the uterine tone using a validated 0 to 10 NRS scale for all cesarean deliveries.18 The NRS score is assigned by the operating obstetrician by palpating the uterine fundus after delivery. This scale requires minimal education; the only instruction provided is that 0 represents a completely flaccid, atonic uterus and 10 represents a firmly contracted uterus (fig. 1A). All obstetricians and anesthesiologists were provided standardized education through a system-wide email, as well as laminated information on the door to each operating theater on how to assess the uterine tone using the NRS tool.
Fig. 1.
Uterine tone assessments embedded in the electronic health record. (A) Infographic depicting uterine tone numerical rating scale (NRS) assessment at 0, 5, and 10 min after placental delivery. The figure was created with BioRender.com. (B) Appearance of the Epic electronic health record best practice alerts windows that prompt the anesthesiologist to record uterine tone scores at 0, 5, and 10 min after placental delivery.
Uterine tone scores were requested using the EHR. The anesthesia information management system module in the Epic (USA) EHR allows time-based intraoperative reminders with triggers based on event markers known as best practice alerts. In this case, a “Uterine Tone Score” alert was tied to the “Baby Delivered” event documented in real-time during every cesarean delivery. A pop-up link prompted the anesthesiologist to enter the uterine tone score (fig. 1B).
To determine optimal timing of these best practice alerts, 40 sequential cesarean deliveries were observed before implementation of the system. Placental delivery was completed greater than 1 min but less than 2 min from the time of fetal delivery in 39 of 40 cesarean deliveries. The hysterotomy was closed but fascia not yet closed 12 min after fetal delivery in 35 of 40 cases. As such, alert intervals of 2, 7, and 12 min after fetal delivery, corresponding to 0, 5, 10 min after placental delivery, were selected.
Quantitative Blood Loss
QBL was measured by labor and delivery nurses trained by online modules followed by five-case proctoring for all cesarean deliveries at the study institution beginning in 2020 as a standard of care. QBL is measured by a combination of volumetric assessment—suction canister contents, subtracting all irrigant and amniotic fluid volume—and gravimetric assessment—weight of all saturated surgical sponges, towels, and pads subtracting dry weights.19
Primary Outcome
Major PPH, defined as QBL in the operating room greater than or equal to 1,500 ml, was the predefined primary outcome. This outcome is consistent with the CMQCC definition of “massive hemorrhage” that necessitates early and aggressive clinical management to reduce major maternal morbidity and mortality.20 We chose this outcome rather than PPH with blood loss greater than or equal to 1,000 ml, because we noted a high incidence of cases meeting this threshold without clinical consequence after our institution began using QBL methodology in 2020. Our institutional data from 2020 to 2021 indicated that major PPH with QBL greater than or equal to 1,500 ml complicated approximately 10% of cesarean deliveries.
Mechanical or Surgical Interventions for Uterine Atony
Mechanical or surgical interventions for uterine atony included any of the following: intrauterine balloon or suction device placement (i.e., Bakri or Jada device placement), uterine compression sutures (B-lynch), blood vessel embolization by interventional radiology, and/or hysterectomy.
Nonatonic Contributors to Bleeding
Documented nonatonic contributors to bleeding were defined as descriptions in the formal operative report of any of the following: hysterotomy extension; atypical hysterotomy type (including classical, T- or J-shaped, or mid-transverse uterine incision); bleeding from a low-lying placental bed; bleeding fibroids; “extensive,” “dense,” or “significant” adhesive disease; uterine rupture; placenta accreta; and/or vaginal or cervical lacerations.
Data Collection
Basic demographic and obstetric data, as well as the primary predictor (uterine tone score) and outcome (derived from QBL) were imported directly from the EHR as documented and unchanged. Other patient characteristics including comorbid medical conditions, indication for cesarean delivery, causes of bleeding during cesarean delivery, units of blood transfusion, surgical interventions for atony, and intensive care admission were obtained by physician chart review due to inconsistent coding in the electronic health record. All data were recorded in the secure REDCap platform (https://redcap.stanford.edu), operated by the Stanford Medicine Research Information Technology team. The REDCap platform services at Stanford are subsidized by (1) the Stanford School of Medicine Research Office and (2) the National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health, through grant No. UL1 TR001085.
Institutional Practices, Oxytocin, and Uterotonics
Standard institutional practice includes an oxytocin bolus at the time of fetal delivery (1 unit for scheduled, low-risk cesarean delivery and 2 units for high-risk or intrapartum cases) followed by initiation of an oxytocin infusion at 7.5 units/h for low-risk and 15 units/h for high-risk or intrapartum cesarean deliveries. Poor initial tone is treated with an additional 2-unit oxytocin bolus and sequential increase of the oxytocin infusion to 15 or 30 units/h. Second-line uterotonic agents are administered in cases of poor response to up-titration of oxytocin, preferentially methylergonovine (0.2 mg) intramuscularly followed by carboprost (250 μg) intramuscularly in the absence of contraindications. Misoprostol is used infrequently in cases of contraindications to both methylergonovine and carboprost or insufficient response to those agents. Tranexamic acid (1 g) is administered if excessive bleeding is noted, greater than or equal to 1,500 ml QBL, or at the time of first unit of blood transfusion in the operating room.
Statistical Analysis
For the primary outcome of major PPH, receiver operating characteristic curves (ROCs) were generated and the area under the ROC curve (AUROC) was calculated using R version 4.2.2, “Innocent and Trusting,” and statistical package “ROCR.”21 All other statistical analyses were conducted using SAS (USA) statistical software, release 3.81 (Enterprise edition). Relative risk of major PPH and 95% CI were estimated using a generalized linear model and Poisson regression with robust standard errors. Predicted risks of severe PPH based on uterine tone NRS were obtained using the equation [E(Y)] = exp[β0 + β1(NRS)] and the β values from the regression model. To address the hypothesis that the uterine tone NRS would specifically predict progression to major PPH due to uterine atony, sensitivity analyses were conducted excluding cases with documented nonatonic bleeding.
These same models were applied for exploration of other relationships with binary outcomes including 0- and 5-min tone scores as predictors and PPH (QBL greater than or equal to 1,000 ml), packed erythrocyte transfusion, and medical and surgical interventions for uterine atony as outcomes. After log-transforming the QBL to approximate a normal distribution,22 the relationship between QBL and uterine tone score was assessed by linear regression, as well as Pearson’s correlation.
Cut points for uterine tone scores were selected based on analysis of the ROC curves and selection of an inflection point or elbow at which incremental detection of true positive cases decreased and false-positive cases increased. This inflection point was generally identified as the closest point to the upper left corner of the graph as described.23 The positive predictive value of the cut point was determined by calculating the incidence of PPH outcomes among patients at or below the selected cut point score. A separate cut point was selected for strong negative predictive value, identified as the lowest score in a horizontal plateau in the ROC curve.
Multivariable Regression Models
To assess the performance of the uterine tone NRS relative to classic clinical risk factors for PPH, we compared the ROC curve from a single-variable model with only uterine tone NRS to two multivariable models: (1) a multivariable model including clinical risk factors and uterine tone NRS and (2) a multivariable model including only clinical risk factors (without uterine tone NRS). The following clinical risk factors were included in multivariable models: extremes of maternal age (teen pregnancy and maternal age greater than 35 yr as variables), race/ethnicity, previous cesarean delivery, pre-eclampsia, insulin-requiring diabetes, pregnancy conceived by in vitro fertilization, suspected fetal macrosomia, polyhydramnios, multiple gestation, placenta previa, oxytocin exposure in labor, chorioamnionitis, placental abruption, maternal anticoagulant therapy, coagulopathy with predelivery fibrinogen less than 200, or thrombocytopenia with platelets less than 100,000.
As an exploratory analysis to assess the contribution of change in uterine tone NRS over time to hemorrhage risk assessment, we also generated multivariable regression models for severe PPH with the following independent variables: absolute value of uterine tone score, change in uterine tone score from the previous assessment, and an interaction term. We compared AUROC values and assessed the magnitude and significance of β values for these variables in our regression models.
The influence of the obstetrician rater upon the uterine tone score was assessed by linear regression with the 10-min uterine tone score as an outcome and obstetrician rater as a categorical predictor. To address the confounder of case-mix based on patient population, the model was adjusted for obstetric service (academic, county, or private). Obstetricians with fewer than 4 cesarean deliveries during the 1-yr study period were omitted from this analysis.
Sample Size
Based on historic data from 2019 and 2020, our institution conducted approximately 1,500 cesarean deliveries per year, complicated by 150 major PPHs with QBL greater than or equal to 1,500 ml. We estimate that a sample of 1,300 deliveries would be sufficient to demonstrate an AUROC of 0.75 (assumptions: major PPH incidence 0.1, CI width of 0.1, and 95% confidence). As such, we conducted 1 yr of prospective data entry to obtain a sufficient sample size.
Results
Over the study period from February 1, 2022, to January 31, 2023, 1,599 cesarean deliveries were performed by 77 attending obstetricians from a mix of academic high-risk, county public health, and private practice services (table 1). PPH and major PPH complicated 31.9% and 9.9% of all deliveries, respectively (tables 2 and 3). Potential nonatonic contributors to bleeding were documented in 33.4% of operative reports.
Table 1.
Descriptive Characteristics of the Study Population
| Characteristic | Value |
|---|---|
| No. of subjects | N = 1,599 |
| Median age | 34 [31–37] yr |
| Age | |
| < 20 yr | 33 (2.1%) |
| 20–29 yr | 297 (18.6%) |
| 30–34 yr | 533 (33.3%) |
| 35–39 yr | 545 (34.1%) |
| ≥ 40 yr | 191 (11.9%) |
| Height (cm) | 161.1 ± 7.5 |
| Weight (kg) | 80.1 ± 17.8 |
| Median body mass index | 29.6 [26.4–34.1] kg/m2 |
| Body mass index | |
| < 25 kg/m2 | 261 (16.3%) |
| 25–29 kg/m2 | 594 (37.1%) |
| 30–39 kg/m2 | 622 (38.9%) |
| 40–49 kg/m2 | 104 (6.5%) |
| ≥ 50 kg/m2 | 18 (1.1%) |
| Race/ethnicity | |
| Asian | 528 (33.0%) |
| Hispanic | 500 (31.3%) |
| Non-Hispanic black | 47 (2.9%) |
| Non-Hispanic white | 383 (24.0%) |
| Other/declined to state | 141 (8.8%) |
| Obstetric service | |
| Academic/high-risk | 629 (39.3%) |
| County public health | 337 (21.1%) |
| Private practice | 621 (38.8%) |
| Other/declined to state | 12 (0.8%) |
| Gestational age | |
| < 28 weeks | 32 (2.0%) |
| 28–33 weeks | 95 (5.9%) |
| 34–36 weeks | 195 (12.2%) |
| 37–38 weeks | 437 (27.3%) |
| 39 weeks | 607 (38.0%) |
| ≥ 40 weeks | 233 (14.6%) |
| No. of previous cesarean deliveries | |
| 0 | 969 (60.6%) |
| 1 | 451(28.2%) |
| 2 | 147 (9.2%) |
| 3 or more | 24 (1.5%) |
| Indication for cesarean | |
| Scheduled | 477 (29.8%) |
| Planned for cesarean but presented with maternal or fetal indication before | 534 (33.4%) |
| Intrapartum | 563 (35.2%) |
| Maternal comorbidities | |
| Diabetes (gestational or pre-existing) | 368 (23.0%) |
| Insulin use | 171 (10.7%) |
| Pre-eclampsia | 310 (19.4%) |
| Magnesium infusion | 163 (10.2%) |
| Chorioamnionitis | 95 (6.0%) |
| Oxytocin infusion before cesarean | 498 (31.1%) |
| Suspected macrosomia | 94 (5.9%) |
| Multiple gestation | 71 (4.4%) |
| Polyhydramnios | 49 (3.1%) |
| Abruption | 44 (2.8%) |
| Coagulopathy | 12 (0.8%) |
| Thrombocytopenia | 18 (1.1%) |
| IVF pregnancy | 225 (14.1%) |
| Tubal ligation performed with caesarean | 179 (11.2%) |
The values are displayed as means ± SD, median [interquartile range], or N (%).
IVF, in vitro fertilization.
Table 2.
Predictor Characteristics of the Study Population
| Predictor (Uterine Tone NRS) | N (%) | ||
|---|---|---|---|
| Assessment 10 min after Placental Delivery | Assessment 5 min after Placental Delivery | Assessment 0 min after Placental Delivery | |
| ≤ 4 | 36 (2.3%) | 82 (5.1%) | 280 (17.5%) |
| 5 | 63 (3.9%) | 131 (8.2%) | 196 (12.3%) |
| 6 | 141 (8.8%) | 234 (14.6%) | 329 (20.6%) |
| 7 | 312 (19.5%) | 390 (24.4%) | 353 (22.1%) |
| 8 | 521 (32.6%) | 494 (30.9%) | 232 (14.5%) |
| 9 | 393 (24.6%) | 183 (11.4%) | 64 (4.0%) |
| 10 | 85 (5.3%) | 44 (2.8%) | 10 (0.6%) |
| Missing | 48 (3.0%) | 41 (2.6%) | 135 (8.4%) |
NRS, numeric rating score (0 to 10).
Table 3.
Outcome Characteristics of the Study Population
| Outcome | Values (N = 1,599) |
|---|---|
| Quantitative blood loss | 800 [588–1,106] |
| < 500 ml | 240 (15.0%) |
| 500–999 ml | 843 (52.7%) |
| 1,000–1,500 ml | 358 (22.4%) |
| > 1,500 ml | 158 (9.9%) |
| Missing | 2 (0.1%) |
| Transfusion | |
| Yes | 107 (6.7%) |
| No | 1,490 (93.3%) |
| Additional oxytocin boluses | |
| Any | 634 (39.8%) |
| Second-line uterotonics | |
| Any | 319 (20.0%) |
| Methylergonovine | 259 (16.3%) |
| Carboprost | 131 (8.2%) |
| Misoprostol | 42 (2.6%) |
| Surgical intervention | |
| Any | 49 (3.1%) |
| Intrauterine compression balloon or suction device | 36 (2.3%) |
| Uterine compression sutures (B-lynch) | 23 (1.4%) |
| Embolization by interventional radiology | 4 (0.3%) |
| Hysterectomy | 8 (0.5%) |
| Potential nonatonic contributors to bleeding in patients with major PPH (N = 100) | |
| Adherent placenta (accreta) | 6 (6.0%) |
| Fibroids/leiomyomas | 25 (25.0%) |
| Surgical causes of bleeding | 76 (76.0%) |
| Low-lying placental bleeding | 23 (23.0%) |
| Vaginal or cervical lacerations | 10 (10.0%) |
| Frequency of PPH cases with documented nonatonic bleeding (N = 254) | |
| Adherent placenta (accreta) | 10 (3.9%) |
| Fibroids | 54 (21.3%) |
| Surgical causes of bleeding | 193 (76.0%) |
| Lower-segment bleeding | 55 (21.7%) |
| Vaginal lacerations | 11 (4.3%) |
The values are displayed as median [interquartile range] or N (%). Potential causes of nonatonic bleeding were determined by physician chart review of the obstetrician’s operative report. Surgical causes of bleeding were defined as hysterotomy extensions, bleeding from the hysterotomy site, “extensive” or “dense” adhesions, or vertical, J- or T-shaped, or high-transverse uterine incision. Many patients had more than one cause of nonatonic bleeding.
Major PPH, primary outcome, defined as quantitative blood loss at delivery greater than or equal to 1,500 ml; PPH, postpartum hemorrhage.
Uterine Tone Scores
Uterine tone NRS was recorded in 91.6% of deliveries at 0 min, 97.4% at 5 min, and 97.0% at 10 min after placental delivery (tables 2 and 3). In 70.7% of patients, uterine tone NRS increased over time. Mean ± SD uterine tone NRS was 6.03 ± 1.81 at the time of placental delivery and 7.75 ± 1.35 by 10 min after placental delivery. The 10- and 5-min uterine tone NRS correlated strongly (r = 0.71, P < 0.0001). A uterine tone NRS value of 10 was infrequent at all timepoints. The distributions of uterine tone scores in various patient and obstetric populations are provided in supplemental figure 1 (https://links.lww.com/ALN/D930).
Primary Outcome
The 10-min uterine tone NRS was strongly associated with major PPH, with an AUROC of 0.78 (table 4; fig. 2; P < 0.0001). In sensitivity analysis excluding potential cases of nonatonic bleeding, the AUROC improved to 0.81 (supplemental table 1, https://links.lww.com/ALN/D937; supplemental fig. 2, https://links.lww.com/ALN/D931). There was a 71% (95% CI, 58 to 86%) increased risk of major PPH for each 1-point decrease in uterine tone NRS at 10 min after placental delivery (table 4). For example, using this model, a patient with a 10-min uterine tone NRS score of 7 has a 10.3% risk of severe PPH, a patient with a score of 6 has a risk of 17.7%, and a patient with a score of 5 has a risk of 30.3%.
Table 4.
Relative Risks and AUROC Curves for Patient Outcomes
| Uterine Tone NRS Timing Relative to Placental Delivery | Outcome | Relative Risk (95% CI) |
AUROC (95% CI) |
|---|---|---|---|
| 10 min after (N = 1,551) | Major PPH | 1.71 (1.58 to 1.86) | 0.78 (0.73 to 0.82) |
| PPH | 1.39 (1.32 to 1.46) | 0.72 (0.69 to 0.74) | |
| Transfusion | 1.69 (1.53 to 1.87) | 0.75 (0.69 to 0.80) | |
| Second-line uterotonic | 1.68 (1.59 to 1.78) | 0.81 (0.79 to 0.84) | |
| Surgical intervention | 2.16 (1.88 to 2.48) | 0.87 (0.81 to 0.93) | |
| 5 min after (N = 1,558) | Major PPH | 1.52 (1.40 to 1.65) | 0.72 (0.68 to 0.77) |
| PPH | 1.30 (1.24 to 1.37) | 0.69 (0.66 to 0.72) | |
| Transfusion | 1.44 (1.30 to 1.60) | 0.68 (0.62 to 0.74) | |
| Second-line uterotonic | 1.60 (1.51 to 1.69) | 0.81 (0.79 to 0.84) | |
| Surgical intervention | 1.76 (1.53 to 2.01) | 0.79 (0.71 to 0.87) | |
| 0 min (N = 1,464) | Major PPH | 1.30 (1.20 to 1.41) | 0.66 (0.61 to 0.71) |
| PPH | 1.20 (1.15 to 1.26) | 0.66 (0.63 to 0.69) | |
| Transfusion | 1.31 (1.18 to 1.46) | 0.65 (0.58 to 0.71) | |
| Second-line uterotonic | 1.48 (1.41 to 1.57) | 0.79 (0.76 to 0.82) | |
| Surgical intervention | 1.45 (1.26 to 1.66) | 0.73 (0.65 to 0.81) |
Second-line uterotonic was defined as methylergonovine, carboprost, or misoprostol administration in the 24 h after delivery. Surgical intervention was defined as an intrauterine suction or balloon compression device, external uterine compression sutures, interventional radiologic embolization, or hysterectomy procedure in the 24 h after delivery. The relative risk of outcomes and 95% CI were calculated for each 1-point decrease in uterine tone score. AUROCs were calculated using unadjusted regression models with all patients included and the uterine tone NRS score as the univariate predictor. P < 0.0001 for all.
AUROC, area under the receiver operating characteristic curve; Major PPH, primary outcome, quantitative blood loss at delivery greater than or equal to 1,500 ml; NRS, numeric rating scale (0 to 10); PPH, postpartum hemorrhage.
Fig. 2.
Relationship between uterine tone numerical rating scale (NRS) and hemorrhage outcomes. (A) Hemorrhage outcomes by uterine tone NRS score 10 min after placental delivery. Postpartum hemorrhage (PPH) is defined as quantitative blood loss (QBL) greater than or equal to 1,000 ml. Major PPH is defined as QBL greater than or equal to 1,500 ml. Transfusion is defined as transfusion of at least one unit of packed red blood cells before hospital discharge. An asterisk (*) denotes the primary outcome, major PPH. (B) Receiver operating characteristic (ROC) curves for uterine tone scores and major postpartum hemorrhage. Separate curves are shown for 10-, 5-, and 0-min postplacental uterine tone NRS as the predictor and major PPH with QBL greater than or equal to 1,500 ml as the outcome. The yellow boxes highlight the cut point scores selected for table 3. (C) Predicted quantitative blood loss per 10-min uterine tone NRS. Predicted blood loss was generated from a generalized linear model fitting log-transformed QBL as the outcome and 10-min uterine tone NRS as the single-variable predictor. AUROC, area under the receiver operating characteristic curve.
Key Secondary Outcomes
The 10-min uterine tone NRS was also strongly associated with PPH and blood transfusion (fig. 2; table 4; supplemental fig. 3, https://links.lww.com/ALN/D932; supplemental fig. 4, https://links.lww.com/ALN/D933; P < 0.0001). Uterine tone NRS collected 0 and 5 min after placental delivery were also significantly related to PPH, major PPH, and transfusion, although less strongly than the 10-min score (table 4).
We found moderate negative correlation between 10-min uterine tone NRS and QBL at delivery (r = −0.42, P < 0.0001), which was similar in magnitude to the correlation between change in hematocrit and QBL (r = 0.41, P < 0.001). Lower uterine tone scores predicted higher QBL (fig. 2C).
Cut Points
A 10-min uterine tone NRS of less than or equal to 6 had high positive predictive value for PPH, major PPH, and transfusion (table 5). At the earlier uterine tone assessment times (0 and 5 min after placental delivery), lower cut point scores of less than or equal to 4 and less than or equal to 5, respectively, also predicted hemorrhage outcomes (table 5). Conversely, a uterine tone NRS greater than or equal to 8 at any timepoint had high negative predictive value of greater than 95% for major PPH and transfusion (table 5), suggesting that no further assessments are likely required if this threshold is achieved in an early assessment. Additional cut points and their positive and negative predictive values can be found in supplemental table 2 (https://links.lww.com/ALN/D938).
Table 5.
Positive and Negative Predictive Values for Select Uterine Tone Cut Points Determined by Receiver Operating Characteristic Curves
| Timing of Uterine Tone NRS | N (%) | PPH | Major PPH | Transfusion |
|---|---|---|---|---|
| Positive Predictive Value, % | ||||
| NRS ≤ 6 at 10 min after placental delivery | 288 (18.0) | 64.2 | 32.9 | 20.6 |
| NRS ≤ 5 at 5 min after placental delivery | 254 (15.9) | 58.3 | 27.2 | 17.9 |
| NRS ≤ 4 at 0 min after placental delivery | 415 (26.0) | 49.4 | 18.3 | 14.5 |
| Negative Predictive Value, % | ||||
| NRS ≥ 8 | ||||
| 10 min after placental delivery | 999 (62.5) | 79.6 | 96.2 | 97.1 |
| 5 min after placental delivery | 721 (45.1) | 82.3 | 96.4 | 96.8 |
| 0 min after placental delivery | 306 (19.1) | 79.7 | 95.1 | 96.1 |
The table shows the positive predictive and negative predictive values for all possible cut points provided in supplemental table 2 (https://links.lww.com/ALN/D938).
Major PPH, quantitative blood loss ≥ 1500 ml; NRS, numeric rating score (0 to 10); PPH, postpartum hemorrhage (quantitative blood loss ≥ 1000 ml)
Relationship to Medical and Surgical Interventions for Uterine Atony
Of all patients (n = 319), 20% received a second-line uterotonic, and 3.1% (n = 49) received mechanical or surgical intervention for uterine atony. Lower uterine tone NRS at all three measured timepoints were strongly associated with medical and surgical interventions for uterine atony (table 4; fig. 3, A to C; supplemental fig. 5, https://links.lww.com/ALN/D934).
Fig. 3.
Relationship between uterine tone numerical rating scale (NRS) and medical and surgical interventions for uterine atony. (A) Uterine atony intervention outcomes by 10-min postplacental uterine tone NRS score. (B) Uterine atony intervention outcomes by 5-min postplacental uterine tone NRS score. (C) Uterine atony intervention outcome by 0-min postplacental uterine tone NRS score. Extra oxytocin was defined as an additional bolus dose of 1 to 3 units of oxytocin after the initial, prophylactic postdelivery bolus. Second-line uterotonic was defined as misoprostol, methylergonovine, or carboprost administration after fetal delivery. Surgical intervention was defined as an intrauterine compression balloon (i.e., Bakri), intrauterine suction device (i.e., Jada), uterine compression sutures (i.e., B-lynch sutures), interventional radiology embolization procedure, or hysterectomy.
Multivariable Models of Severe PPH
A multivariable model of severe PPH incorporating 16 clinical risk factors associated with PPH and the 10-min NRS score only marginally increased the AUROC from 0.78 (single-variable model with only 10-min NRS) to 0.81 (multivariable model). A multivariable model using clinical risk factors without the uterine tone NRS had a lower AUROC of 0.70 (supplemental fig. 6, https://links.lww.com/ALN/D935). A separate multivariable model incorporating the uterine tone score and the change in uterine tone score over time did not significantly improve model performance.
Inter-rater Variability of Uterine Tone Scores
The attending obstetrician accounted for only 13.5% (P < 0.001) of the variability in 10-min uterine tone score after adjusting for the case mix by practice type. In contrast, 20.9% (P < 0.001) of variance in QBL at delivery was attributed to the attending obstetrician after adjusting for the case mix.
Etiologies of Major PPH
Overlapping etiologies of major PPH are shown in figure 4. Uterine atony and surgical bleeding, mostly due to hysterotomy extension, frequently co-occurred in patients with major PPH, as well as PPH (supplemental fig. 7, https://links.lww.com/ALN/D936).
Fig. 4.
Exploration of contributing etiologies of major postpartum hemorrhage (PPH). (A) Uterine atony and nonatonic bleeding. Uterine atony was defined at a 10-min uterine tone numeric rating score (NRS) less than or equal to 6. Major PPH was defined as quantitative blood loss greater than or equal to 1,500 ml. Nonatonic bleeding was defined by physician review of the written operative report narrative including any of the following: hysterotomy extension; atypical hysterotomy type (including classical, T- or J-shaped, or mid-transverse uterine incision); bleeding fibroids; “extensive,” “dense,” or “significant” adhesive disease; bleeding from a low-lying placental bed (i.e., placenta previa, uterine rupture, placenta accreta); or vaginal or cervical lacerations. (B) Etiologies of bleeding in patients with major PPH. Uterine atony was defined at a 10-min uterine tone NRS less than or equal to 6. The “other” category included bleeding from fibroids/leiomyomas (n = 25), abnormally adherent placenta (placenta accreta, n = 6), or vaginal or cervical lacerations (n = 10).
Discussion
In this study, we show that serial uterine tone NRS assessments are feasible to implement in clinical practice for all cesarean deliveries and serve as robust early indicators of progression to major PPH with QBL greater than or equal to 1,500 ml and transfusion. To our knowledge, this is the first large scale implementation of a uterine tone scoring system.
PPH is the leading cause globally of maternal mortality and of severe maternal morbidity in the United States.1 Rates of PPH continue to rise year after year, with increased incidence of uterine atony paralleling increases in PPH.24 Maternal mortality due to PPH is largely considered preventable through early recognition and management.1,5 However, early recognition of uterine atony requires a culture of clear communication between the anesthesia and obstetric teams. Our study provides novel evidence that EHR embedding of uterine tone NRS prompts is a low-cost, low-risk intervention that may facilitate early recognition of uterine atony and associated PPH.
As a secondary aim of our study, we identified that a 10-min uterine tone score less than or equal to 6 has high positive predictive value for PPH, major PPH, and blood transfusion (table 5). At our institution, we have used this cut-point score to trigger practical interventions including ensuring that the attending anesthesiologist is present in the operating room, maximizing medical treatment with oxytocin and second-line uterotonics, placing additional intravenous access, and sending a blood type and cross-match if not already obtained. We have noted that the uterine tone NRS system fosters multidisciplinary communication and heightened awareness of uterine atony and PPH on both sides of the surgical drape, even outside the EHR-triggered intervals. Since terminating data collection for this study, the obstetric anesthesia and obstetrics groups overwhelmingly favored continuing standardized uterine tone NRS assessments for all cesarean deliveries at our institution.
High vigilance and early recognition of PPH are essential considering the poor performance of even the most sophisticated and widely adopted clinical risk stratification systems. Numerous organizations including the CMQCC, the Association of Women’s Health, Obstetric and Neonatal Nurses, and the American College of Obstetricians and Gynecologists Safe Mother Initiative have published PPH risk prediction tools based on predelivery clinical characteristics.7,8,25,26 However, validation studies consistently demonstrate disappointing positive and negative predictive values for patient risk categories. For example, a patient designated as “high risk” for PPH based on the CMQCC model only had a positive predictive value of 10.0% for PPH and 1.0% for transfusion.7,26 In contrast, our study demonstrated that 10-min tone scores less than or equal to 6 had positive predictive values of 64.2% for PPH and 20.6% for transfusion.
Tools such as the uterine tone NRS that aide in early PPH detection may add significant value to current practice centered on predelivery risk stratification. Because a uterine tone NRS is only available once a delivery is underway, clinical risk prediction remains important for predelivery decision-making regarding delivery location, resources, and personnel. Interestingly, in our data set, a multivariable regression model incorporating 16 clinical risk factors underperformed significantly compared to a single-variable model using only the 10-min uterine tone NRS as a predictor of severe PPH. Adding all 16 clinical risk factors into the uterine tone NRS model only marginally improved the area under the ROC curve at the cost of significant added complexity (supplemental fig. 6, https://links.lww.com/ALN/D935). It will be interesting to assess whether integration of uterine tone NRS into predictive algorithms can be used to generate dynamic PPH risk predictions available to clinicians in real time.
The strengths of the current study include its novelty, simplicity, generalizability, automated approach, and prospective design. In addition, this data set was obtained through hundreds of hours of physician chart review of operative report and chart documentation narratives, providing a granular, more nuanced landscape of the causes of major PPH in patients undergoing cesarean delivery than a study reliant on International Classification of Diseases coding (fig. 4). The uterine tone NRS assessment triggered by the EHR serves as a simple, single-variable predictor of progression to major PPH. We conducted this study at a center that serves academic high-risk, county public health, and private practice obstetric practices without significant differences in performance, proving generalizability to a wide variety of clinical practice settings. We believe that this system can easily be translated to low-resource settings, even those without an automated EHR alerting system, where patients suffer disproportionate PPH-related morbidity and mortality and may benefit most from early detection.
We noted one unexpected finding in our study: a small increase in PPH, major PPH, and transfusion among patients with a 10-min uterine tone NRS of 10 as compared to 8 or 9 (fig. 2A). NRS scores of 10 were relatively infrequent. Our clinical experience has been that when a score of 10 is provided by an obstetrician dealing with ongoing nonatonic bleeding, for example due to brisk blood loss from a hysterotomy extension, the obstetrician must communicate definitively to the anesthesiologist that “we do not have a tone problem here [but do have bleeding].” This finding merits further exploration in future studies.
This study is not without potential limitations. These are observational data, and we have not yet determined whether the act of assigning uterine tone NRS scores meaningfully changes patient outcomes. As an additional limitation, the 10-min uterine tone score may not be generalizable to practice settings with shorter operative times. If the fascia is closed within 10 min of placental delivery, fundal palpation for a 10-min uterine NRS would not be feasible. Anticipating this limitation in generalizability to other settings, we provided all outcomes, as well as positive and negative predictive values for uterine tone NRS collected 0 and 5 min after delivery (table 5; supplemental table 2, https://links.lww.com/ALN/D938). We hope that providing full data at the earlier assessment times are helpful to centers with shorter surgical duration that may consider implementing this tool.
Another potential limitation to generalizability is our high rates of PPH (31.9%), major PPH (9.9%), and transfusion (6.7%). This is likely explained by the use of the QBL methodology in a center that serves a large high-risk patient population; these rates are in line with several contemporary publications using QBL, as opposed to estimated blood loss, at academic centers.27–29 For example, nearly identical rates of PPH of 37% have been reported by Chang et al.28 at the University of Calgary. In the recent large multicenter trial out of the Maternal−Fetal Medicine Units Network, 4.3% of cesarean delivery patients required a blood transfusion;30 in another recent case-control study, Rottenstreich et al.27 reported an overall 4.7% transfusion rate.
As a final limitation of our study, the uterine tone NRS score only directly captures PPH resulting from uterine atony. As depicted in figure 4, other overlapping etiologies frequently contribute to PPH. However, while a uterine tone NRS system may not directly capture phenomena such as hysterotomy bleeding or bleeding from a low-lying placental bed, we have observed that it indirectly facilitates early communication between the obstetric and anesthesia teams regarding these other etiologies of PPH.
In the future, we plan to study whether the implementation of standardized uterine tone NRS assessment changes patient outcomes. We hypothesize that shorter time to uterotonic administration and earlier implementation of PPH bundles will decrease blood loss and morbidity among patients with uterine atony. Future work could also combine the uterine tone NRS with other existing PPH risk prediction tools to create a real-time dynamic assessment of PPH risk for a patient undergoing a cesarean delivery. In summary, EHR-driven uterine tone NRS assessments are feasible to implement in standard clinical care and serve as strong early indicators of progression to major PPH and transfusion. This novel, simple system fosters communication between obstetricians and anesthesia care teams and can be easily applied to varied practice settings.
Research Support
Supported by the Stanford Maternal and Child Health Research Institute (Stanford, California) Clinician Educator Award (to Dr. Ansari).
Competing Interests
Dr. Deirdre Lyell has been a consultant to Bloomlife (San Francisco, California) and a stock investor to ZenFlow (San Francisco, California) and receives royalties from UpToDate. The other authors declare no competing interests.
Supplemental Digital Content
Supplemental Fig. 1. Uterine tone NRS in various patient populations, https://links.lww.com/ALN/D930
Supplemental Fig. 2. ROC curves for severe hemorrhage excluding non-atonic bleeding, https://links.lww.com/ALN/D931
Supplemental Fig. 3. ROC curves for postpartum hemorrhage, https://links.lww.com/ALN/D932
Supplemental Fig. 4. ROC curves for transfusion, https://links.lww.com/ALN/D933
Supplemental Fig. 5. ROC curves for PPH interventions, https://links.lww.com/ALN/D934
Supplemental Fig. 6. Multivariable models for severe hemorrhage, https://links.lww.com/ALN/D935
Supplemental Fig. 7. Etiologies of postpartum hemorrhage, https://links.lww.com/ALN/D936
Supplementary Table 1. https://links.lww.com/ALN/D937
Supplementary Table 2. https://links.lww.com/ALN/D938
Supplementary Material
Abbreviations:
- AUROC
- area under the receiver operating characteristic curve
- CMQCC
- California Maternal Quality Care Collaborative
- EHR
- electronic health record
- NRS
- numeric rating scale
- PPH
- postpartum hemorrhage
- QBL
- quantitative blood loss
- ROC
- receiver operating characteristic curve
Published online first on April 11, 2025.
The article processing charge was funded by the Stanford University Department of Anesthesiology, Perioperative and Pain Medicine.
This article is featured in “This Month in Anesthesiology,” page A1.
This article is accompanied by an editorial on p. 4.
Supplemental Digital Content is available for this article. Direct URL citations appear in the printed text and are available in both the HTML and PDF versions of this article. Links to the digital files are provided in the HTML text of this article on the Journal’s Web site (www.anesthesiology.org).
Part of the work presented in this article has been presented at Society of Obstetric Anesthesia and Perinatology Annual Conference in New Orleans, Louisiana, May 3 to 7, 2023, and at the American Society of Anesthesiologists Annual Conference in San Francisco, California, October 13 to 17, 2023.
Contributor Information
Natalie J. Koons, Email: nkoons@stanford.edu.
Chloe Stanwyck, Email: chloestanwyck@stanford.edu.
James J. Xie, Email: jxie@stanford.edu.
Guillermina Michel, Email: gmichel5@stanford.edu.
Deirdre J. Lyell, Email: dlyell@stanford.edu.
Brendan Carvalho, Email: carvalb@stanford.edu.
Brian T. Bateman, Email: bbateman@stanford.edu.
Jessica R. Ansari, Email: jansari@stanford.edu.
References
- 1.Say L, Chou D, Gemmill A, et al. : Global causes of maternal death: A WHO systematic analysis. Lancet Glob Health 2014; 2:e323–33. doi:10.1016/S2214-109X(14)70227-X [DOI] [PubMed] [Google Scholar]
- 2.Committee on Practice Bulletins-Obstetrics: Practice bulletin no. 183: Postpartum hemorrhage. Obstet Gynecol 2017; 130:e168–86. doi:10.1097/AOG.0000000000002351 [DOI] [PubMed] [Google Scholar]
- 3.Bateman BT, Berman MF, Riley LE, Leffert LR: The epidemiology of postpartum hemorrhage in a large, nationwide sample of deliveries. Anesth Analg 2010; 110:1368–73. doi:10.1213/ANE.0b013e3181d74898 [DOI] [PubMed] [Google Scholar]
- 4.Wang Y, Zhao S: Vascular biology of the placenta. San Rafael, California, Morgan & Claypool Life Sciences, 2010. Available at: https://www.ncbi.nlm.nih.gov/books/NBK53254/. Accessed October 11, 2024. [PubMed] [Google Scholar]
- 5.Bienstock JL, Eke AC, Hueppchen NA.: Postpartum hemorrhage. N Engl J Med 2021; 384:1635–45. doi:10.1056/NEJMra1513247 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Ende HB, Lozada MJ, Chestnut DH, et al. : Risk factors for atonic postpartum hemorrhage: A systematic review and meta-analysis. Obstet Gynecol 2021; 137:305–23. doi:10.1097/AOG.0000000000004228 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Association of Women’s Health, Obstetric and Neonatal Nurses: Postpartum hemorrhage (PPH) risk assessment table. 2017. Available at: https://cdn-links.lww.com/permalink/aog/b/aog_134_6_2019_10_06_kawakita_19-1065_sdc2.pdf. Accessed December 9, 2024. [Google Scholar]
- 8.American College of Obstetricians and Gynecologists: Safe motherhood initiative obstetric hemorrhage bundle risk assessment table. 2019. Available at: https://www.acog.org/-/media/project/acog/acogorg/files/forms/districts/smi-ob-hemorrhage-bundle-slides.pdf?rev=419dbda68d694d5d8c3aba4e21014be7. Accessed October 8, 2024. [Google Scholar]
- 9.Rouse DJ, Leindecker S, Landon M, et al. ; National Institute of Child Health and Human Development Maternal–Fetal Medicine Units Network: The MFMU Cesarean Registry: Uterine atony after primary cesarean delivery. Am J Obstet Gynecol 2005; 193:1056–60. doi:10.1016/j.ajog.2005.07.077 [DOI] [PubMed] [Google Scholar]
- 10.Kovacheva VP, Soens MA, Tsen LC: A randomized, double-blinded trial of a “rule of threes” algorithm versus continuous infusion of oxytocin during elective cesarean delivery. Anesthesiology 2015; 123:92–100. doi:10.1097/ALN.0000000000000682 [DOI] [PubMed] [Google Scholar]
- 11.Ansari JR, Kalariya N, Carvalho B, Flood P, Guo N, Riley E: Calcium chloride for the prevention of uterine atony during cesarean delivery: A pilot randomized controlled trial and pharmacokinetic study. J Clin Anesth 2022; 80:110796. doi:10.1016/j.jclinane.2022.110796 [DOI] [PubMed] [Google Scholar]
- 12.El Tahan MR, Warda OM, Rashad A, et al. : Effects of preoperative sublingual misoprostol on uterine tone during isoflurane anesthesia for cesarean section. Rev Bras Anestesiol 2012; 62:625–35. doi:10.1016/S0034-7094(12)70162-9 [DOI] [PubMed] [Google Scholar]
- 13.Sarna MC, Soni AK, Gomez M, Oriol NE: Intravenous oxytocin in patients undergoing elective cesarean section. Anesth Analg 1997; 84:753–6. doi:10.1097/00000539-199704000-00010 [DOI] [PubMed] [Google Scholar]
- 14.Ghaly RG, Flynn RJ, Moore J: Isoflurane as an alternative to halothane for caesarean section. Anaesthesia 1988; 43:5–7. doi:10.1111/j.1365-2044.1988.tb05412.x [DOI] [PubMed] [Google Scholar]
- 15.Butwick AJ, Coleman L, Cohen SE, Riley ET, Carvalho B: Minimum effective bolus dose of oxytocin during elective Caesarean delivery. Br J Anaesth 2010; 104:338–43. doi:10.1093/bja/aeq004 [DOI] [PubMed] [Google Scholar]
- 16.Farber MK, Schultz R, Lugo L, Liu X, Huang C, Tsen LC: The effect of co-administration of intravenous calcium chloride and oxytocin on maternal hemodynamics and uterine tone following cesarean delivery: A double-blinded, randomized, placebo-controlled trial. Int J Obstet Anesth 2015; 24:217–24. doi:10.1016/j.ijoa.2015.03.007 [DOI] [PubMed] [Google Scholar]
- 17.Tabl S, Balki M, Downey K, et al. : Uterotonics in elective caesarean delivery: A randomised non-inferiority study comparing carbetocin 20 μg and 100 μg. Anaesthesia 2019; 74:190–6. doi:10.1111/anae.14480 [DOI] [PubMed] [Google Scholar]
- 18.Cole NM, Abushoshah I, Fields KG, et al. : The interrater reliability and agreement of a 0 to 10 uterine tone score in cesarean delivery. Am J Obstet Gynecol MFM 2021; 3:100342. doi:10.1016/j.ajogmf.2021.100342 [DOI] [PubMed] [Google Scholar]
- 19.Quantitative blood loss in obstetric hemorrhage: ACOG Committee opinion, number 794. Obstet Gynecol 2019; 134:e150–6. doi:10.1097/AOG.0000000000003564 [DOI] [PubMed] [Google Scholar]
- 20.Main EK, Cape V, Abreo A, et al. : Reduction of severe maternal morbidity from hemorrhage using a state perinatal quality collaborative. Am J Obstet Gynecol 2017; 216:298.e1–11. doi:10.1016/j.ajog.2017.01.017 [DOI] [PubMed] [Google Scholar]
- 21.Sing T, Sander O, Beerenwinkel N, Lengauer T: ROCR: Visualizing classifier performance in R. Bioinformatics 2005; 21:3940–1. doi:10.1093/bioinformatics/bti623 [DOI] [PubMed] [Google Scholar]
- 22.Carvalho JFD, Piaggio G, Wojdyla D, Widmer M, Gülmezoglu AM: Distribution of postpartum blood loss: Modeling, estimation and application to clinical trials. Reprod Health 2018; 15:199. doi:10.1186/s12978-018-0641-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Habibzadeh F, Habibzadeh P, Yadollahie M: On determining the most appropriate test cut-off value: The case of tests with continuous results. Biochem Med 2016; 26:297–307. doi:10.11613/BM.2016.034 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Corbetta-Rastelli CM, Friedman AM, Sobhani NC, Arditi B, Goffman D, Wen T: Postpartum hemorrhage trends and outcomes in the United States, 2000–2019. Obstet Gynecol 2023; 141:152–61. doi:10.1097/AOG.0000000000004972 [DOI] [PubMed] [Google Scholar]
- 25.Ende HB: Risk assessment tools to predict postpartum hemorrhage. Best Pract Res Clin Anaesthesiol 2022; 36:341–8. doi:10.1016/j.bpa.2022.08.003 [DOI] [PubMed] [Google Scholar]
- 26.Bingham D, Lyndon A, Lagrew D, Main EK: A state-wide obstetric hemorrhage quality improvement initiative. MCN Am J Matern Child Nurs 2011; 36:297–304. doi:10.1097/NMC.0b013e318227c75f [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Rottenstreich A, Regev N, Levin G, et al. : Factors associated with postcesarean blood transfusion: A case control study. J Matern Fetal Neonatal Med 2022; 35:495–502. doi:10.1080/14767058.2020.1724945 [DOI] [PubMed] [Google Scholar]
- 28.Chang D, Papalia N, Cooper S: Obstetrical blood loss by mode of delivery utilizing qualitative methods: Redefining normal. J Obstet Gynaecol Can 2020; 42:671. doi:10.1016/j.jogc.2020.02.031 [Google Scholar]
- 29.Donahue AP, Beckham J, Edwards J: Postoperative anemia requiring intervention following cesarean delivery—Who should be screened? Am J Obstet Gynecol 2022; 226:S322. doi:10.1016/j.ajog.2021.11.542 [Google Scholar]
- 30.Pacheco LD, Clifton RG, Saade GR, et al. ; Eunice Kennedy Shriver National Institute of Child Health and Human Development Maternal–Fetal Medicine Units Network: Tranexamic acid to prevent obstetrical hemorrhage after cesarean delivery. N Engl J Med 2023; 388:1365–75. doi:10.1056/NEJMoa2207419 [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.