Advertisement

Quantitative Analysis for grading uterine electromyography activities during labor

  • Author Footnotes
    # Permanent address: 9 Jinsui Road, Zhujiang New Town, Guangzhou, Guangdong, China
    Xueya QIAN
    Footnotes
    # Permanent address: 9 Jinsui Road, Zhujiang New Town, Guangzhou, Guangdong, China
    Affiliations
    Department of Obstetrics and Gynecology, Guangzhou Women and Children's Medical Center, Guangzhou Medical University Guangzhou, Guangzhou, China
    Search for articles by this author
  • Bingqian ZHOU
    Affiliations
    Department of Obstetrics and Gynecology, Guangzhou Women and Children's Medical Center, Guangzhou Medical University Guangzhou, Guangzhou, China
    Search for articles by this author
  • Pin LI
    Affiliations
    Department of Obstetrics and Gynecology, Guangzhou Women and Children's Medical Center, Guangzhou Medical University Guangzhou, Guangzhou, China
    Search for articles by this author
  • Robert E. Garfield
    Affiliations
    Department of Obstetrics and Gynecology, University of Arizona College of Medicine-Phoenix, Phoenix, AZ, USA
    Search for articles by this author
  • Author Footnotes
    # Permanent address: 9 Jinsui Road, Zhujiang New Town, Guangzhou, Guangdong, China
    Huishu LIU
    Correspondence
    Correspondence: Huishu Liu, MD, PhD, Department of Obstetrics, Guangzhou Women and Children's Medical Center, Guangzhou Medical University, 9 Jinsui Road, Guangzhou, China, 510623
    Footnotes
    # Permanent address: 9 Jinsui Road, Zhujiang New Town, Guangzhou, Guangdong, China
    Affiliations
    Department of Obstetrics and Gynecology, Guangzhou Women and Children's Medical Center, Guangzhou Medical University Guangzhou, Guangzhou, China
    Search for articles by this author
  • Author Footnotes
    # Permanent address: 9 Jinsui Road, Zhujiang New Town, Guangzhou, Guangdong, China
Open AccessPublished:November 06, 2022DOI:https://doi.org/10.1016/j.ajogmf.2022.100798

      Abstract

      Background

      : The strength of uterine contraction is one of the decisive factors for labor progression and parturition. Clinicians usually encounter difficulties in early identification of inadequate contractions and oxytocin treatment. Electromyography (EMG), an emerging technology for uterine contraction monitoring, can quantify the intensity of myoelectric activity of uterine contraction. Therefore, grading patients with different uterine contraction intensities by EMG is of great significance to clinical intensive management of uterine contraction and labor process.

      Objective

      : To quantify and grade EMG activity during latent phase of the 1st stage of labor and explore its relationship with oxytocin treatment and length of labor.

      Study Design

      : We performed a retrospective cohort study to identify EMG parameters as a predictor for oxytocin treatment and length of labor among a cohort of term singleton primipara (n =508) during latent phase who delivered in Guangzhou between August 2018 and December 2021. EMG parameters were graded according to the quartile method, and the significance of grading and delivery outcome was explored. Univariate and multivariate logistic regression were used to determine the predictors of oxytocin treatment.

      Results

      : Maternal gestational age (aRR 1.2, 95% CI 1.0-1.5), root mean square (aRR 0.01, 95% CI 0.004-0.03) and power (aRR 0.02, 95% CI 0.01-0.05) were significant predictors of oxytocin argumentation. The low EMG activity group had a longer 1st stage labor and total labor time and were more likely to use oxytocin.

      Conclusions

      : EMG parameters root mean square and power had high predictive values for later oxytocin treatment among patients with spontaneous labor. Patients with low grade EMG were more likely need oxytocin treatment. EMG grading is very important for its clinical promotion and use, which could lead to more reliable analyses of oxytocin treatments and eventually to more effective interventions to prevent prolonged labor.

      Keywords

      Introduction

      Numerous studies have confirmed that electromyography (EMG) signal was able to reflect the original process of muscle fiber excitation and the electrical signals recorded through skin were consistent with those recorded through mucosal and serosal electrodes1,2. In comparison with the gold-standard IUPC3, EMG showed high consistency with uterine contraction and better accuracy and sensitivity than TOCO4. EMG activities was also reflective of the frequency and intensity of uterine contraction. Recent advances in EMG have therefore been applied in both clinical practice and research, including the prediction of preterm birth5,6, parturition7,8 and labor arrest9,10, as well as the evaluation of the effects of tocolysis 11-14, oxytocin 10 and patient-controlled epidural analgesia (PCEA) 15-17on EMG activities and outcomes in labor.
      EMG is recognized as an effective means of pregnancy and delivery monitoring, but it is still not widely used in clinical. The use of EMG quantification was limited in clinical practice due to both technical difficulties and the lack of reference values. At present, no technology is able to automatically calculate the EMG intensity in a direct and prompt manner. More importantly, well-defined reference values and appropriate classifications of EMG activities which can be regarded as treatment reference were yet to be established. Traditionally, normative reference values have been established in multicenter studies. Unfortunately, EMG data is collected only by specified equipment, which is inconsistent among different EMG teams 7,18,19. Our team is devoted to the study of uterine EMG during labor and our previous studies have confirmed that EMG intensity and activity were characterized by considerable variability at different and stages of labor and among individuals20. Therefore, in order to achieve better clinical practicability of EMG, this study attempted to quantify and grade EMG activity during latent phase of the 1st stage of labor and explore its relationship with oxytocin treatment and length of labor.

      Materials and Methods

      Patients

      A retrospective observational cohort study was conducted in a single institution (Guangzhou Women and Children's Medical Center, Guangdong, China) from August 2018 through December 2021, which included 508 primiparas with spontaneous labor and intact membranes at term during the first stage of labor with cervical dilation from 0 cm until 6cm. The inclusion criteria were as follows: (1) a singleton pregnancy with a gestational age of 37 to 42 weeks, (2) fetus with occipital presentation, (3) patients had received patient controlled epidural anesthesia (PCEA) before receiving EMG monitoring and had regular uterine contractions on TOCO, (4) Patients had not received oxytocin infusion before EMG were recruited. The completed gestational weeks were determined by the date of the first day of the last menstrual period and confirmed by ultrasound scan. Patients with medical complications of pregnancy or fetal abnormalities confirmed during pregnancy that would be expected to affect delivery mode were excluded(see Table S1). The study protocol was in accordance with the ethical guidelines and approval of Guangzhou Women and Children's Medical Center (protocol number 2018040301). Informed consent was obtained from all patients.
      Patients were asked to remain still while in the supine position without disturbing the electrodes and TOCO used for the recordings. EMG data were not available to the treating physician. Participation in the study did not affect the treatment of patients by any means. All clinical decisions were solely based on the routinely used TOCO and other clinical signs and symptoms. Indications for oxytocin treatment are hypotonic uterine atony that leads to prolonged or arrested labor and delayed fetal head descent.
      Maternal age (years), body mass index (BMI), gestational age, and duration of labor and delivery outcome were recorded.

      Electromyography Recording and Analysis

      Uterine EMG activities were recorded noninvasively from the abdominal surface by using 2 sets of Ag–AgCl Beckman differential bipolar electrodes (Shanghai Jun Kang Medical Supplies Co, Ltd, Shanghai, China). Electrodes were placed around patients’ navel, and each electrode was separated from its respective partner by approximately 3 cm. A reference electrode was placed laterally on the patient's hip. Using PowerLab hardware (ADInstruments, CastleHill, Australia), uterine EMG signals were digitally filtered to yield a final band pass of 0.34 to 1.00 Hz to exclude most components of motion, respiration, and cardiac signals while preserving the main contraction signals where 98% of uterine electrical activity was found15.
      All patients were monitored for at least 30 minutes and also followed with external TOCO using a standard maternal–fetal monitor (Avalon FM20; Philips, Best, the Netherlands). EMG and TOCO recordings were obtained during the latent phase of the first stage of labor for 30 minutes immediately following the definition of cervical dilation by attendants in the delivery room.
      The determination criteria of EMG burst and parameters were obtained from previous publications20-22 . Number of bursts/10 minutes, burst duration, which represents the frequency and duration of uterine contraction. Root mean square (RMS) and power were used to assess the energy of the electrical activity of bursts. Frequency-related parameters including media frequency and peak frequency of the power density spectrum (PDS) for characterizing the uterine electrical signals. All the EMG recording and analysis were done by trained and experienced investigators.

      Outcomes

      The primary outcome was subsequent oxytocin treatment.. The secondary outcome was length of labor.

      Statistical Analysis

      The statistical significance of intergroup differences was evaluated by one-way ANOVA or Kruskal-wallis test when appropriate for pairwise comparisons according to the distribution of variables. Spearman's correlation was used to determine the relationship between EMG activity and length of labor. Multivariate linear regression analysis was used to estimate the association between the duration of the length of labor and clinic data (gestational age, BMI, etc.) and EMG parameters. Logistics analysis was used to identify the correlation of clinic data and EMG parameters with oxytocin treatment.
      All statistical tests were 2-sided, and the level of significance was recognized as p < 0.05. All statistical analyses were performed by using the IBM® SPSS 23.0 software (SPSS Inc., Chicago, IL, USA). and the statistical software R 3.6.1 (R Core Team 2019). A P value 0.05 for two-sided test was considered as statistically significant.

      Results

      General characteristics of the patients

      Table 1 presents the general characteristics of this cohort. Among 508 patients, 227 received oxytocin treatments (oxytocin group) and 281 did not (without oxytocin group) during the next period of labor. The RMS values were divided into three groups (low, median and strong EMG activity groups) by the quartiles(see Table 2)., so was Power values (see table S2). Baseline charactertistcs including age, BMI, neonatal weight and delivery mode were not statistically different among groups. Lower EMG activity was observed in patients at greater gestational age. Low EMG activity group had a longer 1st stage and total length labor and was more likely to use oxytocin (see Table 2).
      Table 1General characteristics of the patients
      CategoryN (%)/mean (SD)/median(ranges)
      Maternal characteristics
      Age,years28.5(3.3)
      BMI,kg/m225.2(23.6,27.24)
      Gestational age,weeks39.6 (38.8,40.3)
      Oxytocin treatment
      With oxytocin227(44.69%)
      Without oxytocin281(55.32%)
      Fetal characteristics
      Neonatal birth weight, g3220.0(3002.5,2450.0)
      1-min Apgar9(8-9)
      5-min Apgar9(9-10)
      Delivery mode
      Spontaneous vaginal delivery420(82.68%)
      Operative vaginal birth (forceps)52(10.24%)
      Cesarean section36(7.09%)
      Labor characteristics
      1st stage of labor,min620(450-763.8)
      2nd stage of labor,min40(27-70)
      3rd stage of labor,min5(4-6)
      Postpartum hemorrhage, mL250(200-300)
      Abbreviation: BMI, body Mass Index; RMS: root mean square
      Table 2Clinical data and EMG characteristics of three grade of RMS
      FactorRMSF/H/X2P
      <25%25-75%>75%
      0.01-0.02mV0.02-0.07 mV0.07-0.42 mV
      Maternal characteristics
      Age,years28.7±3.428.5±3.028.3±3.60.30.7
      BMI,kg/m225.4(23.6,27.0)24.9(23.6,27.2)25.4(23.5,27.4)0.020.9
      Gestational age,weeks39.7(38.9,40.4)39.5(38.4,40.1)*39.7(39.0,40.5)*5.20.006
      Labor characteristics
      Neonatal birth weight,g3210.0(3000.0,3440.0)3240.0(3060.0,3492.5)3160.0(2980.0,3400.0)3.10.2
      1st stage of labor,min693.0(512.5,823.8)620.0(450.0,780.0)*552.5(397.5,720.0)*#21.5<0.01
      2nd stage of labor,min47.5(31.3,84.0)40.0(27.0,69.8)34.0(20.0,60.0)*13.50.001
      3rd stage of labor,min5.0(4.0,6.0)5.0(3.0,6.0)5.0(4.0,7.0)1.80.4
      Total labor,min757.5(570.0,898.8)660.0(506.3,828.8)*575.0(445.0,768.8)*#24.7<0.01
      Postpartum hemorrhage, mL230.0(200.0,330.0)250(200,300)230(200,300)2.10.4
      Oxytocin treatment
      with oxytocin159(100%)56(24.8%)12(9.8%)293.8<0.01
      without oxytocin0170(75.2%)111(90.2%)
      Delivery mode
      Spontaneous vaginal delivery128(80.5%)192(85.0%)100(81.3%)3.40.5
      Operative vaginal birth (forceps)16(10.1%)20(8.8%)16(13.0%)
      Cesarean section15(9.4%)14(6.2%)7(5.7%)
      Uterine EMG parameters
      Number of bursts/10 min4(3,4)4(3,4)4(3,5)3.90.2
      Durantion,s44.3 (38.8,51.0)43.2(33.8,52.9)43.8(35.0,56.8)2.90.2
      Median frequency, Hz0.52(0.49,0.55)0.49(0.46,0.53)*0.47(0.45,0.50)*#41.0<0.01
      Peak frequency, Hz0.43(0.41,0.49)0.42(0.37,0.49)0.40(0.37,0.43)*#24.1<0.01
      Power, nV20.25(0.14,0.41)2.5(1.4,3.6)12.4(7.5,24.0)*#416.9<0.01
      *:compared P values with < 25% group,#:Compared with 25-75% group
      Data are expressed as mean±SD, median(ranges),and N(%)

      EMG activity classification and its clinical predictive value

      We included the variables that were statistically different between the patients with or without oxytocin treatment in the univariate and multivariate logistic regression models to explore potential differential contributions. RMS and power showed independently high performance for the prediction of oxytocin treatment (see Table 3), both of which had a good diagnostic accuracy, as indicated by a receiver operating characteristic (ROC) area under the curve (AUC) value of 0.96 and 0.95(see fig 1).
      Table 3Factors related to oxytocin treatment using univariate and multivariate logistic regression analysis
      pUnivariate RRpMultivariate RR1pMultivariate RR2p
      Age, years0.81.0(0.95-1.1)0.81.0(0.9-1.1)0.81.0(0.9-1.1)0.7
      BMI, kg/m20.61.0(0.9-1.0)0.51.0(0.9-1.1)0.81.0(0.9-1.1)0.6
      Gestational age, weeks0.0031.2(1.1-1.4)<0.011.2(1.0-1.5)0.021.2(1.0-1.5)0.02
      Neonatal birth weight, g0.41.0(1.0-1.001)0.51.0(0.99-1.0)0.91.0(0.99-1.0)0.7
      Duration, s0.90.99(0.98-1.0)0.21.0(0.98-1.02)0.91.0(0.98-1.02)1.0
      Number of bursts/10 min0.30.90.90.8
      RMS, mV*<0.010.01(0.004-0.02)<0.010.01(0.004-0.03)<0.01
      Power, nV2*<0.010.02(0.01-0.05)<0.010.02(0.01-0.05)<0.01
      Median frequency, Hz*<0.011.9(1.5-2.3)<0.011.4 (0.9-2.4)0.51.5(0.9-2.4)0.1
      Peak frequency, Hz*<0.011.6(1.3-1.9)<0.010.9(0.5-1.4)0.080.8(0.5-1.3)0.4
      EMG parameters (RMS, Power, Median frequency and Peak frequency) were transferred by normal scores of SPSS to realize the normal transformation of data. The normality of the scores was evaluated using the Kolmogorov–Smirnov and Shapiro–Wilk tests of normality.
      1: Regression model included all variables presented in the table except Power because RMS and power are colinear
      2: Regression model included all variables presented in the table except RMS
      Abbreviation: BMI, body Mass Index; RMS: root mean square
      Figure 1
      Figure 1?Qry msg="Figure caption is missing please check"?

      Relationship between EMG parameters and length of labor

      We conducted correlation analysis and regression analysis on 472 patients with spontaneous vaginal delivery. In correlation analysis, both peak frequency (Spearman correlation=-0.21) and power (Spearman correlation=-0.20) showed a negative correlation with length of first stage of labor(p<0.001). The same correlation was observed between peak frequency (Spearman correlation=-0.23) and power (Spearman correlation=-0.22) with the total length of labor(p<0.01). Through multivariate linear regression, it was found that gestational age (p=0.007, 0.12, 95% CI: 0.01, 0.09), BMI (p=0.02, 0.11, 95% CI: 0.01, 0.07) and peak frequency (p=0.02, -0.22, 95% CI: -6.98, -0.54) were correlated with the length of total stage of labor, although R2 was only 0.1(see table S3).

      Comment

      Principal Findings

      In this study, we analyzed and described the characteristics of EMG activities during the 1st stage of labor in 508 patients. We found that RMS and power were able to independently yield excellent prediction of subsequent oxytocin treatment. Through grading analysis of EMG activities, we found that low grade of EMG activities indicated high possibility of oxytocin treatment in the follow-up labor process, while high grade EMG activity is associated with lower oxytocin use.

      Results in the Context of What is Known

      EMG provides valuable data concerning contraction intensity, duration and interval. However, there is much ambiguity and inadequacy in current studies on the quantification of EMG characteristics, which were only presented under different conditions such as that EMG activity was intense in preterm5 or term labor7,23, while it was inhibited after the use of epidural analgesia15,16 or tocolysis 24. The lack of an established clinical reference range or grading of parameters limited the application of EMG in clinical practice and research. Therefore, we aimed to grade uterine contractility by EMG activity in this more detailed study.

      Clinical Implications

      Intrapartum assessment of uterine activity is routinely employed to guide active management of labor and delivery. Accordingly, the initial objective of our study was to explore the relationship between EMG parameters and oxytocin treatment. The results indicated that there were significant differences in uterine EMG parameters in patients with and without subsequent oxytocin use. This was in accordance with Vasak et al 10study, which found that the frequency of EMG bursts was higher in patients with augmentation of labor. Our result showed that lower RMS and power of EMG burst was more likely to use oxytocin. We therefore categorized patients into three groups according to EMG activity indicating uterine contractions: hypotonic, normal and hypertonic uterine contraction.
      The secondary objective of our study was to determine the EMG parameters with the length of labor. Our study showed that patients with lower RMS and power, higher median and peak frequency were more likely have longer length of 1st stage and total labor, however, the correlations of which were relatively weak. In linear regression, we did not find that any individual or combination of the five uterine EMG parameters had a significant correlation with the length of labor. One possible explanation was that there were a number of confounding factors affecting the length of labor, such as maternal BMI, gestational weeks, incoordinate uterine action and human intervention like oxytocin treatment, etc.

      Research Implications

      Hypocontractile uterine activity is the most common risk factor for protraction and/or arrest disorders in the first stage of labor. Nowadays it widely be monitored qualitatively by palpation or with TOCO. However, these methods are not accurate enough and are easily affected, such as patient position and obesity. Patients are prone to unnecessary medical intervention due to inaccurate evaluation, such as amniotomy and oxytocin treatment. In order to avoid the risk of unnecessary adverse reactions to patients and fetuses caused by excessive application of oxytocin25, accurate identification of hypotonic uterine contraction is essential. We believe that low-grade EMG may be the EMG characteristics of patients with primary hypotonic uterine contraction. The cesarean section rate was higher in low grade RMS and power group. Though there are many reasons for cesarean section, arrested labor due to uterine atony during labor is also one of the indications. Physicians should be alerted when encountered with patients with low grade EMG, and oxytocin should be used timely to reduce the occurrence of prolonged or arrest labor process and promote the smooth progress of labor process

      Strengths and Limitations

      The strength of this study was that it was to date the largest retrospective control study on EMG of solely primipara in 1st stage of labor. We initially explored the uterine EMG grading, and found its correlation with oxytocin treatment, laying a foundation for the follow-up use of uterine EMG in labor management. However, the EMG grading extrapolated study still require further verification. The main limitation of the trial is as follows. First, this study did not include patients who needed induction of labor, patients with prelabor rupture of the membranes, and patients with complications. Meanwhile this is a single center, retrospective cohort study. All above affected the generalizability of this study. Second, we did not pay attention to the dosage of oxytocin, and the interval between EMG collection and later oxytocin treatment, which may also affect the study conclusion. Nevertheless this is the first attempt to grade EMG activities. We hope that our research can lead to other experts to explore the range of EMG of normal uterine contractions. Future well designed cohort studies that can effectively reduce bias are needed to confirm the effectiveness of this grading method in assessing the clinical outcome, including the use of oxytocin, the length of labor and the mode of delivery etc. In order to establish a better extrapolation of the clinical scope of uterine EMG, a multi-center study of unified EMG monitoring method is still needed.

      Conclusions

      We evaluated five EMG measured parameters and their predictive values for later oxytocin treatment among patients with spontaneous labor. By grading EMG parameters, we identified that low grade EMG patients were more likely need oxytocin treatment. EMG grading is crucial for the clinical promotion and utilization of EMG, which could lead to more reliable analyses of oxytocin treatments and eventually to more effective interventions to prevent prolonged labor.

      Source of Funding

      This study was supported by funds from the Guangzhou High Tech Project "Application of uterine electromyography technology in delivery management" (No. 2019GX07) to Huishu Liu.

      Paper presentation

      The paper had not been presented elsewhere.

      Condensation

      Grading analysis of uterine EMG activities in latent phase of labor.

      References

      • 1. Devedeux D, Marque C, Mansour S, Germain G, Duchêne J. Uterine electromyography: a critical review. American journal of obstetrics and gynecology. 1993;169(6):1636-1653.
      • 2. Buhimschi C, Boyle MB, Garfield RE. Electrical activity of the human uterus during pregnancy as recorded from the abdominal surface. Obstet Gynecol. 1997;90(1):102-111.
      • 3. Euliano TY, Nguyen MT, Darmanjian S, et al. Monitoring uterine activity during labor: a comparison of 3 methods. Am J Obstet Gynecol. 2013 Jan;208(1):66.e1-6.
      • 4. Reinhard J, Hayes-Gill BR, Schiermeier S, et al. Uterine activity monitoring during labour–a multi-centre, blinded two-way trial of external tocodynamometry against electrohysterography. Zeitschrift fur Geburtshilfe und Neonatologie. 2011;215(5):199-204.
      • 5. Lucovnik M, Maner WL, Chambliss LR, et al. Noninvasive uterine electromyography for prediction of preterm delivery. Am J Obstet Gynecol. 2011;204(3):228 e221-210.
      • 6. Eswaran H, Preissl H, Wilson JD, Murphy P, Lowery CL. Prediction of labor in term and preterm pregnancies using non-invasive magnetomyographic recordings of uterine contractions. Am J Obstet Gynecol. 2004;190(6):1598-1602; discussion 1602-1593.
      • 7. Kandil M, Emarh M, Ellakwa H. Abdominal electromyography in laboring and non-laboring pregnant women at term and its clinical implications. Arch Gynecol Obstet. 2013;288(2):293-297.
      • 8. Garfield RE, Maner WL, MacKay LB, Schlembach D, Saade GR. Comparing uterine electromyography activity of antepartum patients versus term labor patients. Am J Obstet Gynecol. 2005;193(1):23-29.
      • 9. Euliano TY, Marossero D, Nguyen MT, Euliano NR, Principe J, Edwards RK. Spatiotemporal electrohysterography patterns in normal and arrested labor. Am J Obstet Gynecol. 2009;200(1):54 e51-57.
      • 10. Vasak B, Graatsma EM, Hekman-Drost E, et al. Uterine electromyography for identification of first-stage labor arrest in term nulliparous women with spontaneous onset of labor. Am J Obstet Gynecol. 2013;209(3):232 e231-238.
      • 11. Tattersall M, Engineer N, Khanjani S, et al. Pro-labour myometrial gene expression: are preterm labour and term labour the same? Reproduction (Cambridge, England). 2008;135(4):569-579.
      • 12. Kandil MA, Abdel-Sattar MM, Abdel-Salam SM, Saleh S, Khalafallah MM. Abdominal electromyography may predict the response to tocolysis in preterm labor. European journal of obstetrics, gynecology, and reproductive biology. 2012;160(1):18-21.
      • 13. Hadar E, Melamed N, Aviram A, et al. Effect of an oxytocin receptor antagonist (atosiban) on uterine electrical activity. Am J Obstet Gynecol. 2013;209(4):384.e381-387.
      • 14. Vinken MP, Rabotti C, Mischi M, van Laar JO, Oei SG. Nifedipine-induced changes in the electrohysterogram of preterm contractions: feasibility in clinical practice. Obstetrics and gynecology international. 2010;2010:325635.
      • 15. Ye Y, Song X, Liu L, et al. Effects of Patient-Controlled Epidural Analgesia on Uterine Electromyography During Spontaneous Onset of Labor in Term Nulliparous Women. Reproductive sciences (Thousand Oaks, Calif). 2015;22(11):1350-1357.
      • 16. Qian X, Wang Q, Ou X, Li P, Zhao B, Liu H. Effects of Ropivacaine in Patient-Controlled Epidural Analgesia on Uterine Electromyographic Activities during Labor. Biomed Res Int. 2018;2018:7162865.
      • 17. Zhao B, Qian X, Wang Q, Ou X, Lin B, Song X. The effects of ropivacaine 0.0625% and levobupivacaine 0.0625% on uterine and abdominal muscle electromyographic activity during the second stage of labor. Minerva anestesiologica. 2019;85(8):854-861.
      • 18. Rosen H, Salzer L, Hiersch L, Aviram A, Ben-Haroush A, Yogev Y. Uterine electric activity during the third stage of labor; a look into the physiology of a deserted stage. The journal of maternal-fetal & neonatal medicine: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet. 2014;27(9):921-925.
      • 19. Trojner Bregar A, Lucovnik M, Verdenik I, Jager F, Gersak K, Garfield RE. Uterine electromyography during active phase compared with latent phase of labor at term. Acta Obstet Gynecol Scand. 2016;95(2):197-202.
      • 20. Qian X, Li P, Shi SQ, Garfield RE, Liu H. Simultaneous Recording and Analysis of Uterine and Abdominal Muscle Electromyographic Activity in Nulliparous Women During Labor. Reproductive sciences (Thousand Oaks, Calif). 2017;24(3):471-477.
      • 21. Qian X, Li P, Shi SQ, Garfield RE, Liu H. Uterine and Abdominal Muscle Electromyographic Activities in Control and PCEA-Treated Nulliparous Women During the Second Stage of Labor. Reproductive sciences (Thousand Oaks, Calif). 2017;24(8):1214-1220.
      • 22. Qian X, Li P, Shi S, Garfield RE, Liu H. Measurement of Uterine and Abdominal Muscle Electromyography in Pregnant Women for Estimation of Expulsive Activities during the 2nd Stage of Labor. Gynecologic and obstetric investigation. 2019:1-7.
      • 23. Lucovnik M, Kuon RJ, Chambliss LR, et al. Use of uterine electromyography to diagnose term and preterm labor. Acta Obstet Gynecol Scand. 2011;90(2):150-157.
      • 24. Lucovnik M, Trojner Bregar A, Bombac L, Gersak K, Garfield RE. Effects of vaginal progesterone for maintenance tocolysis on uterine electrical activity. The journal of obstetrics and gynaecology research. 2018;44(3):408-416.
      • 25. Page K, McCool WF, Guidera M. Examination of the Pharmacology of Oxytocin and Clinical Guidelines for Use in Labor. J Midwifery Womens Health. 2017;62(4):425-433.

      Conflicts of Interest

      The authors report no conflict of interest.

      Acknowledgments

      The authors would like to thank Ming Lei for helpful verbal change of the text. We also thank the nurses and midwives of the Department of Obstetrics, Guangzhou Women and Children's Medical Center for their support of this work.