OBSTETRICS

Interpreting category II fetal heart ratetracings: does meconium matter?Heather A. Frey, MD; Methodius G. Tuuli, MD, MPH; Anthony L. Shanks, MD;George A. Macones, MS, MSCE; Alison G. Cahill, MD, MSCI

OBJECTIVE: Category II fetal heart rate (FHR) tracings are consideredindeterminate; thus, improved risk stratification of category II FHR

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MATERIALS AND METHODSThis observational study was conductedamong the rst 5000 women who en-rolled in a prospective cohort studyof >8000 women. The purpose of theparent cohort, which included allconsecutive term singleton pregnanciesin labor, was to examine the relationshipbetween intrapartum EFM and perinatal

From the Department of Obstetrics and Gynecology, Washington University in St. Louis,St. Louis, MO.

Received March 29, 2014; revised May 23, 2014; accepted June 13, 2014.

Supported by National Institute of Child Health and Human Development (NICHD) grant number R01HD061619-04 (PI: A.G.C.); a training grant from NICHD grant number 5 T32 HD055172-05 (H.A.F.);andWashington University Clinical and Translational Science Awards grant number UL1 TR000448.

The authors report no conict of interest.

Presented at the 34th annual meeting of the Society for Maternal-Fetal Medicine, New Orleans, LA,Feb. 3-8, 2014.

Corresponding author: Heather Frey, MD. Heather.A.Frey@gmail.com

0002-9378/$36.00 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajog.2014.06.033C ategory II fetal heart rate (FHR)tracings1,2 are encountered com-monly during labor.3 Problems withinterpretation of the category II FHRtracing, in part, stem from the diversityof FHR patterns that are included in thisgroup. Additionally, the association be-tween category II FHR tracings and fetalstatus and neonatal outcomes is poorlydened. One study found that increas-ing duration of FHR tracing classiedas category II before delivery was asso-ciated with increased incidence of low

5-minute Apgar sintensive care unitBut, the vast majorcategory II FHR tracoutcomes after delivIt has been sugge

ical factors shouldthe evaluation ancategory II FHR trapredictive abilitymonitoring (EFM)outcomes.3 Meconiuuid is found in 12644.e1 American Journal of Obstetrics& Gynecology DECEMBER 2014ore and neonatalICU) admission.3

y of fetuses with ag will have normalry.4

ed that other clin-be considered inmanagement of

ngs to improve thef electronic fetalfor acidosis and-stained amnioticof all deliveries.5

Multiple studies have reported thatmeconium is associated with adverseneonatal outcomes that include fetalacidemia, low Apgar scores, and a needfor neonatal resuscitation.6-9 Further-more, the risk of neonatal morbidityin the setting of both meconium andan abnormal FHR tracing may exceedthe risk associated with either factorindependently.10-12 We performed thisstudy among women at term with acategory II intrapartum FHR tracingto estimate whether the presence ofmeconium increased the risk of adverseCite this article as: Frey HA, Tuuli MG, Shanks AL, et al. Interpreting category II fetal heart rate tracings: does meconium matter? Am J Obstet Gynecol2014;211:644.e1-8.cord pH, 5-minute Apgar score, and componLogistic regression was used to adjust for contracings is needed. We estimated whether theincreased the risk of adverse neonatal outcom

STUDY DESIGN: This study was conducted withof 5000 women with singleton pregnancieslabor at term. Pregnancies with category II Fbefore delivery were included. FHR data wernurses who were blinded to clinical outcome.presence of meconium. The primary outconeonatal morbidity defined as 1 of the follneurologic morbidity, respiratory morbidity, hytreatment, and sepsis. Secondary outcomes wresence of meconiums.

a prospective cohortho were admitted inR in the 60 minutesextracted by trainedhe exposure was thee was a compositeing: neonatal death,tension that requiredre nursery admission,ts of the composite.unders.

did not. Meconium wamorbidity (adjusted1.78e3.48) and incrassociations remainedration syndrome wersignificantly with the c

CONCLUSION: The pincreased risk of neopattern. This clinical faII FHR patterns in labo

Key words: electronic7 women with category II FHR tracings,ad meconium, and 2564 women (78.7%)associated with higher risk of the compositeds ratio, 2.49; 95% confidence interval,sed risks of the secondary outcomes. Theignificant when infants with meconium aspi-excluded. Thick meconium was associatedmposite morbidity.

sence of meconium is associated with antal morbidity in women with category II FHRtor may assist clinicians in managing category

etal monitoring, fetal heart rate, meconiumoutcomes. The Washington University

FHR tracing, because each tracing wasanalyzed in 10-minute increments inthis study. Women with any 10-minuteFHR pattern in the hour before deliverythat was dened as category III wereexcluded, as were women whose FHRtracing before delivery was category IIfor

category (370-386 weeks; 390-406 weeks;410 weeks), chorioamnionitis, ma-ternal obesity (body mass index 30kg/m2), previous cesarean delivery,hypertension, diabetes mellitus, andoxytocin use. We performed sensitivityanalyses that excluded pregnanciesthat were complicated by meconiumaspiration syndrome (MAS) and cho-rioamnionitis. MAS was dened as res-piratory distress and transthoracicechocardiographic ndings of elevatedmain pulmonary artery pressures.17 Weconducted a stratied analysis basedon the classication of meconium asthin or thick. We explored specic fea-tures within category II FHR patternsto identify whether meconium in thesetting of specic features conferred risk.We estimated the ability of the pres-

ence of meconium to predict adverse

neonatal outcomes among women witha category II FHR tracing by calculatingthe sensitivity, specicity, and positiveand negative predicted values. Similarly,we assessed the test characteristics ofa predictive model that included indi-vidual FHR characteristics in our modelin addition to meconium.Tests with a probability value of

< .05 were considered statistically sig-nicant. All statistical analyses were per-formed using STATA software (version10.0 [special edition]; StataCorp, Coll-ege Station, TX).

RESULTSAmong the 5000 women who wereadmitted at term with a singleton gesta-tion, 3257 women had a category IIFHR tracing in the hour before delivery.Of the women with the category II

FHR tracing, 693 women (21.3%) hadmeconium-stained amniotic uid; in2564 women (78.7%), meconium wasabsent (Figure).Women with meconium were more

likely to be nulliparous and at a moreadvanced gestational age, but lesslikely to have been diagnosed with hy-pertension or diabetes mellitus. Cho-rioamnionitis and operative vaginaldelivery were more likely in pregnancieswith meconium, although the use ofoxytocin was less common amongwomen with meconium than thosewithout meconium (Table 2).Among women with a category II

FHR tracing, meconium was associatedwith an increased risk of neonatal mor-bidity (12.1% vs 5.3%; aOR, 2.49; 95%condence interval [CI], 1.78e3.48).Each component of the composite,

FIGUREFlow diagram of study cohort

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Research Obstetrics ajog.orgFHR, fetal heart rate.

Frey. Category II tracings and meconium. Am J Obstet Gynec644.e3 American Journal of Obstetrics& Gynecol2014.ogy DECEMBER 2014

eajog.org Obstetrics ResearchTABLE 2Comparison of characteristics: pres

Variable

Maternal age, yb

Nulliparity, n (%)

Gestational age, wk (%)

370-386

390-406

410

Raceexcept neonatal death, was also morecommon in pregnancies withmeconium-stained amniotic uid. However, becauseof the rarity of the individual out-comes, only respiratory morbidity andsuspected sepsis reached statistical signif-icance. Higher acuity nursery admission,fetal acidemia, and Apgar score

TABLE 3Comparison of neonatal outcomes: presence or absence of meconiuma

VariableMeconium(n[ 693), n (%)

No meconium(n[ 2564), n (%)

Adjusted odds ratio(95% confidence interval) P value

Composite morbidityb 84 (12.1) 135 (5.3) 2.49 (1.78e3.48) < .01

Death 0 2 (0.1)

Neurologic morbidity 5 (0.7) 8 (0.3)

Respiratory morbidityb 48 (6.9) 60 (2.3) 3.22 (2.13e4.85) < .01

Hypotension that required therapy 1 (0.1) 0

Suspected sepsisb 63 (9.1) 114 (4.4) 1.97 (1.34e2.90) < .01

Higher acuity nursery admissionb 89 (12.9) 149 (5.8) 2.41 (1.75e3.32) < .01c (2.5) 21 (0.8) 2.84 (1.48e5.44) < .01

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Research Obstetrics ajog.orgCOMMENTOur results show that meconium is aclinical factor that can be used for riskstratication in women with a categoryII FHR tracing. The presence of meco-nium was associated with a compositeneonatal morbidity and adverse out-comes that include higher acuity nurs-

Neonatal intensive care unit 17

Special care nurserya 72

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ajog.org Obstetrics ResearchTABLE 5Fetal heart rate characteristics 30 m

Characteristic

Comoutc

Pres(n[

Accelerations presentc 13 (1

Tachycardiad 23 (2

Variabilitye

Always moderate 25 (2

Ever minimal/absent 52 (6

Ever marked 7 (8

Ever moderate 51 (6

Accelerations presentc or evermoderate variabilitye

55 (6

Decelerationsf

No repetitive decelerations 48 (5

Repetitive late 2 (2

Repetitive variable 34 (4

a Associated with the composite adverse outcome in women30 minutes before delivery; d Fetal heart rate>160 beats/mthere was evidence meconium, tachy-cardia, and absent accelerations beforedelivery in the setting of category II FHRtracing. Thus, taking into account thepresence of meconium when treatingwomen with a category II FHR tracingmay be preferable to considering theFHR category in isolation. Incorpora-tion of meconium into clinical decisionrules based on FHR categories should bethe focus of future research.The prospective interpretation of the

FHR tracings by obstetric nurses who areblinded to clinical outcome is a majorstrength of this study. This reduced therisk of bias that is introduced whenthe interpretation of the FHR tracingis performed by an individual who isactively providing clinical care to theparticipant. Additionally, the prospectivestudy design minimized the amountof missing data. Our use of sensitivityanalysis to exclude neonates withMAS is noteworthy. Although multipleother studies have found that meco-nium is associated with adverse neonatal

during the entire 30-minute period before delivery; ever rf Decelerations were considered repetitive if they occurred wit

Frey. Category II tracings and meconium. Am J Obstet Gyninutes before delivery in women with

osite neonatalme, n (%)

Odds ratio (95%confidence interv

nt84)

Absent(n[ 609)

.5) 171 (28.1) 0.47 (0.23e0.88)

.4) 67 (11.1) 3.02 (1.67e5.32)

.8) 212 (34.8) Reference

.9) 371 (60.9) 1.19 (0.70e2.06)

3) 29 (4.8) 2.05 (0.81e5.15)

.7) 368 (63.4) 0.89 (0.55e1.47)

.5) 426 (70.0) 0.81 (0.49e1.37)

.1) 390 (64.0) Reference

4) 20 (3.3) 0.81 (0.09e3.52)

.5) 212 (34.8) 1.30 (0.79e2.15)

ith meconium and category II fetal heart rate before delivery; b Ain any epoch within the last 30 minutes of delivery; e Variability was outcome, it is often unclear whether themorbidity occurs primarily in infantswith MAS. The results of this studysuggest that this association exists inde-pendent of the development of MAS.Furthermore, meconium passage hasbeen reported previously to be associatedwith higher rates of intraamniotic infec-tion18,19; thus, it is conceivable that cho-rioamnionitis is on the causal pathwaythat links meconium to neonatalmorbidity. To investigate this further,we performed a sensitivity analysisthat excluded pregnancies that werecomplicated by chorioamnionitis andfound that the association betweenmeconium and an increased riskof adverse neonatal outcome per-sisted, which suggests an independentassociation.The nding that neonatal morbidity

was increased signicantly when meco-nium was described as thick, butnot thin, is also remarkable. Thickmeconium, in contrast to thin meco-nium, has been described previously as

efers to the presence of the specific variability descriptor during ah 50% of contractions.ecol 2014.

DECEMBER 2014 Amerieconiuma

l)Adjusted oddsratio (95% CI)b P value

0.55 (0.29e1.05) .07

1.49 (0.76e2.92) .25

1.01 (0.58e1.77) .96

0.97 (0.58e1.62) .90

0.96 (0.56e1.65) .90

1.33 (0.79e2.23) .28

sted for chorioamnionitis; c Any acceleration present in theays moderate if the amplitude ranged from 6-25 beats/minhighly correlated with fetal acidosis.6,8,9

This nding may indicate either a dose-response relationship or reect differ-ing causes related to the varying typesof meconium.The use of a composite outcome may

be viewed as a limitation of the study.However, use of the composite enabledus to evaluate the effect of meconium onneonatal outcomes that would not befeasible with the individual neonatalmorbidity. It is also likely that the pres-ence of meconium is related to severalneonatal morbidities, which makes acomposite outcome justiable. Further,the neonatal outcomes that wereconsidered as part of the composite aremore clinically meaningful than morecommonly occurring surrogate mea-sures of morbidity such as low Apgarscore. Our conclusion that meconium isassociated with neonatal morbidity inthe setting of a category II FHR tracingis further strengthened by the ndingthat there were higher rates of thesecondary morbidity outcomes among

ny 10-minute segment in the 30 minutes before delivery;

can Journal of Obstetrics& Gynecology 644.e6

TABLE 6Impact of meconium on risk of composite adverse outcomea

Fetal heart rate characteristicComposite neonataloutcome, n/N (%)

Adjusted odds ratio(95% confidenceinterval)b P value

Accelerations presentc (n 950)Meconium 13/184 (7.1) 1.63 (0.78e3.40) .19

No meconium 35/766 (4.6)

Tachycardia absentd (n 2922)Meconium 61/597 (10.2) 3.20 (2.20e4.66) < .01

No meconium 79/2325 (3.4)

Always moderate variabilitye

(n 1208)Meconium 25/237 (10.5) 2.49 (1.41e4.43) < .01

No meconium 45/971 (4.6)

Ever moderate variabilitye

(n 2102)Meconium 51/437 (11.7) 2.15 (1.42e3.24) < .01

No meconium 92/1665 (5.5)

Accelerations presentc or evermoderate variabilitye (n 2376)

Meconium 55/481 2.33 (1.57e3.45) < .01

No meconium 99/1895

No repetitive decelerationsf

(n 2087)Meconium 48/438 (11.0) 2.48 (1.60e3.84) < .01

No meconium 71/1649 (4.3)

a Among women with specific fetal heart rate characteristics 30 minutes before delivery and category II fetal heart rate;b Adjusted for chorioamnionitis; c Any acceleration present in the 30 minutes before delivery; d Fetal heart rate>160 beats/min in any epoch within the last 30 minutes of delivery; e Variability was always moderate if the amplitude ranged from6-25 beats/min during the entire 30-minute period before delivery; ever refers to the presence of the specific variabilitydescriptor during any 10-minute segment in the 30 minutes before delivery; f Decelerations were considered repetitive if theyoccurred with 50% of contractions.

Frey. Category II tracings and meconium. Am J Obstet Gynecol 2014.

TABLE 7Test characteristics of the presence meconiuma

VariableSensitivity,%

Specificity,%

Positivepredictivevalue, %

Negativepredictivevalue, %

Meconium 38.4 80.0 12.1 94.7

Meconium tachycardia 27.4 88.9 25.6 89.9Meconium absent accelerations 84.5 28.1 13.9 92.9Meconium tachycardia absentaccelerations

26.2 91.2 29.3 89.9

a For the prediction of adverse neonatal outcome in pregnancies with category II fetal heart rate tracing.

Frey. Category II tracings and meconium. Am J Obstet Gynecol 2014.

Research Obstetrics ajog.org

644.e7 American Journal of Obstetrics& Gynecology DECEMBER 2014pregnancies that were complicated bymeconium.We categorized the FHR based on the

last 60minutes of tracing before delivery.Although the time period most proximalto delivery may have the greatest asso-ciation with neonatal outcomes, thisperiod of monitoring may not bereective of the characteristics of theFHR during other time periods in labor.Importantly, this study did not addressthe clinical application of the ndingsin the management of category II FHRtracings. Multiple studies support thehypothesis that meconium passage isstimulated by fetal hypoxia.20-22 How-ever, it is not clear whether it occurs inresponse to chronic or acute stress.Therefore, it is uncertain whether anintervention based on meconium statuswould yield improved neonatal out-comes because it is possible that meco-nium is a sign of a chronic stress statein which the neonatal consequencesare already determined. Additionally,although we demonstrated that there isan association between meconium andadverse neonatal outcome in our study,the neonatal composite morbidity wasabsent in the majority of pregnanciesthat were complicated by meconium(87.9%). It is possible that in utero pas-sage of meconium may not be a sign offetal stress in some pregnancies. Furtherresearch is required to dene the effec-tiveness of the use of meconium as afactor to guide clinical care.Category II FHR tracings often pre-

sent a clinical challenge to obstetricproviders in part because of the vari-ability in neonatal outcomes that arerelated to these EFM patterns. Our re-sults suggest that meconium, and spe-cically thick meconium, is a clinicalfactor that is associated with neonatalmorbidity among pregnancies with acategory II FHR tracing. Although theoverall predictive ability of meconiumfor adverse neonatal outcomes in thissetting is poor, the use of this factor torisk-stratify women may have clinicalutility, especially if it improves our cur-rent interpretation of EFM. In addition,the high negative predictive value sug-gests that the absence of meconium in

the setting of category II FHR tracing

can be considered a reassuring feature.In conclusion, we assert that, in our at-tempts to optimize the care of womenwith a category II FHR tracing, meco-nium is a factor that should be consid-ered in further risk stratication. -

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Interpreting category II fetal heart rate tracings: does meconium matter?Materials and MethodsResultsCommentReferences