Arch Gynecol Obstet (2013) 287:1067–1073 DOI 10.1007/s00404-012-2694-7

MATERNAL-FETAL MEDICINE

Intrapartum fetal asphyxia: study of umbilical cord blood lactate in relation to fetal heart rate patterns Hossam O. Hamed

Received: 14 October 2012 / Accepted: 17 December 2012 / Published online: 29 December 2012 Ó Springer-Verlag Berlin Heidelberg 2012

Abstract Purposes To correlate between umbilical artery cord blood lactate and acid–base status with intrapartum fetal heart rate monitoring, and to measure the reliability of umbilical cord blood lactate for prediction of early neonatal outcome. Methods Sixty-six participants with intrapartum abnormal fetal heart rate monitoring and 60 participants with normal intrapartum recordings were recruited. The abnormal recordings included late onset, atypical variable and simple variable decelerations. After delivery, the arterial cord blood lactate, pH, actual base excess (ABE), and Apgar score were measured in all participants. Results There was significant inverse correlation between cord lactate and pH and ABE in all participants (correlation coefficient = -0.7, p \ 0.0001). The cord lactate was significantly higher in the late onset and atypical variable decelerations groups compared to control (p \ 0.0001). There was no significant correlation between the Apgar score and blood lactate in all groups; however, the sensitivity and specificity of cord lactate to predict low score at 5 min were higher in comparison to cord pH. Conclusions Umbilical cord blood lactate is a reliable marker for intrapartum fetal asphyxia compared to cord acid–base status with better prediction for newborns with low Apgar score.

H. O. Hamed (&) Department of Obstetrics and Gynecology, Women Health Center, Assiut University, Assiut, Egypt e-mail: [email protected] H. O. Hamed Department of Obstetrics and Gynecology, Qassim University, Buraidah, Saudi Arabia

Keywords Umbilical cord blood lactate
Fetal heart rate
Apgar score

Introduction Intrapartum fetal asphyxia is the presence of hypoxia during labor resulted in fetal acidosis and depression of vital functions and an increased risk of long-term morbidity [1]. Electronic fetal heart rate monitoring (EFM) during labor with a cardiotocography (CTG) was established as cornerstone in fetal surveillance [2]. Although normal results indicate that the fetus is getting enough oxygen, intrapartum CTG has a high false-positive rate and is associated with an increased rate of operative deliveries for presumed fetal distress [1]. Bretscher and Saling [3] were first introduced sampling of blood from the fetus’s scalp during labor to analyze pH as an indicator of hypoxia. Since that time, this technique has been regarded as the ideal method of identifying intrapartum fetal hypoxia. However, the analysis of pH which is complicated, costing and needs a relatively large amount of blood (30–50 ll) with sampling failure rates of 11–20 % has been reported [4, 5]. Lactate is a metabolite of anaerobic metabolism that causes increasing metabolic acidosis and reflects tissue hypoxia. As lactate influences the base excess and pH, a possible correlation between these parameters would be expected [6]. Although some authors [7] found no significant correlation between umbilical cord blood lactate and base excess or pH, others [8, 9] found strong correlation. Therefore, lactate concentration in umbilical cord blood at delivery might be a more precise tool in assessment of fetal metabolic acidosis as it measures the metabolic acidosis rather than respiratory acidosis. The other advantage of

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lactate over pH is the easy rapid measurement using electrochemical strip test device which needs a smaller amount of fetal blood (5 ll) [10, 11]. These advantages would favor replacement of the routine postpartum measurement of umbilical artery pH by lactate as an indicator of intrapartum fetal oxygenation. This is especially important in medical litigations in high risk cases with newborns having signs of encephalopathy to exclude intrapartum asphyxia as leading cause for neurological morbidity. The current study aims first to correlate between the umbilical artery blood lactate and pH in different intrapartum fetal heart rate patterns recorded in the active phase of labor and second, to measure the reliability of umbilical cord blood lactate in prediction of early neonatal outcome.

Patients and methods This is a prospective, descriptive, and comparative study conducted in Women’s Health Center, Assiut University, Egypt, in June 2009 through June 2012. The study was approved by the Ethical Review Board of Medical School. The study which included 66 women in labor with singleton, term, cephalic fetus with intrapartum FHR monitoring showed abnormal CTG patterns and another control group of 60 women showed normal intrapartum FHR recordings. According to the definitions reported in Royal College of Obstetrics and Gynecology (RCOG) [12] and American College of Obstetrics and Gynecology (ACOG) clinical guidelines [13], three patterns of FHR abnormalities that could be associated with fetal hypoxia and acidosis were included in this study. First, late onset decelerations in the heart rate, which were defined as slowing of the heart rate after the onset of uterine contractions and represent a transient fall in partial pressure of oxygen (hypoxemia) below a certain threshold. Second, simple variable decelerations defined by ‘pre-shouldering’ followed by a sudden decline and quick recovery to the baseline, followed by another ‘shouldering’ of the FHR. They vary in shape, form and timing and are produced by umbilical cord compression; they may be relieved by repositioning of the mother. Third, atypical variable decelerations with additional features such as late recovery, rebound tachycardia, loss of variability during decelerations, continuation of baseline heart rate at lower level, and decelerations with depth [60 beats and duration [60 s. All recordings were done by external CTG using a Corometrics 170 monitor (GE Healthcare, Chalfont St. Giles, UK). The woman is counted as positive for a specific CTG abnormality if it is recurrent or persistent (50 % of contractions at a given time are associated with decelerations) [2, 12, 13]. The exclusion criteria are maternal medical disorder that could affect their acid–base balance such as uncontrolled

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diabetes mellitus or chronic renal disorders; growth retarded fetuses and women received epidural analgesia or planned to be delivered by elective CS. The women were allocated from the labor ward in the women’s health hospital after taking an informed written consent. The participating women followed the usual intrapartum care according to the department policy including the intermittent electronic FHR monitoring which was done every 30–60 min in the first stage, and every 5–15 min in the second stage according to clinical situation. The course of labor, mode of delivery, and the primary indication for operative delivery was documented. Immediately after delivery, two samples of arterial umbilical cord blood were withdrawn from a double clamped segment into plastic syringes flushed with a heparin solution. The first sample was used for measurement of pH and actual base excess (ABE) within 15 min from sampling using an automatic blood gas analyzer (Optical care laboratory, SYNTHESIS 25). The second sample was used for measurement of plasma blood lactate by enzymatic colorimetric method (LOX/PAP) with lactate oxidase and 4-amino antipyrine (Spectrum diagnostics company, Germany). The sample was centrifuged to separate the plasma to keep the lactate level stable until analyzed within 48 h after storing in a temperature between 4 and 8 °C. Data were presented by mean ± 1SD and/or median and manipulated by GraphPad Prism and SPSS (version 14) statistical packages. Spearman’s non-parametric correlation was used to correlate between blood lactate and each of pH, ABE, and Apgar score. Mann–Whitney U nonparametric test was used for the comparison between lactate values in different CTG patterns. One-way analysis of variance (ANOVA) was used for comparison of clinical characteristics between different groups, and Tukey post test wass applied when ANOVA showed significant difference. Through receiver operator characteristics (ROC) curves and the related tables, the best cut-off point of lactate and pH which predicts the adverse early neonatal outcome was determined. A value of p \ 0.05 was considered significant with 95 % confidence interval.

Results Total of 126 participants in labor were recruited in this study. Sixty women out of 126 had normal intrapartum CTG as a control group, while the remaining 66 women had abnormal CTG patterns: late onset decelerations (n = 22), atypical variable decelerations (n = 21) and simple variable decelerations (n = 23). The median time of measurement of pH and ABE was 6 min (range 5–15 min), while the median for lactate measurement was 5 h (range 1–18 h).

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Table 1 displays the descriptive data and the course and outcome of labor in different groups. There were no significant differences between groups except in late onset and atypical variable decelerations which showed a significant shorter duration of second stage of labor, lower Apgar score and higher rate of CS compared to the other two groups. The main primary indication for those delivered by CS in late onset, atypical variable and simple decelerations groups was the abnormal CTG, while failure to progress was the main indication in normal CTG group. As shown in Table 2, the umbilical artery blood lactate level was significantly higher in late and the atypical variable decelerations groups compared to control, while the pH and ABE were significantly lower. The subgroup analysis of tested blood values in decelerations groups in relation to mode of delivery is shown in Table 3. The median of cord blood lactate, pH, and ABE in participants delivered by operative intervention (CS and instrumental delivery) was comparable to those delivered normally. The scattergram in Fig. 1 shows that cord blood lactate is inversely correlated with cord pH in all participants

(RS = -0.71 p \ 0.001). The detailed analysis in each CTG group, shown in Fig. 1 caption, showed a stronger correlation with pH in late onset decelerations group (p \ 0.0001) and atypical variable decelerations (p \ 0.001) than that with normal CTG and simple variable groups (p \ 0.05). A similar significant inverse correlation was found between blood lactate and ABE in the normal CTG group (RS = -0.42, p \ 0.05), late onset decelerations group (RS = -0.56, p \ 0.01), atypical variable (RS = -0.41, p \ 0.01), and the simple variable decelerations group (RS = -0.52, p \ 0.05) (figures are not displayed). The correlation between Apgar score and umbilical and pH is shown in Table 4. There was an association between 1-and 5-min Apgar score and cord blood lactate and pH at different FHR patterns. Although this correlation was more evident in late and atypical decelerations groups, this did not reach statistical significance. Through the ROC curves, the cut-off value of the best sensitivity and specificity of cord blood lactate and pH to predict low Apgar score at first and after 5 min was determined as shown in Table 5. The sensitivity and

Table 1 Demographic data, course of labor and Apgar score in different groups of fetal heart rate patterns Normal CTG (n = 60) Maternal age (years)

Late onset decelerations (n = 22)

Atypical variable decelerations (n = 21)

Simple variable decelerations (n = 23)

p value NS

26.60 ± 4.62

26.45 ± 5.62

25.45 ± 4.68

25.90 ± 4.49

(19–34)

(18–36)

(18–34)

(17–35)

Parity, median (range)

3 (0–7)

2 (0–5)

3 (0–6)

3 (0–5)

NS

Gestational age (weeks)

39.70 ± 0.80 (37–41)

39.50 ± 0.70 (38–42)

38.60 ± 0.90 (37–42)

38.50 ± 0.50 (37–41)

NS

Duration of active 1st stage (h) Duration of 2nd stage (min)

4.50 ± 1.30 (3–7) 59.40 ± 19.70 (35–85)

4.25 ± 1.10 (2.5–6)

4.60 ± 1.10 (3–6)

4.70 ± 1.00 (3–6.5)

NS

24.50 ± 7.60 (15–40)*

35.50 ± 9.20 (20–50)*

60.20 ± 10.00 (40–80)

\0.001*

Birth weight (kg)

3.29 ± 0.39 (2.7–4.2)

3.27 ± 0.37 (2.8–3.9)

3.24 ± 0.37 (2.8–4.0)

3.21 ± 0.41 (2.7–4.1)

NS

13/21 (61.9) 

7/23 (30.4)

\0.001 

Mode of delivery, ratio (%) CS Total

17/60 (28.3)

17/22 (77.2) 

Abnormal CTG

0/17 (0)

15/17 (88)

11/13 (85)

4/7 (56)

Failure to progress Others

13/17 (76) 4/17 (24)

2/17 (12) 0 (0)

2/13 (15) 0 (0)

2/7 (29.5) 1/7 (14.5)

Instrumental delivery

5/60 (8.8)

3/22 (13.6)

3/21 (14.2)

2/23 (8.6)

NS

Vaginal delivery

38/60 (63) 

2/22 (9)

5/21 (24)

14/23 (61) 

\0.05 

1-min Apgar score median (min–max)

9 (7–10)

6 (3–7)*

7 (4–8)*

8 (5–10)

5-min Apgar score median (min–max)

9.5 (8–10)

8 (5–10)*

8 (6–10)*

9 (8–10)

\0.05*

Values are in mean ± SD (range) unless other is indicated NS non-significant difference between all groups by one-way ANOVA test * Tukey post test showed significant difference when compared with other groups  

Fisher exact test showed significant difference when compared with other groups

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Table 2 Umbilical artery blood lactate, pH and actual base excess in different fetal heart rate monitoring patterns compared to control group Normal CTG (n = 60)

Late onset deceleration (n = 22)

Atypical variable decelerations (n = 21)

Simple variable decelerations (n = 23)

Blood lactate (mmol/L)

1.86 ± 0.99 (0.4 to 5.1)

6.14 ± 1.66 (3.3 to 9.1)*

6.03 ± 1.63 (2.1 to 8.9)*

2.12 ± 0.81 (1.1 to 4.2) 

pH

7.28 ± 0.06 (7.18 to 7.41)

7.11 ± 0.05 (7.04 to 7.31)*

7.12 ± 0.09 (7.02 to 7.33)*

7.26 ± 0.05 (7.16 to 7.34) 

-5.5 ± 1.88 (-9.0 to 2.0)*

-2.90 ± 1.29 (-5.0 to 1.0) 

Actual base excess (mmol/L)

-2.56 ± 0.70 (-4.10 to 1.10)

-8.03 ± 2.14 (-12 to 3.0)*

Values are in mean ± SD (range) * p value \ 0.0001 compared to controls by t test  

p value is non-significant ([0.05) compared to control by t test

Table 3 Blood lactate, pH and actual base excess in relation to mode of delivery in deceleration groups

Blood lactate (mmol/L) pH Actual base excess (mmol/L)

Late-onset decelerations (n = 22)*

Atypical variable decelerations (n = 21)*

Simple decelerations (n = 23)*

Operative delivery (n = 20)

Normal delivery (n = 2)

Operative delivery (n = 16)

Normal delivery (n = 5)

Operative delivery (n = 9)

Normal delivery (n = 14)

6.10 (3.5 to 9.1)

5.90 (3.3 to 8.8)

5.50 (2.1 to 8.9)

5.40 (2.4 to 8.6)

2.10 (1.3 to 4.3)

2.00 (1.1 to 4.2)

7.10 (7.04 to 7.3) -8.0 (-11.7 to -2.9)

7.10 (7.07 to 7.31) -7.8 (-12.0 to -3.0)

7.12 (7.04 to 7.33) -5.5 (-9 to -1.9)

7.11 (7.02 to 7.31) -5.4 (-9 to -2.0)

7.24 (7.18 to 7.34) -2.9 (-4.8 to -1)

7.25 (7.16 to 7.33) -2.8 (-5.0 to -1)

Values are in median (range) * P value is [0.05 when all blood values in operative deliveries (CS and instrumental) were compared to normal deliveries in all deceleration groups

the atypical variable decelerations group. The median value of blood lactate and cord pH in those newborns was 6.6 and 7.08, respectively.

All groups RS =-0.71

7.5

P< 0.001

pH

7.3

Discussion

7.1

6.9 0.0

2.5

5.0

7.5

10.0

Lactate mmol/l

Fig. 1 Scatter diagram showing the correlation between umbilical arterial cord blood lactate and pH in all participants (n = 126). Spearman’s correlation coefficient (RS) in different FHR groups: normal CTG group (n = 60): RS = -0.62 (p \ 0.05); late onset decelerations group (n = 22): RS = -0.80 (p \ 0.0001); atypical variable decelerations group (n = 21): RS = -0.73 (p \ 0.001); simple variable decelerations group (n = 23): RS = -0.55 (p \ 0.05)

specificity of blood lactate and pH were comparable at the 1 min, while after 5 min, the cord blood lactate had higher sensitivity and specificity to predict newborns with an Apgar score \7 compared to cord pH. Three newborns were admitted to the NCU for oxygen therapy (\4 h) without any signs of encephalopathy. Two of them were in the group of late onset decelerations, and the other one in

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The diagnosis of asphyxia at birth is a critical issue that needs combination of intrapartum and postpartum clinical fetal assessment together with essential laboratory parameters to identify those with higher risk for neurological damage. The current cord blood lactate level in normal CTG group (1.86 ± 0.99) is close to others reported a median of arterial cord blood lactate that ranged from 1.87 to 2.2 mmol/L [14–16], but much lower than Gjerris et al. [10] who reported a mean of 4.63 ± 2.33. A different methodology through measuring lactate in whole blood could be an explanation [10]. The mean value of cord artery blood pH recorded in normal CTG group in current study (7.28 ± 0.06) is close to others reported 7.28 ± 0.05 [15], 7.27 ± 0.05 [16] and 7.24 ± 0.07 [17]. This decrease in pH is a physiologic sequence due to increased carbon dioxide load from the growing fetus, with a limited gas exchange over aging

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Table 4 Correlation between Apgar score and umbilical cord blood lactate and pH in different fetal heart rate patterns Groups of fetal heart rate monitoring patterns

1-min Apgar score

5-min Apgar score

pH

Umbilical cord blood lactate

pH

RS

RS

RS

p value

p value

Umbilical cord blood lactate p value

RS

p value

Normal CTG (n = 60)

0.21

NS

-0.13

NS

0.31

NS

-0.43

NS

Late onset decelerations (n = 22)

0.26

NS

-0.22

NS

0.39

0.07

-0.44

0.06

Atypical variable decelerations (n = 21) Simple variable decelerations (n = 23)

0.07 0.18

NS NS

-0.23 -0.11

NS NS

0.35 0.28

NS NS

-0.41 -0.33

0.07 NS

RS Spearman’s correlation coefficient Table 5 The sensitivity, specificity and the best cut-off value of umbilical artery cord blood pH and lactate for prediction of adverse clinical neonatal outcome Apgar score

Umbilical cord blood pH (n = 126)

Umbilical cord blood lactate (n = 126)

Sensitivity (%)

Specificity (%)

Cut-off

Sensitivity (%)

Specificity (%)

Cut-off

Apgar score \ 4 at 1 min

63

72

7.18

67

75

4.1

Apgar score \ 7 at 5 min

55

78

7.13

68

89

4.8

placental membranes. The high level of fetal hemoglobin type may also affect the buffering capacity of the fetus [17]. The current data confirm the development of fetal metabolic acidosis in late onset decelerations and atypical variable decelerations groups as evidenced by the significantly lower umbilical artery pH and ABE and higher blood lactate compared to normal CTG group. In susceptible fetuses, the repeated uterine contractions cause insufficient placental perfusion. On the fetal side, the O2 level will drop, CO2 will accumulate, and pH will consequently start to drop. If hypoxic conditions persist, anaerobic glycolysis will result and pyruvate will be metabolized to lactate. When the concentration of lactate rises, the extra hydrogen ion (H?) is buffered by HCO3, and the ABE level decreases. SBE is a compute for the buffer capacity of the whole body’s extra cellular fluid compartment. This will lead to a lowering of the buffer capacity, and the fetus can develop a metabolic acidosis [18, 19]. This is evidenced in current study by the significant inverse correlation between cord blood lactate and each of pH and ABE in normal and abnormal CTG groups as lactate increases H? and consequently pH measure the increase in (H?) concentration [8, 10, 20–22]. Our data in late-onset, atypical, and simple variable decelerations showed comparable cord blood lactate, pH, and ABE in patients with operative delivery to those delivered normally. This confirms that the levels of these cord blood markers depend mainly on the degree of fetal hypoxia and acidosis that develops intrapartum regardless of delivery mode. This is in agreement with others reported that concentrations of lactate in umbilical blood samples obtained by cordocentesis in normoxaemic healthy human

fetuses at 17–38 weeks of gestation did not differ from those determined at elective CS at term [16, 20]. Regarding the early neonatal clinical outcome, the current data showed that umbilical cord blood lactate and pH had inverse correlation with the 1- and 5-min Apgar scores in all CTG groups; however, this was not statistically significant. This is in agreement with others [23, 24] reported that Apgar score gives no information of the cause of acidosis/hypoxia and has a very low predictive value in identifying long-term morbidity. This is because it may be affected by other factors such as respiratory obstruction by secretions, the anesthetic drugs, or cardiovascular malformations [23, 24]. As a result, Apgar score is considered a simple and repeatable method to quickly and summarily assess the health of newborn children regardless of the cause. This view is supported by both the American College of Obstetricians and Gynecologists and the American Academy of Pediatrics, who have challenged the use of Apgar score to define birth asphyxia [25]. American College of Obstetricians and Gynecologists have concluded that hypoxia close to delivery, severe enough to cause significant neonatal encephalopathy, should be associated with an umbilical artery pH \7.00, a metabolic component to the acidosis, and low Apgar scores \3 for more than 5 min [25]. Others tried gestational age-adjusted values of umbilical lactate and pH and reported significantly better correlation with Apgar score \7 than crude values; however, for Apgar score \4, the differences were not significant [26]. Through the ROC curves, the values of cord lactate and pH that correspond to the highest sensitivity and specificity were determined at the apex of the curve. We found a

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cut-off value of 4.8 mmol/L of cord blood lactate that had sensitivity and specificity of 68 and 89 % to predict low Apgar score \7 after 5 min. This is comparable to others who reported a cut-off value 4.3 of scalp lactate which could predict the same Apgar score with a sensitivity and specificity of 66 and 69 %, respectively [27]. In agreement with others [15], the comparison between pH and lactate in terms of sensitivity and specificity revealed more reliability of lactate in prediction of Apgar score \7 at 5 min compared to pH. This could be explained by the role of lactate in identifying the severe forms of fetal asphyxia resulting in metabolic or mixed acidosis, a condition that causes persistence of low Apgar score after 5 min rather than the mild forms of respiratory acidosis that mostly improve early with neonatal resuscitation. The small number of newborns admitted to neonatal care unit makes it difficult to withdraw an accurate conclusion for the value of cord blood lactate that predict neonates need oxygen therapy or have neurological affection. In conclusion, the cord blood lactate is reliable and easily measured marker for intrapartum fetal asphyxia with good correlation with cord acid–base status. It has better prediction value than cord pH for newborns with low Apgar score. Further studies are needed with adjusted sample size to find the relation between cord blood lactate and long-term neurological outcome of the newborn. Acknowledgments The author acknowledges Dr. Manal M. Kamal, MD, Physiology Department, Assiut University for her assistance in measurement of umbilical blood lactate and Dr. Maher M. Ahmad, MD, Professor of Pediatrics, Assiut University for his kind supervision to assess the neonates by staff in-charge. Conflict of interest declare.

The author has no conflicts of interest to

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