Hidden Acidosis

Hidden acidosis: an explanation of acid–base andlactate changes occurring in umbilical cord bloodafter delayed samplingP Mokarami,a N Wiberg,b P Olofssona

a Institution of Clinical Sciences, Department of Obstetrics and Gynaecology, Sk�ane University Hospital, Lund University, Malm€o, Swedenb Institution of Clinical Sciences, Department of Obstetrics and Gynaecology, Sk�ane University Hospital, Lund University, Lund, Sweden

Correspondence: Dr P Mokarami, Department of Neurology, Sk�ane University Hospital, S–20502 Malm€o, Sweden.

Email [email protected]

Accepted 25 December 2012. Published Online 10 April 2013.

Objective To explore the ‘hidden acidosis’ phenomenon, in which

there is a washout of acid metabolites from peripheral tissues

in both vaginal and abdominal deliveries, by investigating

temporal umbilical cord blood acid–base and lactate changes after

delayed blood sampling.

Design Prospective comparative study.

Setting University hospital.

Sample Umbilical cord blood from 124 newborns.

Methods Arterial and venous cord blood was sampled

immediately after birth (T0), and at 45 seconds (T45), from

unclamped cords with intact pulsations taken from 66 neonates

born vaginally and 58 neonates born via planned caesarean section

at 36–42 weeks of gestation. Non-parametric tests were used for

statistical comparisons, with P < 0.05 considered significant.

Main outcome measures Temporal changes (T0–T45) in

umbilical cord blood pH, the partial pressure of CO2 (PCO2) and

O2 (PO2), and in the concentrations of lactate, haematocrit (Hct),

and haemoglobin (Hb).

Results In both groups all arterial parameters, except for PCO2in

the group delivered by caesarean section, changed significantly

(pH decreased and the other variables increased). There were

corresponding changes in venous acid–base parameters. When

temporal arterial changes were compared between the two groups,

the decrease in pH and increase in PCO2were more pronounced in

the group delivered vaginally. Neonates born vaginally had

significantly lower pH and higher lactate, Hct, and Hb

concentrations at T0 and T45 in both the artery and the vein. At

T45, arterial PCO2and PO2

levels in the group delivered vaginally

were also significantly higher.

Conclusions Delayed umbilical cord sampling affected the acid–base balance and haematological parameters after both vaginal and

caesarean deliveries, although the effect was more marked in the

group delivered vaginally. The hidden acidosis phenomenon

explains this change towards acidaemia and lactaemia. Arterial

haemoconcentration was not the explanation of the acid–basedrift.

Keywords Blood gases, delayed sampling, hidden acidosis, lactate,

pH, umbilical cord blood.

Please cite this paper as: Mokarami P, Wiberg N, Olofsson P. Hidden acidosis: an explanation of acid–base and lactate changes occurring in umbilical cord

blood after delayed sampling. BJOG 2013;120:996–1002.

Introduction

Delayed umbilical cord clamping at vaginal delivery results

in a decrease in pH and base excess (BE), and an increase

in the partial pressure of O2 (PO2), the partial pressure of

CO2 (PCO2), and lactate concentration in the umbilical

artery.1–3 These changes towards acidaemia and lactaemia

can be explained by the ‘hidden acidosis’ phenomenon.

During uterine contractions, the fetal circulation is centra-

lised at the expense of perfusion of low-priority organs and

peripheral tissues,4 with a build-up of acid metabolites

peripherally. When the newborn starts to breathe suffi-

ciently the peripheral perfusion is restored and the

‘trapped’ metabolites surge into the central circulation and,

after some seconds, can be detected in umbilical cord

blood.3 The phenomenon has also been demonstrated in

animal studies at the restoration of the peripheral circula-

tion after provoked hypovolaemic shock.5,6 Soon after vol-

ume expansion has started, a rapid drop in pH and

increase in lactate concentration are seen. In animal limb

tourniquet ischaemia–reperfusion experiments, a similar

phenomenon is seen during reperfusion.7,8

996 ª 2013 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2013 RCOG

DOI: 10.1111/1471-0528.12234

www.bjog.orgGeneral obstetrics

Our hypothesis was that hidden acidosis occurs in the

newborn (Figure 1). As newborns after planned caesarean

delivery (caesarean section) seldom show acrocyanosis, we

hypothesized that hidden acidosis would be most pro-

nounced after vaginal delivery. The opening of peripheral

vascular beds might result in changes in haemoconcentra-

tion in the cord blood, and therefore we investigated tem-

poral changes not only in blood gases and lactate

concentration, but also in haematocrit (Hct) and total hae-

moglobin (ctHb) concentration.

Methods

Arterial and venous umbilical cord blood were sampled from

124 newborn singletons immediately after birth (T0), and

again at 45 seconds (T45), from unclamped umbilical cords

with intact pulsations. The women’s length of gestation was

determined at an early second trimester ultrasound, and all

were found to be at 36–42 weeks of gestation. Of the 124

neonates, 66 were born vaginally in cephalic presentation

and 58 were delivered by planned caesarean section. The

newborns included in the study were expected to have no

need of immediate rescue procedures that would interfere

with the delayed cord clamping. The women who delivered

vaginally were included in a previously published study.3

Women in the group delivering vaginally were recruited

to the study at admission to the labour and delivery ward,

and women in the group delivering by caesarean section

were asked to participate a few hours before the operation.

All caesarean sections were planned and the indications

were breech presentation or maternal request. Women

undergoing spinal anaesthesia were placed in supine posi-

tion, tilted 15º to the left, and received prehydration. Bupi-

vacaine and fentanyl were used for spinal anaesthesia.

Simultaneously, an intravenous infusion of ephedrine

(50 mg in 500 ml of sodium chloride solution) was started

and adjusted with the aim to maintain a mean arterial

pressure within 25% of its initial value. Women undergo-

ing general anaesthesia also received prehydration. Drugs

administered at general anaesthesia were thiopental, sux-

amethonium, and sevoflorane. After cord clamping, all

women received oxytocin.

During cord blood sampling, babies delivered vaginally

were placed on the abdomen of the mother, whereas babies

born by caesarean section were placed between the

mother’s legs and kept warm under a towel. The procedure

was meticulously prepared, and the samples were taken and

analysed by one of the authors (N.W.), who was not

involved in the obstetric care of the women. Blood was

drawn first from the cord artery and then, within a few

seconds, and at the same location on the cord, from the

vein. The next pair of samples were taken 45 seconds later,

and the needle punctures were made a few millimetres clo-

ser to the placenta. A 0.6- or 0.9-mm needle was used, and

the samples were collected in 2–ml pre-heparinised plastic

syringes. A minimum of 0.5 ml of blood from each vessel

was used for analysis in the blood gas analyser (ABL735;

Radiometer A/S, Copenhagen, Denmark). All samples were

analysed within 15 min, in chronological order. The radi-

ometer analyser works by measuring pH and PCO2by

potentiometry, PO2 and lactate by amperometry, and ctHb

by spectrophotometry. ctHb includes deoxy-, oxy-,

carboxy-, and methemoglobin. Hct is available as a derived

parameter, calculated according to the formula: Hct =0.0485 9 ctHb + 8.3 9 10�3. The analyser was operated

in an accredited laboratory (Laboratory Medicine Sk�ane,

Clinical Chemistry, Lund and Malm€o).

All women in labour were monitored with cardiotocog-

raphy during the second stage of labour. Small for gesta-

tional age (SGA) was defined as a birthweight below – 2

SD from the gestational age-adjusted mean value, appropri-

ate for gestational age (AGA) was defined as a birthweight

within the mean � 2 SD range, and large for gestational

age (LGA) was defined as a birthweight above the

mean + 2 SD.9

Statistical analysesThe Mann–Whitney U test was used for comparison of

continuous parameters between groups, and the Wilcoxon

signed-ranks matched-pairs test was used for longitudinal

comparisons. Values are reported as median and range or

mean with 95% confidence interval (95% CI), as appropri-

First few minutes after birth

pH

Lactate

PostpartumLabour Birth

Figure 1. Schematic illustration of the hidden acidosis phenomenon.

The grey box represents the first few minutes after birth, when a steep

decrease in pH and an increase in lactate concentration are first seen,

according to the hypothesis.

ª 2013 The Authors BJOG An International Journal of Obstetrics and Gynaecology ª 2013 RCOG 997

Acid–base changes after delayed umbilical cord sampling

ate. A two-tailed P < 0.05 was considered to be statistically

significant. Statistical analyses were performed with the aid

of STATVIEW� (SAS Institute, Cary, NC, USA). As umbilical

cord blood gas and lactate values are dependent on gesta-

tional age,10–12 comparisons between groups delivered vagi-

nally and by caesarean section were also performed using

cord arterial pH adjusted to a gestational age of 280 days,

according to the regression coefficient �0.00096 per day of

gestational age.10

Results

The characteristics of the study population are shown in

Table 1. Gestational age at delivery was significantly lower,

and Apgar score (AS) at 1 minute was significantly higher,

in the group delivered by caesarean section. One newborn

had an AS of 4 at 1 minute, but otherwise all scores at

1 minute were � 8 and at 5 and 10 minutes were � 9.

Serial blood samples were taken in all 124 cases, but four

analyses at T0 (one vaginal delivery and three caesarean

sections) and ten analyses at T45 (six vaginal deliveries and

four caesarean sections) failed because of instrument failure

or blood clotting. For each parameter, only cases with valid

measurements obtained at both T0 and T45 were included

in the statistical analyses. Data for arterial and venous

acid–base and haematological measurements are shown in

Tables 2 and 3.

Longitudinal changes between T0 and T45

Longitudinal changes in arterial blood gases, and in lactate,

Hct, and ctHb concentrations are illustrated in Figure 2.

With the exception of PCO2in the group delivered by cae-

sarean section (P = 0.4), all blood gas and lactate parame-

ters changed significantly. Acid–base changes in venous

blood were in the same directions as in arterial blood,

although in the group delivered vaginally only the increase

in lactate was significant (P = 0.001), and in the group

delivered by caesarean section only the decrease in pH

(P = 0.03) and increase in lactate (P < 0.0001) were signifi-

cant (not shown in Figure 2). Hct and ctHb increased sig-

nificantly in the artery in both groups, whereas venous

values decreased significantly in the group delivered vagi-

nally (P � 0.04), and remained unchanged in the group

delivered by caesarean section (P � 0.2).

Vaginal versus caesarean deliveryWhen longitudinal arterial pH, lactate, and PCO2

changes

were compared between groups, the decrease in pH and

increase in PCO2were found to be significantly greater in

the group delivered vaginally (P � 0.04), but there was no

statistically significant difference between the groups

regarding the increase in lactate concentration from T0 to

T45 (P = 0.9). Adjusting pH for the difference in gesta-

tional age between the groups did not change the results.

Neonates born by vaginal delivery had significantly lower

pH values and higher lactate, Hct, and ctHb concentrations

at T0 and T45, in both the artery and the vein, compared with

neonates delivered by caesarean section (Tables 1 and 2). At

T45, PCO2and PO2

in the artery in the group delivered vagi-

nally were also significantly higher.

Spinal versus general anaesthesiaNeonates in the group delivered by caesarean section with

spinal anaesthesia (n = 52) had lower pH values, and

higher PCO2and lactate concentration at T0, compared with

neonates in the general anaesthesia group (n = 6), but only

the difference in lactate concentration was statistically sig-

nificant (P = 0.03).

Table 1. Characteristics of the study population (n = 124)

Vaginal delivery

(n = 66)

Caesarean

delivery (n = 58)

Maternal characteristics

Duration of second

stage of labour (min)

41 (5–234) –

Duration of

pushing (min)

24 (4–90) –

Induction of labour 5 (7.6%) –

Instrumental birth 9 (13.6%) –

Drugs administered

Pethidin 6 (9.1%) –

Oxytocin 31 (47.0%) –

Nitrous oxide 50 (75.8%) –

Anaesthesia

Epidural 15 (22.7%) –

Spinal – 52 (90.0%)

General – 6 (10.0%)

Newborn characteristics

Gestational age

(weeks)*

40+0 (36+0 – 42+0) 38+4 (36+4 – 40+3)

Birthweight (g) 3595 (2560–4405) 3535 (2516–5320)

SGA 3 (4.5%) 0

AGA 62 (93.9%) 47 (81.0%)

LGA 1 (1.5%) 11 (19.0%)

Apgar score

1 minute* 9 (4–10) 9 (8–10)

5 minute 10 (8–10) 10 (7–10)

10 minute 10 (9–10) 10 (9–10)

Cardiotocography

Intermediate 13 (19.7%) –

Pathological 3 (4.5%) –

*The difference in gestational age and Apgar score at 1 minute was

statistically significant (Mann–Whitney U test; P � 0.03) between

the two groups.

Values are median (range) or number of cases (%).


Mokarami et al.

Discussion

This study showed significant changes in acid–base and

haematological parameters in umbilical cord blood when

sampling was delayed by 45 seconds, with these changes

being more marked for pH and PCO2in the group delivered

vaginally. The similar increases in lactate concentration in

the two groups indicate that considerable hidden acido-

sis was also present in the group delivered by caesarean

section.

The lack of change in venous PCO2indicates that placen-

tal perfusion and gas exchange were maintained during the

first 45 seconds, after both vaginal and abdominal deliver-

ies. Thus, the temporal increase in arterial PCO2must be a

result of CO2 inflow from the newborn, and not from the

placenta, or of an accumulation of CO2 in the blood cir-

cuit. Moreover, the significant increase in PO2indicates the

rapid establishment of functional pulmonary ventilation,

which would result in the escape of CO2 and in a lowering

of PCO2unless there was a considerable continuing fetal

Table 2. Arterial blood gas, lactate, haematocrit (Hct), and total haemoglobin (ctHb) concentration median (range) values obtained immediately

after birth (time T0), and again 45 seconds later (T45), in unclamped umbilical cords with intact pulsations after vaginal delivery and caesarean

delivery

Vaginal Caesarean T0 T45 Vaginal versus

caesarean

Vaginal Caesarean Vaginal Caesarean Significance of

difference (P)

n n Median (range) Median (range) Median (range) Median (range) T0 T45

pH 58 39 7.235 (7.008–7.379) 7.305 (7.162–7.397) 7.207 (7.005–7.384) 7.296 (7.116–7.424) <0.0001 <0.0001

PCO2(kPa) 58 39 7.55 (5.24–11.6) 7.30 (5.86–9.56) 7.87 (5.94–11.8) 7.57 (5.56–10.4) 0.3 0.03

PO2(kPa) 57 39 2.31 (0.62–7.93) 1.99 (1.18–3.72) 2.66 (1.09–4.94) 2.28 (1.18–3.25) 0.1 0.02

Lactate

(mmol/l)

56 37 4.8 (2.0–13.3) 1.8 (1.1–4.8) 5.5 (2.3–13.3) 2.2 (1.5–6.2) <0.0001 <0.0001

Hct 57 38 0.507 (0.051–0.625) 0.452 (0.409–0.585) 0.514 (0.423–0.635) 0.460 (0.372–0.583) <0.0001 <0.0001

ctHb

(g/l)

57 38 167 (134–205) 148 (133–191) 168 (138–208) 151 (121–191) <0.0001 <0.0001

The Mann–Whitney U test was used for group comparisons.

Table 3. Venous blood gas, lactate, haematocrit (Hct), and total haemoglobin (ctHb) concentration median (range) values obtained immediately

after birth (time T0), and again 45 seconds later (T45), in unclamped umbilical cords with intact pulsations after vaginal delivery and caesarean

delivery

Vaginal Caesarean T0 T45 Vaginal versus

caesarean

Vaginal Caesarean Vaginal Caesarean Significance of

difference (P)

n n Median (range) Median (range) Median (range) Median (range) T0 T45

pH 64 41 7.331 (7.068–7.471) 7.371 (7.320–7.479) 7.329 (7.470–7.474) 7.367 (7.318–7.469) <0.0001 <0.0001

PCO2(kPa) 64 41 5.49 (3.91–9.70) 5.78 (4.37–7.46) 5.42 (4.05–9.54) 5.77 (4.69–7.54) 0.2 0.1

PO2(kPa) 63 41 3.57 (1.46–15.70) 3.46 (1.87–7.45) 3.68 (1.52–7.38) 3.46 (1.40–6.43) 0.6 0.9

Lactate

(mmol/l)

60 40 4.6 (1.9–10.9) 1.5 (1.1–2.7) 4.7 (2.1–10.8) 1.6 (1.2–3.0) <0.0001 <0.0001

Hct 63 38 0.515 (0.401–0.648) 0.455 (0.410–0.585) 0.513 (0.058–0.633) 0.456 (0.389–0.590) <0.0001 <0.0001

ctHb

(g/l)

64 39 168 (131–212) 148 (133–191) 168 (126–208) 149 (127–193) <0.0001 <0.0001

The Mann–Whitney U test was used for group comparisons.



contribution. As it is unlikely that the CO2 contribution

was a result of a sudden rise in neonatal metabolism, a

washout of CO2 from peripheral tissues is the most plausi-

ble explanation for this finding.

After 45 seconds, arterial blood showed a small but sig-

nificant haemoconcentration and venous blood showed a

haemodilution in the group delivered vaginally. A relevant

question is, then, whether these concentration changes

could have influenced the temporal acid–base and lactate

changes. According to Stewart’s physicochemical concept, a

change towards alkalosis should occur during haemocon-

centration, as dehydration results in a higher [OH�].13 In

the present study, the changes in haemoconcentration par-

alleled changes towards acidosis in the artery, indicating

that the temporal acetous change was not a result of the

haemoconcentration.

The study was performed in cases in which minimal

neonatal assistance was expected to be required, and only

two newborns in the group delivered vaginally and none

in the group delivered by caesarean section had an umbil-

ical artery pH <7.10 in the first samples. Both these new-

borns had a pathological cardiotocogram. One newborn

was vigorous immediately, with 1-, 5-, and 10-minute AS

scores of 8, 9, and 10, respectively, whereas the other was

initially moderately depressed, and had corresponding AS

scores of 4, 8, and 10. Interestingly, in the newborn with

a 1-minute AS score of 8, the blood gas and lactate values

deteriorated further by 45 seconds of age: pH changed

7,18

7,20

7,22

7,24

7,26

7,28

7,30

7,32

7,0

7,2

7,4

7,6

7,8

8,0

8,2

8,4

8,6

45

46

47

48

49

50

51

52

53

54

1,5

2,0

2,5

3,0

3,5

4,0

4,5

5,0

5,5

6,0

6,5

145

150

155

160

165

170

175

1,9

2,0

2,1

2,2

2,3

2,4

2,5

2,6

2,7

2,8

2,9

pHP O

2 (kP

a)H

ct (%

)

P CO

2 (kP

a)ct

Hb

(g/L

)La

ctat

e (m

mol

/L)

T0 T0T45 T45

Caesarean deliveryVaginal delivery

*

****

***

NS

*

***

****

****

********

***

Figure 2. Measurements of arterial umbilical cord blood gases, and concentrations of lactate, haematocrit (Hct), and total haemoglobin (ctHb)

obtained immediately after birth (T0), and then again 45 seconds later (T45), in unclamped umbilical cords with intact pulsations after vaginal and

caesarean deliveries. The figure shows mean values and 95% confidence intervals. The Wilcoxon signed-ranks test was used to compare values at

T0 and T45: *P < 0.05; **P < 0.01; ***P < 0.001; ****P < 0.0001; NS, not significant.


Mokarami et al.

from 7.06 to 7.02; PCO2changed from 10.0 to 10.5 kPa;

BE changed from –12.7 to –15.3 mmol/l; and lactate chan-

ged from 12.2 to 12.9 mmol/l. In the depressed newborn,

the values remained mainly unchanged: pH was 7.01 at

both time points, PCO2changed from 11.2 to 11.8 kPa, BE

changed from –14.9 to –14.4 mmol/l, and lactate concen-

tration was 13.3 mmol/l at both time points. These obser-

vations further support the hypothesis that hidden acidosis

is a physiological phenomenon, occurring in newborns with

a rapidly established circulation.

It was not expected that the hidden acidosis phenome-

non would occur so clearly in neonates born by caesarean

section, as these neonates were not exposed to hypoxic

stress by uterine labour contractions; however, it is well

known that fetal/neonatal effects occur during regional

anaesthesia for planned caesarean section. Despite precau-

tions in terms of prehydration and vasopressor administra-

tion, spinal anaesthesia in particular is frequently associated

with maternal hypotension and lower umbilical cord arte-

rial pH.14–18 Vasopressor substances can cross the pla-

centa,14,19–22 and the maternal supine wedged position

during caesarean section frequently results in fetal heart

rate changes as a result of occult aortocaval compression.23

Doppler ultrasound has shown uteroplacental circulation to

be affected after spinal blockade.16,19,24,25 In concordance

with these findings, the present study showed higher lactate

values in the spinal anaesthesia group than in the general

anaesthesia group. It seems that, even with the most mod-

ern techniques for spinal anaesthesia, this side effect is dif-

ficult to avoid.26

An interesting finding was that at T0, PO2was similar in

the groups delivered vaginally and by caesarean sections,

but at T45 it was significantly higher in the group delivered

vaginally, as a result of a steeper increase. This demon-

strates the protective role of vaginal delivery, with the more

effective release of lung surfactant and alveolar expansion,

absorption of pulmonary fluid, and rapid circulatory tran-

sition to extra-uterine life. At 45 seconds, alveolar clearance

of fluid and alveolar expansion are the most important

processes.27

Strengths and weaknessesRepeated blood sampling performed by an experienced

obstetrician and analyses within 15 minutes in chronologi-

cal order minimised the sampling and measurement errors.

The inclusion of only newborns presumed to be vigorous

makes extrapolation to asphyxiated newborns problematic.

InterpretationEven small blood gas changes can affect the interpretation

of a newborn’s status and lead to a false diagnosis of acido-

sis, as we have previously demonstrated.3 Hypoxic neonates

are expected to have a more pronounced circulatory cen-

tralisation and hidden acidosis, and, as they already have

lower pH levels, an additional decrease is more likely to tip

them below the lower limit of the reference interval. It

would be difficult to create reliable normal reference inter-

vals taking late cord blood sampling into account, because,

as discussed above, vigorous newborns would show changes

towards acidaemia, lactaemia, and hypercapnia, whereas

depressed newborns would show small changes.

Conclusion

Delayed cord blood sampling with intact pulsations affected

umbilical acid–base values and haematological parameters

following both vaginal and caesarean deliveries. A change

towards acidaemia and lactaemia can be explained by the

hidden acidosis phenomenon. A small degree of haemocon-

centration occurred in arterial blood, and haemodilution

occurred in venous blood, but these changes could not

explain the change in acid–base status.

Disclosure of interestsThe authors state explicitly that there are no conflicts of

interest in connection with this article.

Contribution to authorshipPM was involved in the conception and planning of the

study, analysis of the data, and writing of the article; NW

was involved in the conception, planning, and carrying out

of the study, analysis of the data, and writing of the article.

PO was involved in the conception and planning of the

study, analysis of the data, and writing of the article.

Details of ethics approvalThe study was approved on 24 February 2006 by the Cen-

tral Ethical Review Board, Stockholm, Sweden (reference

number €O 50–200), and all the women gave their informed

oral and written consent to participate in the study.

Funding

This study was supported by grants from Region Sk�ane

and the Medical Faculty at Lund University (ALF). The

funding sources had no role in the writing of the article or

in the decision to submit it for publication.

AcknowledgementNone. &

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