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Neonatal Transitional Physiology:
A New Paradigm
Early clamping of the umbilical cord at birth, a practice developed without adequate evidence,
causes neonatal blood volume to vary 25% to 40%. Such a massive change occurs at no other
time in one’s life without serious consequences, even death. Early cord clamping may impede
a successful transition and contribute to hypovolemic and hypoxic damage in vulnerable new-
borns. The authors present a model for neonatal transition based on and driven by adequate blood
volume rather than by respiratory effort to demonstrate how neonatal transition most likely oc-
curs at a normal physiologic birth. Key words: capillary erection, cardiopulmonary adaptation,
the first breath, hypovolemia, neonatal blood volume, neonatal transition, nuchal cord, placental
transfusion, polycythemia, postpartum placental respiration, umbilical cord clamping
Judith S. Mercer, CNM, DNSc, FACNM
Associate Clinical Professor
University of Rhode Island
Kingston, Rhode Island
Rebecca L. Skovgaard, CNM, MS
Associate in the Department of
Obstetrics and Gynecology
University of Rochester at Highland
Hospital
Rochester, New York
Assistant Professor in the School
of Nursing
University of Rochester
Editorial Staff, Strong Perifax
CURRENT ANALYSIS OF knowledge
related to neonatal transitional phys-
iology reveals that early cord clamping
may interfere with completion of a normal
physiologic neonatal transition. An end
result of this interference with transitional
physiology is a 25% to 40% reduction in
the neonate’s blood volume.1,2In other
circumstances over the life span, such
a massive restriction in blood volume
would result in severe consequences,
even death. Human babies are remarkably
adaptable, and in most cases no appar-
ent harm is initially evident. However,
practitioners are obligated to establish a
rationale for early neonatal management
and then to apply it in practice. The exist-
ing evidence suggests that the intervention
of early cord clamping evolved without
adequate evidence-based rationale and,
accordingly, is deserving of careful sci-
entific review.3The debate remains:
what is optimal care—what do all babies
need initially? Do some babies experience
The authors would like to thank Margaret McGrath,
PhD, RN, for her inspiration, encouragement, and
guidance throughout the development of this work.
Submitted for publication: November 9, 2000
Accepted for publication: April 20, 2001
56
J Perinat Neonat Nurs 2002;15(4):56–75
c
°2002 Aspen Publishers, Inc.
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Neonatal Transitional Physiology 57
harm because of inadequate blood and
red cell volume? Synthesizing knowledge
from several disciplines, this article
presents a new model for explaining
physiologic neonatal transition that pro-
motes an alternative view about placental
transfusion and the importance of delayed
cord clamping in the first minutes of life.
The application of this model to practice
may lead to benefits for all newborns and
may be especially important for compro-
mised infants who do not have adequate
perfusion.
Two factors, the singular role of the
red blood cell (RBC) in the body and the
idea that a significant reduction in RBCs
at birth does no harm, must be explored
in examining any relationship between
neonatal transition and cord clamping
interval. In recent years, advances in
physiological measurement tools and
understanding of physiologic and patho-
logic processes have been made that may
substantiate the evidence against early
cord clamping. Application of this new
knowledge to the issue of fetus-to-neonate
transition argues for a reformulation of
current practice and presents a rational
basis for optimal clinical practice. Of key
importance are these two facts: that the
only oxygen-carrying component in the
body is the RBC,4and that, in a typical
approach to early neonatal management
today, immediate cord clamping, a reser-
voir of RBCs is routinely, according to
tradition, discarded with the placenta.
The problem occurs when oxygen deliv-
ery is the primary concern in neonatal
illness. These include respiratory dis-
tress syndrome, persistent pulmonary
hypertension, necrotizing enterocolitis,
and hypoxic-ischemic encephalopathy.
Discovery of any potential relationship
of the pathologic processes of these
conditions to essential hypovolemia
in the newborn has been hampered
by the fact that there is no reliable, avail-
able, clinically useful measure for RBC or
blood volume in the neonate.2The lack
of evidence to guide practice, the assump-
tion that early cord clamping can “do no
harm,” and the relative connection that
the RBC is the only transporter of oxygen
lead to the conclusion that reexamina-
tion of the consequences of early versus
delayed cord clamping is warranted.
The second key issue in explaining the
normal neonatal transition is the rationale
for the establishment of breathing. Tradi-
tional views for causality of first breath
have focused exclusively on the respi-
ratory and neurological system.5–8 These
theories have claimed asphyxia at birth,
touch, cold and sensory stimulation, frog
breathing, and chest recoil as potential
explanations for the first breath.7,8These
theories were developed prior to the
discovery that fetuses perform breathing
movements in utero. None of these ex-
planatory theories have held up to scrutiny
upon closer examination.9While early
cord clamping appears to hasten an in-
fant’s first breath, severely depressed ba-
bies do not breathe spontaneously—an in-
teresting paradox worthy of investigation.
Alternate analysis and synthesis of cur-
rent knowledge can produce a more plau-
sible model for the pathways to successful
extrauterine respiration.
LITERATURE REVIEW
In the last decade, there has been a
resurgence of interest in the issue of
optimal cord clamping time and its
effect on neonatal transition. Recent
studies show the benefits of delayed cord
clamping as improving the neonate’s
cardiopulmonary adaptation,10 blood
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Table 1. Effects of placental transfusion on human neonatal systems in the first 6 hours
after birth
Blood volume/Component measures
•Blood volume17–21 +
•Red cell mass17–21 +
•Plasma volume17–19,21 +
•Hematocrit15,16,21–24 =,+
Vascular pressures
•Atrial pressure25 +
•Pulmonary artery26 +
•Systolic blood pressure11,12,23 +
Blood flow
•Right and left ventricular output21 =
•Renal blood flow27 +
•Cutaneous blood flow (skin temperature)28 +
•Systemic and pulmonary resistance10,29 +
•Blood viscosity10,21,30 +
•Vascular hinderance10 −
•Red blood cell flow10 +
•Cerebral red blood cell flow10 +
•Gastrointestinal red blood cell flow10 +
Other cardiac effects
•Heart rate26,31 =
•Cardiac size23 +
•EKG signs of cardiac load22 +
•Preejection period22,32 +
•Murmurs23 −
Renal function
•Effective renal blood flow27 +
•Glomerular filtration rate27 +
•Urine flow27 +
•Urinary sodium excretion27 −
Respiration
•Respiratory rate31,33 +
•Lung compliance33,34 −
•Function residual capacity33,34 −
•Expiratory grunting31 +
Key: +=increased; −=decreased; ==no change found.
pressures,11–13 oxygen transport and
red blood cell flow,10,14 days on oxygen
and ventilation,15 and anemia.16 Earlier
studies demonstrated consistent physio-
logical effects in newborns.17–34 Table 1
summarizes the findings.
What is not agreed upon by clinicians
and researchers is the meaning of the
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Neonatal Transitional Physiology 59
findings—are they harmful or beneficial?
Delayed cord clamping seems to prevent
shock-like parameters and anemia (refer to
Table 1). However, concerns exist about
volume overload and polycythemia.35–37
Unfortunately, the wide range of study de-
signs and definitions of variables prevents
a meaningful meta-analysis of the stud-
ies. An additional shortcoming is that few
studies evaluate outcomes beyond the first
few hours after birth. The volume of di-
verse studies and the lack of an organiz-
ing framework for understanding this re-
search thwart any attempt to synthesize
the literature or direct further knowledge
development. A theoretical model for the
transition from fetus to neonate is essen-
tial to establish the blueprint for under-
standing this critical physiologic process.
A gap exists because no current model
for neonatal transition adequately explains
the relationships among oxygen transport,
RBC volume, and initiation of breathing, or
predicts the effects of early versus delayed
cord clamping.
The goal of a theoretical model is to
connect and find meaning in a group
of related concepts for the purpose of
understanding, describing, or explaining
a phenomenon.38 Such models provide
and dictate hypotheses for research. Test-
ing and further development may lead to
prediction of outcomes and prescription
for practice. Clinical sciences need pre-
scriptive models to guide interventions
and to provide underlying rationale for
A gap exists because no current model
for neonatal transition adequately
explains the relationships among oxygen
transport, RBC volume, and initiation of
breathing, or predicts the effects of
early versus delayed cord clamping.
practice.39 The development and use of
models to direct research reduces the risk
that a single factor, examined out of con-
text, will direct interventions. The fol-
lowing situation-specific model presents
a description of and explanation for the
physiologic processes of normal neonatal
transition.
The hypothesis proposed is that a suc-
cessful neonatal transition is dependent
upon a newborn having an adequate blood
volume to recruit the lung for respiratory
function through capillary erection and
an adequate red cell volume to provide
enough oxygen delivery to stimulate and
maintain respiration. The mechanism that
initiates fetal breathing in utero is cur-
rently unknown, but it is thought to be
sensitive to oxygen.9,40 This same oxygen-
sensitive mechanism is the more likely
candidate to begin and maintain neona-
tal breathing at birth. Capillary erection
may also be important for other vulnera-
ble structures in the neonate’s body. The
explanation of origins for this model rests
upon the development of an adequate
blood volume in the neonate—a substan-
tially greater blood volume than is neces-
sary for the fetus during intrauterine life,
when maternal “life support” obviates the
need for much fetal organ function.
This model for successful neonatal
transition takes into account the research
findings related to timing of cord clamping
and the evidence for physiological mecha-
nisms underlying this dramatic transition
to life after birth. The model is dia-
grammed and the relevant documentation
to support the model is summarized.
OVERVIEW OF THE MODEL
Figure 1 presents an overview of the
Blood Volume Model for physiologic
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Fig 1. The blood volume model for physiologic neonatal transition.
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Neonatal Transitional Physiology 61
neonatal transition. The following para-
graphs detail the processes summarized in
the model.
In the fetal state, one third to one half
of the fetal-placental blood volume is in
the placenta (Step 1). The essential process
of respiration, gas exchange, takes place
in the placenta. Within the fetus, the pul-
monary circulation receives only 8% of the
cardiac output (CO). The vast majority of
blood volume contained within the fetus
supports systemic circulation. There is no
apparent indication that demands for sys-
temic circulation decrease at the time of
birth. In fact, the opposite is most likely
true, as the gut and all other organs gain
increased function at birth. A dramatic in-
crease in pulmonary circulation occurs,
demanding 40% to 55% of the neonatal
CO for extrauterine respiration. This tran-
sition requires a redirection of the CO and
an increase in blood volume if adequate
perfusion to other vital structures is to be
maintained.
During birth, the uterine myometrium
contracts around the emptying uterine
cavity, causing compression of the pla-
centa and transfer of blood to the fetus/
neonate (Step 2). Second stage contrac-
tions generate intrauterine pressures of 80
to 100 mmHg and force blood from the pla-
centa to the fetus. This process is depen-
dent on three factors: (1) a patent umbilical
vein; (2) a decrease in the blood volume
remaining in the placenta; and (3) an in-
crease in the corporal fetal/neonatal blood
volume, blood pressure, and oxygen lev-
els. The rise in fetal/neonatal blood pres-
sure (due to increased blood volume,
Step 3) overrides the high pulmonary vas-
cular resistance to begin the process of
lung recruitment via capillary erection
(Step 4). Increased blood pressure and
blood flow cause the erection of alveo-
lar capillaries that support the alveolar
structure and recruit the lung tissue.41 Es-
sentially, a capillary network surrounds
each alveolus as a collapsed, fluid-filled
sphere in the fetal state. When the capillary
network is perfused at birth, hydrostatic
pressure expands the sphere secondary
to increased pressure from full expansion
(erection) of the capillary plexuses cover-
ing each alveolus. Each alveolus, attached
to the capillary network through elastic
fibers in the extracellular matrix, is pas-
sively pulled open to an expanded state
(see Fig 2) allowing effortless entry or air
(Step 4C).42
The alveolus is further made ready for
the first breaths as lung fluid diffuses
across the alveolar-capillary membranes,
driven by the higher colloid concentration
within the capillaries (Step 4B). When the
unclamped umbilical cord continues to
pulsate, it allows the newborn to equili-
brate blood volume, oxygen levels, and
pH through ongoing placental exchange
(Step 5A). The increased red blood cell
flow raises the level of oxygen (Step 5B),
stimulating the respiratory center to
initiate breathing—exactly the same
mechanism used to initiate fetal breathing
movements in utero (Steps 5C and 6).
Compression of the placenta continues as
the uterus empties, transferring more of
the placental-fetal blood to the baby. Gas
exchange and acid-base adjustment may
continue during this transition. When
the oxygen level in the newborn’s venous
blood is elevated from 15 mmHg (fetal lev-
els) to 36 mmHg, the normal extrauterine
level, the umbilical arteries close, shutting
down any further blood flow from the
infant’s body to the placenta (Step 7). The
next few uterine contractions may squeeze
a small amount of additional remaining
blood through the umbilical vein to the
infant, ensuring maximum RBCs for oxy-
genation and normal infant blood volume.
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Fig 2. Schema of respiratory unit: relationship of alveoli and capillary plexuses. Source: Copyright,
1999. Icon Learning Systems, LLC, a subsidiary of Hava MediMedia USA Inc. Reprinted with per-
mission from ICON Learning Systems, LLC, illustrated by Frank H. Netter, MD. All rights reserved.
Documentation and support for each step
in the model follow.
Documentation and References for Model
The following section presents the ra-
tionale, documentation, and references for
the processes in the model shown in
Figure 1. Each process in the model is re-
iterated before discussion. Although cre-
ation of a model allows for conjecture,
most of the concepts included here are
well documented in published studies. By
necessity, each step in the model is dis-
cussed as though it happens in linear or-
der, although, in fact, the model functions
in a recursive pattern until equilibrium is
reached.
Step 1: In the fetal state, 40% of the CO
goes to the placenta while only 8% goes to
the fetal lungs.
In the fetal state, one third (full-term) to
one half (pre-term) of the blood in the fetal-
placental circulation (FPC) at any point
in time is in the placenta fulfilling the
respiratory function of gas exchange.2,17
Within the fetus, the circulation to the
lungs receives 8% to 10% of the CO. A dra-
matic increase of 32% to 47% in respira-
tory circulation occurs at birth, demanding
40% to 55% of the CO. Adequate perfusion
of both the respiratory and systemic cir-
culations in the neonate requires a partial
transfusion of the placental blood volume
to the neonate.
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Neonatal Transitional Physiology 63
Step 2: Second stage uterine contractions
create pressures of 80 mmHg or more in
the uterus, transferring blood volume to
the fetus.
Caldeyro-Barcia and colleagues43 docu-
mented uterine contractions of approxi-
mately 80 mmHg pressure within the uter-
ine cavity as the fetus descends into the
birth canal. This pressure, exerted inter-
mittently on the placenta acts to force addi-
tional placental blood into the fetus during
contractions before and immediately after
birth while still allowing for fetal-maternal
exchange between contractions.44 As the
uterus extrudes the fetal head (one fourth
of fetal mass) and body, it effectively
compresses the placenta, causing more of
the fetal-placental blood volume to trans-
fer to the infant. The pressure of 80 mmHg
is equal to Jaykka’s findings that pressures
of 80 mmHg are required to overcome the
pulmonary vascular resistance in cadaver-
ous fetal lungs45,46 (see below).
Step 3: Increased pressure on the pla-
centa forces increased perfusion and be-
gins to open the pulmonary vessels.
Increased uterine pressures of second
stage labor and birth may begin the
process of increasing perfusion.43 Yao,
Hirvensalo, and Lind documented in-
creased placental transfusion in babies af-
ter maternal contractions.44 Higher atrial
and pulmonary artery pressures were
found in late-clamped (LC) versus early-
clamped (EC) infants in the first few hours
after birth, demonstrating increased perfu-
sion and more pulmonary capillary filling
in the LC infants.25,26
Step 4A: Increased perfusion leads
to capillary erection in the pulmonary
vessels.
Jaykka’s45,46 physiologic adaptation
theory of capillary erection in the lungs
offers a logical explanation for the phe-
nomenon of lung recruitment at birth.
Jaykka concluded that, at birth, the sud-
den entry of blood under pressure into
the pulmonary capillaries that surround
each alveoli causes the alveoli to become
individually symmetrically erect (re-
cruited), thus easing entry of air. Jaykka
designed an experiment to test the
process of inflation using accompa-
nying microscopic anatomy of the
lung from stillborn infants and fetal
lambs. He tested the effect of inflation
alone, the effect of forcing dye through
the pulmonary artery to mimic pulmonary
perfusion, and a combination of these two
methods.
First, he inflated the lungs with air alone
and found that the expansion did not pro-
ceed uniformly. He had difficulty injecting
the India ink to mimic capillary circulation
when he attempted to do so after the in-
flation. On microscopic examination,
alveolar walls were found to be irregular
and thin in shape and stretched around
globular air spaces with considerable
areas remaining unstained (unrecruited),
as demonstrated in Figure 3. Next, in
other lungs, he forced India ink in the
pulmonary artery at 80 mmHg pressure
and found that the capillary system in
the excised lung became rigid or erect
from the liquid forming a framework
that supported the respiratory unit. The
resulting microscopic picture resem-
bled that of a normal aerated lung (see
Fig 4). Last, he injected the India ink
under pressure first and then inflated
the lungs. He needed much less pressure
to inflate the lungs when the vascu-
lar system was already distended with
the India ink. With these “perfused”
lungs, he was able to inflate so much
air that the lungs became buoyant. The
microanatomical picture of these lungs
resembled those of a normally aerated lung
and was similar to the lung that had been
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Fig 3. Inflation with air. Note irregular disten-
sion with over-distended alveoli in one area
and atelectasis in other areas. Source: Reprinted
with permission from Acta Paediatr; 47, Jaykka
S. Capillary erection and the structural ap-
pearance of fetal and neonatal lungs, 484–500,
1958.
experimentally treated with only liquid
injected into the vascular system under
pressure (refer to Fig 5). He concluded
that this process of capillary erection
is an essential step in normal neonatal
cardiopulmonary adaptation. In a modi-
fication of this experiment, Avery47 also
found that lungs were easier to inflate at
lower pressures if they were first perfused.
These studies support the concept that
the establishment of normal neonatal
respiration is based on the adequate flow
of blood into the lung bed.
Recent studies detailing ultrastructural
development of the lung in rats from fetal
through neonatal stages seem to verify
Jaykka’s work and, if anything, suggest that
adequate pulmonary blood flow maintains
an important role in effective respiratory
function from birth to some time after.48
In the rat lung, which is often used as
Fig 4. Thin section from lung with forced
capillary distension using India ink. Source:
Reprinted with permission from Acta Paediatr;
47, Jaykka S. Capillary erection and the struc-
tural appearance of fetal and neonatal lungs,
484–500, 1958.
a model for the study of human lung
structure and function, three morpholog-
ical phases precede the development of
a mature, alveolar lung. At term and for
the first few days after birth, the terminal
lung is in a saccular phase, with relatively
smaller air spaces and thick intrasaccular
septa containing multiple capillaries (see
Fig 6). Not until seven days of life does the
typical alveolar structure begin to develop,
with thin intra-alveolar septa in which
there lies a single capillary in contact with
the air space on each side of the septum.
The thick, vascular septa present at birth
and for the following week may play an
important role in the structural support of
respiratory function in early neonatal life
and may be similar to what Jaykka saw
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Neonatal Transitional Physiology 65
Fig 5. Capillary erection. Note distended, full capillaries bulging into the alveolar spaces. Source:
Reprinted with permission from Acta Paediatr; 47, Jaykka S. Capillary erection and the structural
appearance of fetal and neonatal lungs, 484–500, 1958.
in his experiments (refer to Fig 4 and
Fig 5). Progress to normal alveolar struc-
ture and function may rest upon adequate
pulmonary blood flow. Further, the effi-
ciency of gas exchange across the thick
intrasaccular septa would necessarily be
lower than that in a mature alveolar lung
and would likely function best in the
presence of generous pulmonary blood
volume.
Step 4B: Increased pulmonary perfusion
pulls lung fluid from the alveoli across the
capillary membrane.
Fetal lung fluid, which is in essence am-
niotic fluid, contains very little protein
and has a low colloid osmotic pressure.
Once the capillaries are filled with blood,
which has a high colloid osmotic pressure,
the alveolar fluid is rapidly absorbed into
the pulmonary capillaries. The fluid has to
cross only one alveolar cell and one blood
capillary cell, constituting a distance of
less than 2 µm (refer to Fig 2).49 Thus,
the process of capillary erection is proba-
bly an essential part of the rapid change
from the “wet” lung of the fetus to the
“dry” lung needed by the neonate for gas
exchange. Capillary erection may be the
stimulus for the lung to change both struc-
ture and function immediately at birth
Capillary erection may be the stimulus
for the lung to change both structure and
function immediately at birth from an
organ of fluid secretion to an organ of
gas exchange.
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Fig 6. Left: the lung of a 2-day-old rat newborn with saccular structure. Intrasaccular septa are thick
with capillaries located on both sides of the septa (large arrows). Right: Lung of a 21 day old rat new-
born with alveolar structure. Alveolar septa are mainly thin; they accommodate only one capillary
(small arrows). Original magnification X 400. Source: Reprinted with permission from Folia Histo-
chemica et Cytobiologica, 36(1). Wasowicz M, Biczysko W, Marszalek A, Yokoyama S, Nakayama I.
Ultrastructural studies on selected elements of the extracellular matrix in the developing rat lung
alveolus, 3–13, 1998.
from an organ of fluid secretion to an or-
gan of gas exchange.9
Step 5A: Umbilical circulation contin-
ues to provide oxygenation, volume ex-
pansion, and pH correction.
Significant blood flow in the umbilical
cord after birth can be palpated easily
and has been documented. Stembera and
colleagues50 developed a unique method
to study the actual volume of blood flow
through the human umbilical cord in the
first few minutes after birth. From 113
measurements of thermodilution taken be-
tween 20 and 265 seconds after birth
in 17 neonates, they were able to doc-
ument blood flow of 248 mL/min in
the average 3 kg newborn (approximately
75 ±7 mL/min per kilogram). In the first
100 to 120 seconds, the rate of flow did
not change in comparison with the first
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reading at approximately 20 to 40 seconds.
After 1.5 to 2 minutes, they found a marked
decrease of flow in most, but not all, cases.
In distressed infants, they recorded a flow
of 50 mL/min per kilogram.51 This study
supports the idea that the transition to ex-
trauterine respiration may be made grad-
ually and without undue stress, as the
neonate is able to rely on blood flow
through the placenta for oxygenation dur-
ing the first minutes of life while blood vol-
ume is equilibrating.
Yao and Lind18 clearly documented the
increased blood volume that occurs when
the umbilical circulation is left intact.
They estimated that 50% of the transfusion
occurs within one minute if the infant
is at the level of the introitus and 100%
by 3 minutes. Lowering the baby at least
30 cm speeds the transfusion so that max-
imum transfusion occurs in 1 minute.
This additional blood volume has been
shown to increase perfusion,52 raise blood
pressure,11,12 and increase RBC delivery
to the vital organs.10 Higher blood pres-
sures have been consistently documented
in preterm and full term babies with de-
layed cord clamping by several sources
in older23,24 and more recent studies.11,12
Arcilla et al26 have shown higher pul-
monary artery pressures along with higher
blood pressures in babies with delayed
clamping.
Steps 5B and C: Increased systemic per-
fusion leads to elevated oxygen levels that
initiate continuous respiration.
Increased perfusion leads to better cap-
illary distention,52 higher blood pre-
ssure,11–13 and additional RBCs to carry
maximum oxygen.18 Increased oxygen lev-
els have been shown to stimulate contin-
uous fetal breathing movements in utero
while the administration of low oxygen
gas mixtures to the ewe caused fetal
breathing to cease.40 Ventilation of fetal
lambs with 100% oxygen initiated contin-
uous breathing.9“Breathing [movements]
can occur in the fetus [lamb] in the ab-
sence of transient hypoxemia to stimulate
the chemoreceptors and without any of
the sensory stimuli thought to be impor-
tant for the establishment of continuous
breathing at birth.”9(p 1122) It is probable
that this adaptive process continues after
birth to assist in initiating breathing in
the neonate. Babies who are well-perfused
breathe spontaneously while pale, limp in-
fants require resuscitation and often in-
tubation. While this information appears
counterintuitive, suppression of breath-
ing by low oxygen levels may be a
physiologic response in a stressed infant,
assuming uninterrupted umbilical circula-
tion. In this circumstance, the infant can
rely on the placenta for essential oxy-
genation while circulatory corrections are
made to establish adequate pulmonary per-
fusion effecting capillary erection before
breathing.
Steps 4C and 6: Air enters erect alveoli
gently or with crying and continuous res-
pirations begin.
With placental gas exchange supporting
the neonate immediately after birth, the
first breathing efforts may develop grad-
ually and gently. Immediate cord clamp-
ing may stimulate earlier, more aggressive
breathing efforts; however, these efforts are
likely to be ineffective at gas exchange and
in fact may be counterproductive.53
A major hypothesis of this paper is
that time to accomplish capillary erec-
tion is essential for adequate lung per-
fusion. Capillary erection appears to be
essential to the process of establishing
extrauterine respiration. This is consis-
tent with the finding that babies with de-
layed cord clamping have been found to
take the first breath later than babies with
early cord clamping.54 Evidence for this
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hypothesis is found in the work of Marquis
and Ackerman,53 who devised a technique
to examine placental respiratory function
in the immediate neonatal period. They
clamped one umbilical artery (UA) im-
mediately after birth and measured blood
gases. They clamped the second UA up to
37 seconds after birth and found no change
in the blood gases, even though several ba-
bies had breathed over six times. They con-
cluded that little gas exchange takes place
in the neonate’s first few breaths. Dunn55
reported higher 5-minute Apgar scores in
a group of babies with delayed clamping
when compared to a similar group who
had early clamping. Thus, when the cord
is left intact, the baby’s first cry may not
occur until there has been adequate trans-
fer of blood volume to recruit the lung,
fully perfuse the body, and stimulate the
respiratory center with the higher oxy-
Fig 7. Cross section of early clamped umbilical cord on the left (within 10 sec) and late-clamped
cord (over 3 min postpartum) on the right. Source: Reprinted from European Journal of Cardiology,
Vol. 5/3, Lind J, Human fetal and neonatal circulation, 265–281, c
°1977; with permission from
Elsevier Science.
gen levels. Even in babies who cry ear-
lier, the first breaths are not effective at gas
exchange.53
Step 7: Increased oxygen levels cause
closure of umbilical arteries and umbilical
circulation ceases.
The umbilical arteries, but not the vein,
are sensitive to oxygen and will close
when adequate oxygenation is achieved.
Figure 7 compares cross sections of early
and late clamped umbilical cords showing
closure of the umbilical arteries after cord
clamping at 3 minutes.56 McGrath et al57
examined sections of the umbilical cord
exposed to oxygen and found that the ar-
teries, but not the vein, were sensitive
to oxygen at 36 mmHg. After birth, oxy-
gen tension in the venous circulation (um-
bilical arteries) increases from the fetal
level of 15 mmHg to the neonatal level
of 40 mmHg. This rise in venous oxygen
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Neonatal Transitional Physiology 69
is most likely an adequate stimulus to ef-
fect closure of the umbilical arteries. In the
physiological range, increased oxygen did
not contract the umbilical vein that carries
oxygenated blood to the fetus/neonate.
It is likely that this same level of
oxygenation also begins to close other
similar oxygen-sensitive structures, such
as the ductus arteriosus, thus promot-
ing the transition to neonatal circulation
and respiration. Buckels et al found mur-
murs in all 17 early clamped babies and
none in the 15 late clamped babies they
studied.23 The increase in blood volume
that follows physiologic closure of the
umbilical vessels is also likely to con-
tribute to neonatal circulatory changes.
Linderkamp19 states, “Studies in newborn
lambs have shown that an increase of 50%
in blood volume causes the ductus arte-
riosus to close as a result of decreasing
pressure gradient between the aorta and
arteria pulmonalis.”(p.580) Thus, increased
blood volume, with its higher oxygen de-
livery capacity, appears to support more
successful neonatal transition.
Cord pulsations may continue for sev-
eral minutes after birth and can be read-
ily palpated. The flow slows immensely
but does not close entirely in some cases,
perhaps providing for further equilibra-
tion if needed.50 Spontaneous closure of
the umbilical arteries within a few min-
utes after birth may be a protective mech-
anism that would have guarded against
unregulated blood loss in newborns in
more primitive settings. The longer pa-
tency of the umbilical vein may serve to
protect the most stressed infants and of-
fer a small amount of additional RBCs
and nutrients. Yao and colleagues44 docu-
mented that maternal uterine contractions
effected complete placental transfusion by
approximately 3 minutes after birth. Third
stage administration of oxytocic medica-
tion reduces that time by half, confirm-
ing the role of the uterus in placenta
transfusion.44
Step 8: Stasis of blood in the umbilical
vein occurs; the placenta separates.
Typically, the placenta separates from
the uterus within a few minutes after
birth. In the 1930s, Brandt,58 using dye
and X-rays, documented that the placenta
rarely separated before 3 minutes. While
separation ends the exchange of gases
within the placenta, blood volume is still
available for the infant.
DISCUSSION
To date, our knowledge related to the
physiology of neonatal transition has been
segmented and scattered among different
disciplines. The development of this
model is an effort to synthesize what is
known into a whole. Its core concept is
that an uninterrupted umbilical circula-
tion will assist in the establishment of an
adequate blood volume to perfuse the body
and an adequate RBC flow to oxygenate
and stimulate the respiratory center.
The model underscores the value of
maintaining umbilical circulation in the
first minutes after birth. This approach
provides for adequate neonatal blood vol-
ume and allows a gradual and gentle,
but effective, physiologic transition to ex-
trauterine breathing. This interpretation of
the neonatal transition process runs con-
trary to some long-held beliefs of many ob-
stetric and pediatric care providers. These
beliefs often (and necessarily) have been
based on limited or conflicting empiri-
cal data. Reasonable consideration of this
model will require reevaluating current
knowledge relevant to several related is-
sues. These include beliefs about neonatal
polycythemia and jaundice and issues re-
lated to neonatal resuscitation procedures.
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Neonatal Polycythemia and Jaundice
The belief that delayed cord clamping
causes polycythemia and jaundice will
probably be the single greatest obstacle to
research on and acceptance of this model.
Currently, this belief is so prevalent that
one often finds it stated in the literature
as accepted unreferenced fact.36,37,59 Con-
cerns about the potential for polycythemia
and neonatal jaundice when cord clamp-
ing is delayed were initially raised in pub-
lications by Saigal et al60–61 who reported
symptomatic polycythemia in 2 of 42 ba-
bies held 30 cm (12 in) below the per-
ineum for 5 minutes. In contrast, there are
larger studies from the 1960s and 1970s
that report no symptomatic polycythemia
when infants were held at the level of
the perineum and cord clamping was
delayed until pulsations ceased.17,18,23–29
A comprehensive review of the literature
on cord clamping shows that most re-
cent controlled trials do not support this
concern.62
Polycythemia has long been a perplex-
ing disorder that is difficult to manage and
even to diagnose. It does have associa-
tions that are clearly unrelated to the tim-
ing of cord clamping. Pregnancy compli-
cations such as preeclampsia/eclampsia,
maternal diabetes, small or large for ges-
tational age conditions, and fetal genetic
abnormalities all bear increased risk for
neonatal polycythemia.37,38,63,64 Kurlat63
found that the risk of polycythemia in
appropriate size infants of hypertensive
mothers was 12.6-fold greater than that
The belief that delayed cord clamping
causes polycythemia and jaundice will
probably be the single greatest obstacle
to research on and acceptance of this
model.
of the general newborn population. In
a study of diabetic mothers, 5% of in-
fants had polycythemia.65 Diagnostic dif-
ficulties have persisted due to problems
related to the unreliability of labora-
tory indicators for blood volume and
hemoconcentration.65,66 The blood test
most commonly used for diagnosis, the
hematocrit, can be influenced by factors
as simple as site of sampling or time of
testing.67,24
One new hypothesis has been put forth
that may better explain the pathophysio-
logic processes and lead to more effective
treatment. Jones et al65 and Wardrop et al66
suggest that an elevated hematocrit oc-
curs when hypoxia induces a failure of the
vascular endothelial integrity, leading to
capillary leakage. This failure of the en-
dothelium allows components of plasma
such as salt, water, and albumin to leak
from the intravascular space, causing a sec-
ondary hemoconcentration and poor cor-
relation between the hematocrit and blood
volume.65,66 Their findings raise doubts
about the results of older studies that used
albumin markers such as radioactive I125
to measure blood volumes.17,19,60,61 Leak-
age of tracer attached to albumin across the
capillary membranes would lead to falsely
high blood volume results—especially in
sick or hypoxic infants.2,65,66
Polycythemia appears to be a multifac-
torial problem—it occurs most often in ba-
bies who have other serious problems—yet
it is often assumed to be the cause,
rather than a result, of any overarching
problem.37 This scientific flaw, as Werner37
so aptly points out, causes polycythemia to
continue to vex the neonatologists.
Issues Related to Neonatal Resuscitation
This model raises several issues related
to neonatal resuscitation. These include
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Neonatal Transitional Physiology 71
the development of techniques for bedside
resuscitation that dispense with the need
for immediate cord ligation, inquiry into
the possible risks of ventilation efforts that
precede adequate pulmonary perfusion,
and the potential of placental transfusion
for avoiding the need for volume expan-
sion in resuscitative efforts.
Successful resuscitation can occur at the
perineum with an intact umbilical cord. In
many hospital settings, this would require
a new, but perhaps beneficial, interdisci-
plinary team effort. A neonate can be kept
warm and dry and monitored for respira-
tory effort, heart rate, and color on the bed
nearly as easily as anywhere else. When
indicated, equipment for positive pressure
ventilation can be brought to the infant.
Lowering the infant as much as cord length
will allow for 30 to 60 seconds while dry-
ing the baby can speed placental transfu-
sion and provide volume expansion before
clamping the cord when it must happen
quickly.18 Optimal management in cases
where meconium is present in amniotic
fluid needs further investigation. Immedi-
ate clamping of the cord may be likely to
induce a first breath prior to adequate suc-
tioning after birth. A better approach may
be to keep the baby unstimulated, with
cord intact at the perineum, while the na-
sopharynx is carefully suctioned.
Jaykka’s work decades ago suggested that
forceful ventilation prior to recruitment
of the lung brought about by pulmonary
perfusion and capillary erection damaged
the alveoli. Clark68 suggests that the lungs
of ventilated newborns are most dam-
aged when the lung is recruited and dere-
cruited with each breath—exactly what
would happen without adequate support
from the full capillary plexuses. Allowing
time and blood volume for adequate capil-
lary perfusion and erection to occur, even
(or perhaps especially) in premature in-
fants, may help protect the delicate tissue
of the neonatal lung and promote effective
respiratory function. The need for imme-
diate intubation is under study for preterm
infants.69
A poor response to resuscitative mea-
sures in the delivery room is often at-
tributed to neonatal volume depletion.70
The ideal volume expander, and the
only one with oxygen-carrying capacity,
is whole blood. If one places a pale, limp
baby at the level of the perineum or lower,
the baby will get about 10 mL/kg of whole
blood while resuscitation is being per-
formed, as long as the heart rate is good
and the cord is pulsating.1
CONCLUSION
Since the beginning of mammalian life,
young have been born attached to a life-
line which supports their transition to ex-
trauterine life. The process of birth invari-
ably involves a period of maternal and
neonatal rest before any active measure re-
sults in a severing of the umbilical cord.
There have been two exceptions to the nor-
mal recovery process: human birth in some
settings of recent times, and the attended
births of thoroughbred foals.
In 1959, equine researchers Mahaffey
and Rossdale71 reported on an often fa-
tal “convulsive syndrome” in newborn
thoroughbred foals that occurred only
to “foals born indoors, under human
supervision.”(p 1224) Human supervision of
foaling at that time included rapid cord
clamping, contrary to natural (unsuper-
vised) settings, in which a mare and foal
typically rest for about a half hour. The
cord is then broken when either the mare
or the foal rises. Pathology findings from
foals that died of convulsive syndrome
included an absence of aeration of the
alveoli, with lung tissue so dense that it
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72 JOURNAL OF PERINATAL AND NEONATAL NURSING/MARCH 2002
rapidly sank in fixative, and presence of
hyaline structures.72
Foal or baby, “human supervision” at
birth should, at the least, do no harm.
While the United States remains at 25th73
in the worldwide ranking of infant mor-
tality, with little change in the past sev-
eral years, we must consider all possible
sources of potential harm to babies. A dif-
ference in blood volume of 25% to 40% is
not insignificant. The current typical prac-
tice of immediate cord clamping, espe-
cially of those infants potentially in most
need of additional red blood cells, needs to
be reconsidered.74 Examination of short-
term and long-term neonatal outcomes
with variations in cord clamping practices
and methods of resuscitation is essential.
These issues demand a better understand-
ing of and respect for the normal physi-
ologic processes involved in labor, birth,
and the neonatal transition. Continued re-
search on the issue of neonatal transition
for full-term and premature infants and the
effect of cord clamping timing is urgently
needed.
In fact, the current knowledge base
is limited even to the extent that typ-
ical practices and the beliefs on which
they are based are mostly undocumented.
A survey of American certified nurse-
midwives revealed that one-third feel
strongly that clamping should be delayed
until the newborn has completed a suc-
cessful transition.75 They believe that this
delay allows time for the neonate to gently
make the transition to extrauterine respi-
ration and to self-regulate blood volume.
Midwives who practice early clamping
(26%) believe that delay has no benefit
and often fear it will cause polycythemia
and jaundice.75 Similar descriptions of
practices or beliefs among other groups
of obstetric and pediatric practitioners
are not available. International practices
and experiences are not shared in the
literature.
Research-based evidence for practice is
lacking. Management of the umbilical cord
at the time of birth is probably most fre-
quently done without thought, and clamp-
ing of the cord is often seen as merely a
task. The presentation of the blood volume
model for neonatal transition is a frame-
work presented as an alternative to com-
monly held beliefs. It is put forth in an ef-
fort to encourage the application of critical
thinking to this potentially significant is-
sue, and to foster and frame the research
that will answer the questions raised.
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