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STATE-OF-THE-ART REVIEW
Amniotic Fluid and the Clinical
Relevance of the Sonographically
Estimated Amniotic Fluid Volume
Oligohydramnios
Everett F. Magann, MD, Adam T. Sandlin, MD, Songthip T. Ounpraseuth, PhD
Invited paper
The amniotic fluid volume (AFV) is regulated by several systems, including the intramembranous pathway, fetal production (fetal urine and lung fluid) and uptake (fetal
swallowing), and the balance of fluid movement via osmotic gradients. The normal
AFV across gestation has not been clearly defined; consequently, abnormal volumes
are also poorly defined. Actual AFVs can be measured by dye dilution techniques and
directly measured at cesarean delivery; however, these techniques are time-consuming,
are invasive, and require laboratory support, and direct measurement can only be done
at cesarean delivery. As a result of these limitations, the AFV is estimated by the amniotic fluid index (AFI), the single deepest pocket, and subjective assessment of the AFV.
Unfortunately, sonographic estimates of the AFV correlate poorly with dye-determined
or directly measured amniotic fluid. The recent use of color Doppler sonography has not
improved the diagnostic accuracy of sonographic estimates of the AFV but instead has
led to overdiagnosis of oligohydramnios. The relationship between the fixed cutoffs of
an AFI of 5 cm or less and a single deepest pocket of 2 cm or less for identifying adverse
pregnancy outcomes is uncertain. The use of the single deepest pocket compared to
the AFI to identify oligohydramnios in at-risk pregnancies seems to be a better choice
because the use of the AFI leads to an increase in the diagnosis of oligohydramnios, resulting in more labor inductions and cesarean deliveries without any improvement in
peripartum outcomes.
Key Words—amniotic fluid; amniotic fluid index; oligohydramnios; single deepest
pocket
Received February 22, 2011, from the Departments of Obstetrics and Gynecology (E.F.M.,
A.T.S.) and Biostatistics (S.T.O.), University of
Arkansas for the Medical Sciences, Little Rock,
Arkansas USA. Revision requested March 30,
2011. Revised manuscript accepted for publication
May 22, 2011.
Address correspondence to Everett F. Magann,
MD, Department of Obstetrics and Gynecology,
University of Arkansas for the Medical Sciences,
4301 W Markham St, Slot 518, Little Rock, AR
72205 USA.
E-mail: [email protected]
Abbreviations
AFI, amniotic fluid index; AFV, amniotic
fluid volume; NICU, neonatal intensive care
unit
Dynamics of the Amniotic Fluid Volume
Amniotic fluid provides an ideal environment for normal fetal
growth and development. It provides the fetus with a source of
water, protects the fetus from trauma, allows for normal movements
critical for anatomic development, and contributes to the development of the fetal lungs.1 The physiologic characteristics of the dynamics influencing the amniotic fluid volume (AFV) are complex
and not clearly understood. To understand the AFV, knowledge of
the pathways for potential amniotic fluid movement and the regulatory mechanisms involved must be taken into consideration.
There are several potential sources influencing AFV: fetal urine production, fetal swallowing, secretion of fetal lung fluid, the intramembranous pathway (movement of water and solutes between
amniotic fluid and fetal blood and the placenta), the transmembra-
©2011 by the American Institute of Ultrasound in Medicine | J Ultrasound Med 2011; 30:1573–1585 | 0278-4297 | www.aium.org
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nous pathway (movement of water and solutes across the
surface area of the amnion and chorion), secretions by the
fetal oral-nasal cavities, and movement of water across the
highly permeable fetal skin during early gestation.2 We will
consider each of these influences as they relate to the dynamics of maintaining the AFV.
Composition and Osmolality of Amniotic Fluid
Amniotic fluid consists of 98% to 99% water.2 Early in
human pregnancy, the AFV is isotonic with maternal or
fetal plasma and contains minimal amounts of proteins.1
In early gestation, substantial amounts of amniotic fluid are
present before the establishment of fetal urine production.
Little is known about the dynamics of amniotic fluid early
in gestation, but a likely scenario is the active transport of
solutes across the amnion into the amniotic space with
water moving passively down the chemical gradient.2 Fluid
may also arise as a transudate of plasma across fetal nonkeratinized skin or from the mother across the uterine deciduas and/or the placental surface.1
Much more is known about the dynamics of the AFV
in the second half of pregnancy after fetal skin keratinizes
at 22 to 25 weeks’ gestation, resulting in the prevention of
further water movement across skin. As the gestational age
increases, amniotic fluid osmolality and sodium concentrations decrease, which is thought to be due to the increasing production of diluted fetal urine. Amniotic fluid
osmolality ultimately reaches 250 to 260 mOsm/mL at
term.2 Fetal osmolality (≈278 mOsm/mL) remains close
to maternal osmolality (280 mOsm/mL), which limits the
amount of water transfer between the fetal and maternal
circulations under normal conditions.3
Fetal Urination
Fetal urine production is the predominate source of amniotic fluid in the second half of pregnancy, as evidenced by
the almost complete absence of amniotic fluid with renal
agenesis or fetal urinary tract obstruction. Fetal urine first
enters the amniotic space at 8 to 11 weeks’ gestation and
constantly increases throughout gestation.4 Fetal urine
production per kilogram of fetal body weight at 25 weeks
is approximately 110 mL/kg per 24 hours, and it is approximately 190 mL/kg per 24 hours at 39 weeks.5 Estimates of human fetal urine output have been made from
sonographic studies of the fetal bladder measured at regular intervals. The best estimate of the human fetal urine
output at term is 700 to 900 mL per day.2
The fetus is able to respond to changes in fluid status
by adjusting urine flow and thereby contributes to the regulation of the AFV.1 In 2003, Thurlow and Brace6 ob-
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served that fetal ovine hypoxia was associated with increased urine flow, as opposed to the often-associated
chronic fetal hypoxia and low AFV. This finding suggests
that human regulation of the AFV is also likely mediated by
other mechanisms such as intramembranous absorption7
in addition to changes in fetal urine production at times
of fetal hypoxia. Similarly, Gagnon et al7 found that the
reduction in the AFV seen with chronic severe placental
insufficiency in sheep was not due to a decrease in fetal urinary production but due to an increase in the intramembranous absorption of amniotic fluid, resulting in an overall
decrease in the AFV.
Fetal Swallowing
Fetal swallowing plays a vital role in the maintenance of
the AFV, as evidenced by the association of hydramnios
with disturbances in fetal swallowing. The human fetus begins to swallow at the same time that fetal urine begins to
enter the amniotic cavity, around 8 to 11 weeks’ gestation.2
Near term, the human fetus swallows an estimated average of 210 to 760 mL per day.8
There are few human studies evaluating fetal swallowing; thus, our current knowledge is based primarily on
observations using the ovine model, which is well established in evaluating human fetal physiologic development.
Studies have shown many similarities between the ovine
fetus and the human fetus with regard to fetal swallowing
behavior and the rates of ingested fluid in utero. Studies in
fetal sheep, as well as humans, show that the fetus usually
swallows during episodes of fetal breathing activity.5,9 Fetal
hypoxia has been shown to suppress fetal swallowing in the
ovine fetus,10 whereas decreases in amniotic fluid osmolality and increases in fetal plasma osmolality will increase
fetal swallowing.11 In 1976, Minei and Suzuki12 reported
that esophageal ligation in primate fetuses resulted in the
development of hydramnios; however, the AFV returned
to normal before delivery. It is thought that fetal sheep
maintain a constant AFV after esophageal ligation with
continued urine flow by increasing intramembranous absorption.13 These studies suggest that the human fetus is
able to modulate swallowing under various conditions similar to that which has been observed in the ovine model;
however, it is not likely the major regulatory mechanism
by which the human fetus maintains its AFV.
Fetal Lung Fluid
Secretion of fetal lung fluid into the amniotic fluid cavity is
well established and accepted. This idea is supported by
the measured amount of phospholipids in the amniotic
fluid as tests for fetal lung maturity, which are of pulmonary
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origin and not passed in substantial quantities in the fetal
urine. There is little, if any, notable osmotic exchange between amniotic fluid and fetal plasma in the lung because
the fetal glottis serves to prevent backflow of amniotic fluid
into the trachea.3 This concept is evident by the observation that meconium staining is common, whereas meconium aspiration is rare and often occurs in the setting of
severe fetal hypoxia. In 1972, Liley14 reported that after
intra-amniotic injection of contrast media, in only 4 of
more than 800 patients was there evidence either radiologically or histologically of contrast medium detectable in
the fetal or neonatal lung and noted that these 4 pregnancies were “highly pathological.” An outflow of approximately 200 to 400 mL per day has been shown in
near-term fetal sheep.15 Brace et al10 demonstrated that in
fetal sheep, approximately 50% of the secreted lung fluid
entered the amniotic fluid, and the remainder was swallowed as it exited the trachea. This process results in a net
secretion of 100 to 200 mL per day.
Secretion flow is thought to be due to the active transport of chloride ions across the epithelial lining of the developing fetal lungs.2 It has been shown that in utero
ligation of the trachea in other animal species results in expansion of the fetal lung, thought to be due to the continued production of fetal lung fluid.2 It is generally accepted
that fetal lung secretion allows for pulmonary lung expansion, which serves to promote fetal lung development.1
Thus, secretion of lung fluid into the amniotic fluid is likely
a substantial contributor to the AFV, although factors regulating fetal lung fluid secretion are poorly described, and
the exact amount of lung fluid flowing into the amniotic
fluid in the human fetus has not been quantified.
Intramembranous and Transmembranous Pathways
The sum of the fetal urine production plus the secreted
fetal lung fluid minus the amount removed via fetal swallowing leaves approximately 400 mL in excess within the
amniotic cavity.3 As gestation progresses and fetal urine
production as well as secreted lung fluid increases, there
must be a mechanism by which to compensate for this excess and maintain balance. This mechanism is termed the
intramembranous pathway. It is estimated that in the nearterm ovine fetus, approximately 200 to 500 mL per day is
absorbed via the intramembranous route.16
Intramembranous movement of water and solutes
into the fetal circulation across the fetal vessels on the surface of the placenta is driven by the osmotic difference between the fetal circulation and the amniotic fluid. In other
animal species, studies have demonstrated that the AFV
returns to a homeostatic state even after large quantities of
J Ultrasound Med 2011; 30:1573–1585
fluid are infused into the amniotic fluid cavity or after
esophageal ligation.1 This finding suggests that there is a
continuous flow of water and solutes from the amniotic
fluid into the fetal circulation. Only approximately 35% of
intramembranous movement of fluid depends on the osmotic gradient between the amniotic fluid and the fetal circulation, as observed in an ovine study.17 Therefore, there
must be other nonpassive mechanisms that contribute to
the intramembranous pathway.
There appears to be membrane asymmetry with regard to the bidirectional flow within the intramembranous
pathway.1 Solutes appear not to cross in the same amounts
from the amniotic fluid to the fetal circulation and from the
fetal circulation to the amniotic fluid cavity.1 This finding
was demonstrated in 2002 by Faber and Anderson17 using
radiolabeled albumin, which rapidly crossed from amniotic fluid to fetal blood in pregnant sheep, but they saw no
movement of radiolabeled albumin from the fetal circulation across to the amniotic fluid. Additionally, intramembranous absorption is increased with ligation of the ovine
fetal esophagus, which suggests a mechanism by which intramembranous flow is increased when the ability to swallow is eliminated.16
There is a strong relationship between the maternal
fluid status and fluid balance between the fetal circulation
and the AFV. The intramembranous pathway likely plays
a role in correcting the fetal volume status during times of
maternal dehydration. Animal studies reflect that during
maternal dehydration states, the maternal serum osmolality increases, resulting in water movement from the fetal
circulation to the maternal circulation; this resulting fetal
dehydration results in increased fetal osmolality and promotes movement of water flow from the amniotic fluid to
the fetal circulation to restore the fetal intravascular volume with a resultant decrease in the AFV.3 The opposite
effect is also true. In 2003, Magann et al18 showed that intravenous maternal hydration with 1 L of fluid increased
both the actual and sonographically estimated AFV in the
human fetus, with an average increase in the actual AFV of
188 mL. Similarly, Kilpatrick et al19 showed that maternal
hydration with 2 L of water in a patient with a low AFV can
increase the human fetal amniotic fluid index (AFI) by up
to 31%.
There is little support for movement of fluid via the
transmembranous pathway as a major contributor to the
AFV in the second half of pregnancy. In sheep, studies
suggest that only 10 mL per day in late gestation may be
absorbed by the uterus in the setting of normal osmolality.20 There have been experimental studies that imply
that the amniotic membrane may be abnormal when
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there is a low or high AFV, ie, thinner in the presence of
a low AFV and thicker in the presence of a high AFV.21
Given the large surface area of the amnion and chorion,
it is obvious why membrane permeability has been a proposed regulator of the AFV. However, little is known regarding the permeability and filtration characteristics as
they relate to amniotic fluid dynamics. Clearly, our
knowledge of intramembranous and transmembranous
movement of amniotic fluid remains deficient.
Secretions by the Fetal Oral-Nasal Cavities and Other
Influences
Studies of late-gestation sheep have shown that approximately 25 mL per day is secreted by the fetal oral-nasal cavities.22 This amount is small and is not considered a main
source of amniotic fluid. On the basis of information about
transepidermal water loss in the preterm infant, it is generally accepted that there is movement of water across the
highly permeable fetal skin before 22 to 25 weeks’ gestation, which contributes to the AFV in the first half of pregnancy. It is also reasonable to assume that there is a
relationship between fetal weight and the AFV. Fetal urine
production seems to be influenced by weight, with more
fetal urine produced as the fetus becomes larger, which is
evident as fetal urine production increases with the growing fetus across gestation. However, Magann et al23
showed that the neonatal birth weight was not correlated
with a dye-determined or sonographically estimated AFV.
Likewise, Owen et al24 showed that there was no clinical
correlation between the AFI and estimated human fetal
weight.
Clinical Correlation of AFV Dynamics
What was once thought to be a stagnant pool of fluid with
turnover once per day, the AFV, is now considered to be a
complex system involving numerous forces and pathways
that influence the influx and efflux of fluid and solutes
within the amniotic fluid cavity and regulating mechanisms of each that are yet to be completely understood.
The regulatory balance seems to be focused at 3 levels:
first, the intramembranous pathway involving control of
the movement of fluid and solutes between fetal blood
within the placenta and membranes; second, regulation
of the inflows and outflows from the fetus in terms of fetal
urine production, which is influenced by hormones such
as arginine, aldosterone, angiotensin II, atrial natriuretic
peptide, and vasopressin in a similar fashion as in adults2;
and last, regulation by the maternal-fetal relationship,
which influences the fluid balance driven primarily by osmotic gradients.
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To a certain extent, the AFV correlates with the status
of the fetus and the placenta. A knowledge and understanding of the interplay that takes place to maintain balance within the amniotic fluid cavity are crucial, allowing
the practitioner to more readily identify abnormalities in
this process, which may be the result of maternal or fetal
disease states.
What Is a Normal AFV in Singleton Pregnancies?
The issue of what is considered a normal AFV during pregnancy is vital to the practice of the general obstetrician,
family practice physician, and maternal-fetal medicine specialist alike. The AFV is the summation of influx and efflux
of fluid within the amniotic space. Abnormalities of the
AFV have been associated with adverse pregnancy outcomes.25,26
To label a volume of amniotic fluid as abnormal, the
normal volumes of amniotic fluid across gestation must be
defined. By convention, on the basis of definitions and cutoff values used in studies of the AFV in the literature and
the definitions given by several major texts, there are multiple accepted definitions of an abnormal AFV. A low AFV
(oligohydramnios) has been defined as the following:
less than 200 mL,27 less than 500 mL total volume,28,29
below the 5th percentile for gestational age,30 a single deepest pocket of less than 2 cm,31–33 an AFI of less than 5
cm,25,26,33–35 and a subjectively low AFV.36 An increased
AFV (polyhydramnios) can be defined as follows: greater
than 2000 mL total volume,37 above the 95th percentile
for gestational age,34 a single deepest pocket of greater than
8 cm,38 an AFI of greater than 24 cm39 or greater than 25
cm,40 and a subjectively increased AFV.36
Changes in the AFV Across Gestation
Several studies have attempted to define “normal” AFVs
across gestation. When discussing the AFV, it is important to point out that there are multiple studies published
in the literature that provide reference curves reflecting
the changes in the AFV across gestation in normal pregnancies. The volume defined as a normal AFV changes
depending on the gestational age at which the AFV is
measured.
In 1972, Queenan, et al41 used dye-determined methods with para-aminohippurate to directly measure the
AFV of 187 patients across gestation from 15 to 16
weeks to 41 to 42 weeks. They showed a wide range of
fluid volumes across gestation and observed that the
AFV increased as pregnancy advanced from the 15th to
the 20th week and then remained relatively constant
from the 20th through the 41st week.41 Their study showed
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that the AFV peaked at 33 to 34 weeks’ gestation, gradually
decreased to term, and then decreased at a greater rate after
41 weeks.
In 1989, Brace and Wolf42 defined normal amniotic
fluid changes across gestation. They derived “normal” values from a compilation of 705 pregnancies from 12 previously published studies ranging from 8 to 43.2 weeks.42–53
A normal pregnancy was defined as a pregnancy without
evidence of fetal anomalies, fetal death, spontaneous abortion, preeclampsia, or maternal or fetal disease. Fetuses
with “oligohydramnios” and “polyhydramnios” were included in the analysis if the outcome was “good.” Brace and
Wolf 42 reported a peak AFV of 931 mL at 33.8 weeks with
a decrease in the AFV thereafter. Initially, a polynomial regression was used for the analysis, and the data were then
log transformed to overcome statistical “problems” that
arose using polynomial regression.42 Once the data were
log transformed, analysis of variance was used to analyze
the data, and the authors found no statistically significant
change in the AFV from 22 to 39 weeks’ gestation, with an
average volume of 777 mL and a range of 630 to 817 mL.42
Using polynomial regression, they showed the AFV to decrease by 8% per week after 40 weeks’ gestation.42
In 1997, Magann et al54 performed another study to
assess normal AFVs across gestation. This study was undertaken for several reasons: first, the patients in the study
by Brace and Wolf42 were obtained from 12 different studies conducted by 23 different investigators published between 1962 and 1977, and second, the average sample size
per study was 60 or fewer patients, and the studies used a
combination of techniques to measure the AFV, either by
direct measurement at the time of hysterotomy (with the
possibility of blood contamination) or a variety of dye
dilution techniques (some of which remain unvalidated).
As a result, these potential confounding variables may have
influenced the AFV determinations in the study by Brace
and Wolf.42 Magann et al54 measured the AFV of 144 singleton pregnancies between 15 and 40 weeks using the
same “normal” pregnancy criteria as Brace and Wolf.42
One investigator performed all of the amniocenteses using
a single dye-dilution technique for measurement with
analysis performed in the same laboratory.
Additionally, a formulation derived from the Richards
growth curve55 was used to plot the data across gestation.
Using nonlinear regression and logarithmic transformation with the growth curve model, the AFV was found to
increase across gestation with a peak at 40 weeks. This finding is contrary to the previously published conclusion of
Brace and Wolf,42 who found that the AFV remained stable from 22 to 39 weeks, but is consistent with some of the
J Ultrasound Med 2011; 30:1573–1585
conclusions drawn by Queenan et al.41 Magann et al54
maintained that although polynomial regression and multivariate analysis can empirically model trends over the
range of the observed data, these equations are not accurate when dealing with the physiologic characteristics of
the growth process. These equations provide information
only over a limited range of the growth cycle and are therefore regarded as less than optimal for studies of the growth
process.56,57 A growth curve model would therefore be
more appropriate because it allows one to incorporate biologically interpretable parameters that apply to a larger
range of the growth cycle. A polynomial model, if extrapolated to earlier gestational ages, would actually yield a negative AFV value. Using the growth curve model with time
0 at conception, the AFV is 0, and as gestational age increases, the AFV increases. Thus, this growth model has
the ability to fit the data and offer a physiologic basis for
that modeling. This model may prove to be superior to the
previously published methods of statistical analysis, but
further analyses of the various data sets using this model
need to be performed. These 3 published normal AFVs
across gestation have notable similarities and differences
(Figure 1).
Because the actual AFV can only be calculated by amniocentesis and dye dilution techniques or directly measured at the time of cesarean delivery, the AFV is usually
estimated by sonography. An often-cited reference to a
“normal” AFV in pregnancy is a 1990 article by Moore and
Cayle,34 who attempted to define the normal AFI in pregnancy. They evaluated 791 patients with normal pregnanFigure 1. Comparison of normal amniotic fluid volumes (dye determined
or directly measured) across gestation: Brace and Wolf,42 Magann et
al,54 and Queenan et al.41
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cies. Their definition of normal was as follows: gestation
between 16 and 44 weeks, adequate obstetric dating, no
structural abnormalities on sonography, normal pregnancy without complications, term delivery with a neonatal birth weight between the 10th and 90th percentiles,
and a normal neonatal course.34 Moore and Cayle measured the AFI according to the criteria established by
Rutherford et al25 and plotted the measurements across
gestation, Using polynomial regression and logarithmic
transformation, Moore and Cayle34 found the mean AFI
curve to rise starting at 16 weeks, peak at 27 weeks, plateau
until 33 weeks, and then decline until 42 weeks. They observed that the AFI decreased by 12% per week after 40
weeks.34
In 2007, Machado et al58 found results similar to
those of Brace and Wolf.42 This prospective study evaluated the AFI of 2868 patients. They analyzed their data
using multiple linear regression and quadratic polynomial
adjustments and found the AFI across gestation to be
practically constant between 20 and 33 weeks’ gestation
and then began to decrease after 33 weeks, with the most
notable decrease after the 38th week.
In 2000, Magann et al33 performed a prospective
study to determine normal values for the sonographically
measured AFI, single deepest pocket, and 2-diameter
pocket in normal human pregnancy. Normal pregnancy
was defined the same as it was by Moore and Cayle.34 The
exclusion criteria included growth abnormalities, gestational age extremes (<14 or >42 weeks), and a depressed
Apgar score of less than 7 at 5 minutes. They recruited 50
patients at every gestational age between 14 and 41 weeks,
for a total of 1400 patients. The data were analyzed using
linear regression and logarithmic transformation, to be
consistent with the work done previously by Moore and
Cayle.34 Magann et al33 found that when the AFI is used
to define the fluid status across gestation, it increases from
14 to 31 weeks and then declines thereafter. When the single deepest pocket 2-diameter pocket is used, the AFV increases from 14 to 20 weeks’ gestation, plateaus between
20 and 37 weeks, and then gradually declines thereafter
through the 41st week. How does that study compare to
the study by Moore and Cayle34 with regard to defining a
“normal” value for the sonographically estimated AFV? If
you were to consider the individual cases in the study by
Magann et al and use the curve of Moore and Cayle, you
would find that 36% of the patients in the study by Magann
et al study who had normal outcomes would have been labeled as having abnormal (either oligohydramnios or polyhydramnios) fluid volumes according to the curve of
Moore and Cayle.
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Another investigation by Lei and Wen59 constructed
an AFI curve by gestational week in 5496 Chinese women.
The 5th, 50th, and 95th percentiles of this study were
different from the curves of both Moore and Cayle and
Magann et al across gestation (Figure 2). The curves of
both Lei and Wen and Magann et al had an AFI that was
less at each gestational age than the curve of Moore and
Cayle. The curves of Lei and Wen for the 5th and 95th percentiles were greater than those of Magann et al at less than
22 and greater than 36 weeks but less at each gestational age
between 22 and 36 weeks.48 These findings suggest that the
“normal” AFV at a point in gestation may be different depending on the population being investigated, and perhaps
population-specific curves should be established to better
define the normal AFV to prevent increased interventions
with no ultimate change in pregnancy outcomes.
In summation, there is yet to be a clearly defined normal value for the AFV or for the estimated AFV at each
week across gestation; therefore, “abnormal” cannot be defined. The definitions of oligohydramnios by Queenan et
al,41 Brace and Wolf,42 and Magann et al33 differ markedly
from widely used fixed cutoffs such as an AFV of less than
200 mL27 or less than 500 mL.28,29 Whether the actual AFV
decreases in late gestation, remains steady throughout
most of the third trimester, or increases throughout gestation with a peak at term is yet to be clearly established. Ideally, a normal AFV should be defined as a value between
defined high and low values, which are linked to adverse
pregnancy outcomes at each point across gestation. Importantly, a value defined as a normal AFV cannot in and
of itself guarantee a good perinatal outcome.
Figure 2. Comparison of amniotic fluid volume indices in normal populations: Lei and Wen,59 Magann et al,33 and Moore and Cayle.34
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Measurement of the AFV
Methods of Sonographic Estimation of the AFV
(AFI, Single Deepest Pocket, 2-Diameter Pocket,
and Subjective Assessment)
The AFV can be measured by dye dilution techniques at
the time of amniocentesis28,29 or can be directly measured
at cesarean delivery.27 These methods are time-consuming, are invasive (done at the time of amniocentesis), and
may require laboratory support (dye dilution techniques),
and some can only be done at the time of delivery (direct
measurement technique). Because of these limitations, the
AFV is estimated by sonography.
There are 4 reported techniques used to estimate the
AFV. Two of these are used frequently: the AFI25,26,34 and
the single deepest pocket.31,60 A third technique is subjective assessment, although how frequently the subjective assessment is used is uncertain.36,61 The fourth technique,
the 2-diameter pocket technique,37 is no longer used because it was shown not to be a better predictor of an abnormal AFV than the AFI.62
Correlation of a Sonographically Estimated AFV With
a Dye-Determined or Directly Measured AFV
The correlation of a sonographic estimate of amniotic fluid
with a known fluid volume was suggested by Moore and
Brace.63 The uteri of 5 near-term sheep were exteriorized,
and all of the amniotic and allantoic fluid was removed.
The uteri were then filled with normal saline, and at each
100-mL increment of fluid, an AFI was obtained until 2 to
2.5 L of saline had been instilled. The AFI was then compared to infused volumes using curve-fitting formulas.
A good correlation (r = 0.94) was observed between the
infused saline and the AFI. Both the dye-determined fluid
calculation using para-aminohippurate and direct measurement at cesarean delivery have been shown to have
good concordance (r = 0.99), and either can be used in determining the actual AFV.64
Sepulveda et al65 amnioinfused 16 pregnancies between 16 and 28 weeks’ gestation with severe oligohydramnios or anhydramnios and intact membranes. They
observed a linear relationship between the infusion and the
AFI, but only 30% of the variation in the AFI could be explained by the infused volume. Croom et al66 estimated the
AFV with sonography (AFI and single deepest pocket) in
term pregnancies and correlated those measurements with
a dye-determined fluid volume using para-aminohippurate
and calculated after amniocentesis. They observed that
both the AFI and single deepest pocket reliably identified
a normal fluid volume and the 2 pregnancies with oligoJ Ultrasound Med 2011; 30:1573–1585
hydramnios. None of the pregnancies had polyhydramnios, but the authors observed that at high volumes, the
AFI overestimated the AFV.
Dildy et al29 used 13 different sonographic measurements and compared them to a dye-determined volume
and observed that the sonographically estimated AFV
could lead to an overestimation of the dye-determined
AFV by 89% at low volumes and an underestimation of
54% at high volumes. Magann et al28,37 assessed the association of a sonographic estimate of the AFV with a dyedetermined fluid volume in two investigations and
observed that the sensitivity of the AFI for oligohydramnios was 6.7% in one study and 8.7% in the other investigation. Horsager et al27 estimated the AFV by sonography
and directly measured the fluid at cesarean delivery and
observed that the sensitivity of sonography for detecting
a low AFV was only 18%. Chauhan et al67 compared the
ability of two methods of amniotic fluid assessment (2diameter amniotic fluid pocket versus AFI) to predict
oligohydramnios or polyhydramnios using receiver operating characteristic curves and regression analysis and
observed that both sonographic measurements were inaccurate predictors of actual oligohydramnios or polyhydramnios when compared with dye dilution or direct
measurements of the actual AFV at cesarean delivery. Another investigation assessed the accuracy of the 2 × 2-cm
pocket for identifying a low AFV in singleton pregnancies
and noted that more than 90% of dye-determined oligohydramnios was not detected.68
An analysis of an AFI and a single deepest pocket
below the 3rd and 5th percentiles and above the 95th and
97th percentiles for detecting dye-determined or directly
measured oligohydramnios and polyhydramnios in 291
singleton pregnancies identified 11% to 27% with oligohydramnios and 33% to 46% with hydramnios.30 The
overall sensitivities of the AFI and single deepest pocket
from these studies for identifying actual normal fluid
ranged from 71% to 98%. The sensitivities and specificities for detecting actual oligohydramnios vary among the
published studies (Table 1).
Color Doppler Sonography for Estimation of the AFV
The use of color Doppler sonography has been suggested
in the evaluation of the AFV to eliminate pockets of fluid
containing the umbilical cord not detected by gray scale
sonography and thereby increase the detection of oligohydramnios. Bianco et al69 reported a significant reduction
in the measured AFI and a significant increase in the number of pregnancies with a diagnosis of oligohydramnios
when color Doppler sonography was used. In all probabil-
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Table 1. Comparison of the Predictability of the Sonographically Estimated Amniotic Fluid Volume for Identifying Dye-Determined and Directly
Measured Oligohydramnios
Study
Define Oligohydramnios
Sample Size
Horsager et al27
<200 mL
40
Chauhan et al67
<500 mL
144
Magann et al28
<500 mL
40
Amniotic Fluid Collection
Sensitivity
AFI <5 cm
AFI <8 cm
Largest vertical pocket <3 cm
AFI ≤5 cm
2-diameter amniotic pocket volume ≤15 cm2
AFI ≤5 cm
Largest vertical pocket
2-diameter amniotic pocket volume ≤15 cm2
0.18
0.36
0.18
0.05
0.58
0.067
0.0
0.60
Specificity
1.00
1.00
1.00
0.98
0.74
1.00
1.00
0.84
AFI indicates amniotic fluid index.
ity, this reduction in the estimated AFV was due to the elimination of amniotic fluid pockets when color Doppler sonography showed them to be filled with the umbilical cord.
Magann et al70 also observed a reduction in both the
AFI and the single deepest pocket by approximately 20%
with the use of color Doppler sonography compared to
gray scale sonography alone. In their investigation, they
compared the AFI and single deepest pocket to a dyedetermined AFV using color Doppler versus gray scale
sonography and observed that color Doppler sonography
led to overdiagnosis of oligohydramnios. Disturbingly,
color Doppler sonography not only did not identify any
more pregnancies with dye-determined oligohydramnios
but also labeled 9 of 42 women with normal AFVs as having oligohydramnios.70
Subjective Evaluation of Amniotic Fluid
Subjective assessment of the AFV and the quasiobjective
(AFI and single deepest pocket) techniques are both currently used to estimate the AFV. Few studies have linked
the subjective evaluation of AFV with a dye-determined or
directly measured AFV. In an assessment of the AFV at less
than 24 weeks, there was no difference in the accuracy of
subjective assessment (visual interpretation without sonographic measurements) compared to objective assessment
(visual interpretation with sonographic measurements) in
the correct identification of dye-determined amniotic
fluid.71 In another investigation of 63 pregnancies in the
second and third trimesters of pregnancy comparing subjective assessment (visual interpretation without sonographic measurements) and objective assessment (visual
interpretation with sonographic measurements) with dyedetermined fluid volumes, neither operator experience nor
the sonographic technique was observed to greatly affect
the accuracy of sonographic estimates of the AFV.36
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Amniotic Fluid Volume and Pregnancy
Outcomes
Dye-Determined AFV and Pregnancy Outcome
There are a very limited number of investigations with a
dye-determined AFV and intrapartum and perinatal outcomes within 72 hours of the AFV determination. One
investigation37 with a dye-determined AFV from 50 singleton pregnancies and delivery within 48 hours of that
AFV calculation observed a greater risk of cesarean delivery for fetal labor intolerance in the hydramnios group
compared to the normal group (P = .03), and the results
approached significance in the oligohydramnios group
compared to the normal group (P = .056). No differences
were observed between groups (oligohydramnios, normal, and hydramnios) for the risk of meconium-stained
amniotic fluid, variable decelerations influencing delivery,
or low 5-minute Apgar scores.
In another study of 100 unlabored women who had
their AFV determined by a dye dilution technique just before elective cesarean delivery, oligohydramnios was not
predictive of a low umbilical artery pH at delivery.72 In a
third investigation, 10 intrapartum and perinatal outcomes were evaluated in 74 pregnancies with a dyedetermined fluid volume and delivery within 72 hours.73
The dye-determined fluid volumes labeled as oligohydramnios, normal, and polyhydramnios were not predictive of adverse intrapartum or neonatal outcomes (fetal
heart rate variability, variable decelerations, late decelerations, fetal labor intolerance, need for amnioinfusion, intrauterine growth restriction, birth weight, mode of
delivery, umbilical artery pH <7.2, or neonatal intensive
care unit [NICU] admissions).73
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Sonographically Estimated AFV Using the AFI and
Pregnancy Outcomes
In one of the early studies linking an AFI with an adverse
pregnancy outcome, Rutherford et al25 observed a greater
risk of nonreactive nonstress tests, fetal heart rate decelerations, meconium staining, cesarean delivery for labor intolerance, and low Apgar scores in women with an AFI of 5 cm
or less. Other studies have also observed an increased risk of
adverse pregnancy and neonatal outcomes in those pregnancies with an AFI of 5 cm or less,35,74 but not all investigators agree that an AFI of 5 cm or less is associated with an
adverse pregnancy outcome. In both low-risk patients75 and
at-risk patients,76–79 oligohydramnios has not been linked to
adverse pregnancy or perinatal outcomes in other studies.
It is essential that our estimate of the AFV is accurate
and correlates with pregnancy outcomes for it to be meaningful in our management of at-risk pregnancies. Why are
a number of the studies contradictory in the correlation
between fixed cutoffs for oligohydramnios (AFI of ≤5 versus >5 cm) and intrapartum and perinatal outcomes? The
conclusions of some of the investigations are easy to understand after the articles are carefully evaluated.
In the study by Casey et al35 (adverse pregnancy outcomes after 34 weeks in pregnancies with an AFI of ≤5
versus >5 cm), after the data set was corrected for malformations and congenital syndromes, there was no difference between the pregnancies with an AFI of 5 cm or less
versus those with an AFI of greater than 5 cm in the risk of
a cesarean delivery for fetal labor intolerance, umbilical
cord arterial pH of less than 7, NICU admissions, seizures
in the first 24 hours after delivery, or neonatal death. Many
intrapartum outcomes evaluated (fetal heart rate tracing
influencing delivery, cesarean delivery for fetal labor intolerance, and Apgar scores) by the studies comparing AFIs
of 5 cm or less versus those of greater than 5 cm are subjective. The only two objective assessments are the presence of meconium and the umbilical cord arterial pH.
In a meta-analysis, Chauhan et al80 observed an increased risk of cesarean deliveries for fetal labor intolerance
and an Apgar score of less than 5 at 7 minutes in the group
with an AFI of 5 cm or less versus women with an AFI of
greater than 5 cm but observed no difference in the risk of
the objective outcome of neonatal acidosis (umbilical cord
arterial pH <7.0) between the two groups. Additionally,
investigators group many intrapartum and perinatal outcomes together in their analyses, and perhaps only some
of those outcomes are affected by low fluid volumes (eg,
fetuses with anomalies, preterm premature rupture of
membranes, growth-restricted fetuses below the 5th percentile, and postdate pregnancies).
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Estimated AFV Using the Single Deepest Pocket and
Subsequent Pregnancy Outcomes
Chamberlain et al31 evaluated the relationship of a single
deepest pocket, corrected for major congenital anomalies,
as a standalone test without any other antenatal testing and
perinatal mortality in 7582 high-risk referred patients. The
perinatal mortality rates for single deepest pocket measurements were as follows: greater than 2 cm to less than 8
cm, 1.97 per 1000 births; 1 cm or greater to 2 cm or less,
37.74 per 1000; and less than 1 cm, 109.4 per 1000.
Clinical Relevance of the Sonographically
Estimated AFV
Should We Use the AFI, the Single Deepest Pocket, or
Subjective Assessment to Estimate the AFV?
In a study of 1168 patients, Moore81 evaluated the ability
of the single deepest pocket compared to the AFI to detect
an abnormal AFV. Using the AFI, he labeled 76 women
with olioghydramnios compared to 32 using the single
deepest pocket. Moore concluded that the AFI was superior to the single deepest pocket because it identified more
women with oligohydramnios.81 However, the AFI and
single deepest pocket were compared only to each other
and not to the directly measured or dye-determined AFV.
Magann et al82 challenged the concept that the AFI
was superior to the single deepest pocket in the identification of abnormal AFVs. They compared the AFI and single deepest pocket with the dye-determined AFV to
determine whether either was superior in the detection of
abnormal AFVs in 179 singleton pregnancies. They concluded that neither technique was superior to the other,
and both techniques were unreliable in the identification of
an abnormal AFV.82 Subjective assessment of amniotic
fluid (visual interpretation without sonographic measurements) has been compared to quasiobjective methods (visual interpretation with sonographic measurements), and
both techniques were found to be similar, with neither able
to independently identify abnormal AFVs.36
How Does the AFI Compare to the Single Deepest
Pocket in the Prediction of Adverse Pregnancy
Outcomes?
Four recent randomized trials assessed the AFI versus
single deepest pocket in the prediction of pregnancy and
neonatal outcomes. Alfirevic et al83 randomized 500 pregnancies of greater than 290 days to fetal monitoring with
either a nonstress test and the AFI or a nonstress test and
the single deepest pocket. The AFI labeled 10% of the
women as having oligohydramnios versus 2% using the sin-
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gle deepest pocket (P = .0008), resulting in more labor inductions but without any differences in intrapartum or
perinatal outcomes except a trend for more cesarean deliveries (18.8% versus 13.2%) in the AFI group.
Chauhan et al84 evaluated at-risk pregnancies undergoing antenatal testing with a nonstress test and AFV estimation. The patients were randomized to either the AFI
or the single deepest pocket. They observed that significantly more patients were identified as having oligohydramnios using the AFI (17%) compared to the single
deepest pocket (10%; P =.002). No differences were noted
in the variable decelerations influencing delivery, late decelerations influencing delivery, mode of delivery, number
of cesarean or assisted vaginal deliveries for a nonreassuring fetal heart rate tracing, 1- and 5-minute Apgar scores
of less than 7, umbilical artery pH of less than 7.1 or less
than 7, or NICU admissions between groups.
In a randomized trial, Moses et al85 compared the AFI
and the single deepest pocket on admission to labor and
delivery to determine whether either was predictive of intrapartum outcomes. Oligohydramnios was diagnosed
more frequently (25% versus 8%) using the AFI compared
to the single deepest pocket (P < .001). Both techniques
failed to identify patients who subsequently underwent
amnioinfusion for fetal distress (P = .864), variable (P =
.208) or late (P = .210) decelerations that influenced delivery, fetal distress in labor (P = .220), cesarean delivery
for fetal distress (P = .133), or NICU admissions (P = .686).
They concluded that neither technique identified a pregnancy that was at risk for an adverse outcome.
Magann et al86 conducted a randomized trial to compare the AFI and the single deepest pocket in the estimation of the AFV in at-risk pregnancies undergoing antenatal
testing with a biophysical profile. The AFI significantly increased the number of pregnancies labeled as oligohydramnios (38% versus 17%) compared to the single
deepest pocket (P < .001). There was no difference in the
number of women with oligohydramnios in the AFI group
undergoing cesarean delivery for fetal intolerance of labor
versus the single deepest pocket group (13%; P =.676).
More women (12%) with normal fluid by the AFI method
(AFI >5 cm) underwent cesarean delivery for fetal distress
compared to the women (6%) with normal fluid by the
single deepest pocket technique (P =.037). They concluded that the use of the AFI offers no advantage in detecting adverse outcomes compared to the single deepest
pocket measurement with a biophysical profile. In fact, the
use of the AFI may result in more interventions by labeling
twice as many at-risk pregnancies as having oligohydramnios than with the single deepest pocket technique.
1582
A comparison of the AFI and the single deepest
pocket as a screen for preventing adverse pregnancy outcomes was also the focus of a Cochrane review.87 The
review found no differences in the primary outcomes,
NICU admissions, or perinatal deaths.87 There were more
women with a diagnosis of oligohydramnios, more labor
inductions, and more cesarean deliveries for a nonreassuring fetal heart rate tracing using the AFI but no differences
in the number of nonreassuring fetal heart rate tracings,
assisted vaginal deliveries with or without a nonreassuring
fetal heart rate tracing, umbilical artery pH of less than 7.1,
Apgar score of less than 7 at 5 minutes, presence of meconium, or NICU admissions. The authors of the review concluded that the single deepest pocket was a better choice
for antenatal testing because the AFI increased the diagnosis of oligohydramnios and labor inductions without any
improvement in peripartum outcomes.
Conclusions
In this review, we aimed to provide an overview of the dynamics of the AFV, a synopsis of what is considered in the
literature to be a “normal” AFV and a “normal” AFV as it
changes across gestation, as well as a look at the various
techniques for, and implications of, the sonographically
estimated AFV as it relates to the detection of a low AFV.
Measurement of the AFV as it relates to polyhydramnios
was not specifically addressed in this review, nor was measurement of the AFV in twin gestations.
The dynamics of the AFV are complex and not entirely understood. The regulatory balance of the AFV
seems to be focused at 3 main levels: the intramembranous
pathway, fetal urine production, which can be influenced
by several hormones, and the osmotic fluid gradient provided by the maternal-fetal relationship. As stated previously, there are yet to be clearly defined “normal” values
for the AFV and the AFV across gestation. Ideally, a normal
AFV should be defined as a value between well-defined
high and low values, which is linked to an adverse pregnancy outcome at each point across gestation. However,
these values have yet to be clearly established in the literature and are difficult to directly link to adverse pregnancy
outcomes.
There are several published curves in the literature attempting to define a “normal” AFV across gestation, each
with its own limitations and each differing from the next in
what it defines as “normal.” Selection of an AFV curve that
is most consistent with the specific population the health
care provider is managing should be considered.
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There are two main techniques used to estimate AFV
via sonography: measurement of the AFI and the single
deepest pocket. Both of these techniques can be unreliable in their ability to precisely estimate the actual AFV.
Neither the AFI nor the single deepest pocket technique
is superior to the other in the detection of oligohydramnios. Both methods have relatively low sensitivity for their
detection of a low AFV. Color Doppler sonography does
not aid in the detection of oligohydramnios; in fact, it appears to overdiagnose oligohydramnios. Another generally accepted method for evaluating the AFV and one that
is widely used by many experienced sonographers is subjective assessment of the AFV. This method has been compared to quasiobjective methods using the AFI and single
deepest pocket; neither technique was found to be superior
to the other, and neither was able to reliably identify abnormal AFVs.36,71
Additional studies are needed to determine whether
there is an association between subjective assessment of the
AFV and adverse pregnancy outcomes. On the basis of the
studies referenced in this review, the use of the AFI compared to the single deepest pocket for estimation of the AFV
results in overdiagnosis of oligohydramnios, leading to unnecessary interventions (eg, labor inductions), which often
contribute to increased morbidity and mortality without
any improvement in perinatal outcomes.84–87
References
1.
2.
3.
4.
5.
6.
7.
8.
9.
Beall MH, Van Den Wijngaard, JPHM, Van Gemert MJC, Ross MG.
Amniotic fluid dynamics. Placenta 2007; 28:816–823.
Modena AB, Fieni S. Amniotic fluid dynamics. Acta Biomed 2004;
75(suppl):11–13.
Moore TR. Amniotic fluid dynamics reflect fetal and maternal health and
disease. Obstet Gynecol 2010; 116:759–765.
Abramovich DR, Page KR. Pathways of water transfer between liquor
amnii and the feto-placental unit at term. Eur J Obstet Gynecol 1973;
3:155–158.
Lotgering FK, Wallenberg HCS. Mechanisms of production and clearance of amniotic fluid. Semin Perinatol 1986; 10:94–102.
Thurlow RW, Brace RA. Swallowing, urine flow, and amniotic fluid response to prolonged hypoxia in the ovine fetus. Am J Obstet Gynecol 2003;
189:601–608.
Gagnon R, Harding R, Brace RA. Amniotic fluid and fetal urinary responses to severe placental insufficiency in sheep. Am J Obstet Gynecol
2002; 186:1076–1084.
Prichard JA, Deglutition by normal and anencephalic fetuses. Obstet Gynecol 1965; 25:289–297.
Harding R, Bocking AD, Sigger JN, Wickham PJ. Composition and volume of fluid swallowed by fetal sheep. Q J Exp Physiol 1984; 69:487–495.
J Ultrasound Med 2011; 30:1573–1585
10. Brace RA, Wlodek ME, Cock ML, Harding R. Swallowing of lung liquid
and amniotic fluid by the ovine fetus under normoxic and hypoxic conditions. Am J Obstet Gynecol 1994; 171:764–770.
11. Ross MG, Nijland MJ. Fetal swallowing: relation to amniotic fluid regulation. Clin Obstet Gynecol 1997; 40:352–365.
12. Minei LJ, Suzuki K. Role of fetal deglutination and micturition in the production and turnover of amniotic fluid in the monkey. Obstet Gynecol
1976; 48:177–181.
13. Matsumoto LC, Cheung CY, Brace RA. Effect of esophageal ligation on
amniotic fluid volume and urinary flow rate in fetal sheep. Am J Obstet Gynecol 2000; 182:699–705.
14. Liley AW. Disorders of amniotic fluid. In: Assali NS (ed). Pathophysiology
of Gestation. New York, NY: Academic Press; 1972:157–206.
15. Adamson TM, Brodecky V, Lambert TF, et al. The production and composition of lung fluid in the in-utero foetal lamb. In: Comline RS, Cross
KW, Dawes GS, et al (eds). Foetal and Neonatal Physiology. Cambridge,
England: Cambridge University Press; 1973:208–216.
16. Gilbert WM, Brace RA. The missing link in amniotic fluid volume regulation: intramembranous absorption. Obstet Gynecol 1989; 74:748–754.
17. Faber JJ, Anderson DF. Absorption of amniotic fluid by amniochorion in
sheep. Am J Physiol Heart Circ Physiol 2002; 282:H850–H854.
18. Magann EF, Doherty DA, Chauhan SP, Barrilleaux SP, Verity LA, Martin JN Jr. Effect of maternal hydration on amniotic fluid volume. Obstet
Gynecol 2003; 101:1261–1265.
19. Kilpatrick SJ, Safford KL, Pomeroy T, Hoedt L, Scheerer L, Laros RK.
Maternal hydration increases maternal amniotic fluid index. Obstet Gynecol 1991; 78:1098–1102.
20. Anderson DF, Faber JJ, Parks CM. Extraplacental transfer of water in the
sheep. J Physiol 1988; 406:75–84.
21. Hebertson RM, Hammond ME, Bryson MJ. Amniotic epithelial ultrastructure in normal, polyhydramnic, and oligohydramnic pregnancies.
Obstet Gynecol 1986; 68:74–79.
22. Brace RA. Amniotic fluid volume and its relationship to fetal fluid balance:
review of experimental data. Semin Perinatal 1988; 10:102–112.
23. Magann EF, Doherty DA, Chauhan SP, Moses J, Newnham JP, Morrison
JC. Is there a relationship to dye determined or ultrasound estimated amniotic fluid volume adjusted percentiles and fetal weight adjusted percentiles? Am J Obstet Gynecol 2004; 190:1610–1614.
24. Owen P, Osman I, Farrell T. Is there a relationship between fetal weight
and amniotic fluid index? Ultrasound Obstet Gynecol 2002; 20:61–63.
25. Rutherford SE, Phelan JP, Smith CV, Jacobs N. The four-quadrant assessment of amniotic fluid volume: an adjunct to antepartum fetal heart
rate testing. Obstet Gynecol 1987; 70:353–356.
26. Baron C, Morgan MA, Garite TJ. The amniotic fluid volume assessed intrapartum on perinatal outcome. Am J Obstet Gynecol1995; 173:167–174.
27. Horsager R, Nathan L, Leveno KJ. Correlation of measured amniotic fluid
volume and sonographic predictions of oligohydramnios. Obstet Gynecol
1994; 83:955–958.
28. Magann EF, Nolan TE, Hess LW, Martin RW, Whitworth NS, Morrison JC. Measurement of amniotic fluid volume: accuracy of ultrasonography techniques. Am J Obstet Gynecol 1992; 167:1533–1537.
1583
3011jumonline.qxp:Layout 1
10/18/11
1:07 PM
Page 1584
Magann et al—Amniotic Fluid Volume Dynamics and Clinical Correlation
29. Dildy GA III, Lira N, Moise KJ Jr, Riddle GD, Deter RL. Amniotic fluid
volume assessment: comparison of ultrasonographic estimates versus
direct measurements with a dye-dilution technique in human pregnancy.
Am J Obstet Gynecol 1992; 167:986–994.
30. Magann EF, Doherty DA, Chauhan SP, Busch FW, Mecacci F, Morrison JC. How well do the amniotic fluid index and single deepest pocket
indices (below the 3rd and 5th and above the 95th and 97th percentiles)
predict oligohydramnios and hydramnios? Am J Obstet Gynecol 2004;
190:164–169.
31. Chamberlain PF, Manning FA, Morrison I, Harman CR, Lange IR. Ultrasound evaluation of amniotic fluid volume, I: the relationship of marginal and decreased amniotic fluid volumes to perinatal outcomes. Am J
Obstet Gynecol 1984; 150:245–249.
32. Morris JM, Thompson K, Smithey J, et al. The usefulness of ultrasound assessment of amniotic fluid in predicting adverse outcome in prolonged
pregnancy: a prospective blinded observational study. BJOG 2003;
110:989–994.
33. Magann EF, Sanderson M, Martin JN, Chauhan S. The amniotic fluid
index, single deepest pocket, and two-diameter pocket in normal human
pregnancy. Am J Obstet Gynecol 2000; 182:1581–1588.
34. Moore TR, Cayle JE. The amniotic fluid index in normal human pregnancy. Am J Obstet Gynecol 1990; 162:1168–1174.
35. Casey BM, McIntire DD, Bloom SL, et al. Pregnancy outcomes after antepartum diagnosis of oligohydramnios at or beyond 34 weeks’ gestation.
Am J Obstet Gynecol 2000; 182:909–912.
36. Magann EF, Perry KG Jr, Chauhan SP, Anfanger PJ, Whitworth NS, Morrison JC. The accuracy of ultrasound evaluation of amniotic fluid volume
in singleton pregnancies: the effect of operator experience and ultrasound
interpretative technique. J Clin Ultrasound 1997; 25:249–253.
37. Magann EF, Morton ML, Nolan TE, Martin JN Jr, Whitworth NS, Morrison JC. Comparative efficacy of two sonographic measurements for the
detection of aberrations in the amniotic fluid volume and the effects of
amniotic fluid volume on pregnancy outcomes. Obstet Gynecol 1994;
83:959–962.
38. Chamberlain PF, Manning FA, Morrison I, Harman CR, Lange IR. Ultrasound evaluation of amniotic fluid volume. II. The relationship of increased amniotic fluid volume of perinatal outcome. Am J Obstet Gynecol
1984; 150:250–254.
39. Carlson DE, Platt LD, Medearis AL, Horenstein J. Quantifiable polyhydramnios: diagnosis and management. Obstet Gynecol 1990; 75:989–993.
40. Phelen JP, Ahn MO, Smith CV, Rutherford SE, Anderson E. Amniotic
fluid index measurements during pregnancy. J Reprod Med 1987; 32:601–
604.
41. Queenan JT, Thompson W, Whitfield CR, Shah SI. Amniotic fluid volumes in normal pregnancies. Am J Obstet Gynecol 1972; 114:34–38.
42. Brace RA, Wolf EJ. Normal amniotic fluid volume changes throughout
pregnancy. Am J Obstet Gynecol 1989; 161:382–388.
43. Abramovich DR. The volume of amniotic fluid in early pregnancy. J Obstet Gynaecol Br Commonw 1968; 75:728–731.
44. Charles D, Jacoby HE, Burgess F. Amniotic fluid volumes in the second
half of pregnancy. Am J Obstet Gynecol 1965; 93:1042–1047.
1584
45. Gadd RL The volume of the liquor amnii in normal and abnormal pregnancies. J Obstet Gynaecol Br Commonw 1966; 73:11–22.
46. Gillibrand PN. Changes in amniotic fluid volume with advancing pregnancy. J Obstet Gynaecol Br Commonw 1969; 76:527–529
47. Haswell GL, Morris JA. Amniotic fluid volume studies. Obstet Gynecol
1973; 42:725–732.
48. Marsden D, Huntingford PJ. An appraisal of the Coomassie blue dilution
technique for measuring the volume of liquor amnii in late pregnancy.
J Obstet Gynaecol Br Commonw 1965; 72:65–68.
49. Nelson MM. Amniotic fluid volumes in early pregnancy. J Obstet Gynaecol
Br Commonw 1972; 79:50–53.
50. Rhodes P. The volume of liquor amnii in early pregnancyJ Obstet Gynaecol
Br Commonw 1966; 73:23–26.
51. Sinha R, Carlton M. The volume and composition of amniotic fluid in
early pregnancy. J Obstet Gynaecol Br Commonw 1970; 77:211–214.
52. van Otterlo LC, Wladimiroff JW, Wallenburg HC. Relationship between
fetal urine production and amniotic fluid volume in normal pregnancy
and pregnancy complicated by diabetes. Br J Obstet Gynaecol 1977;
84:205–209.
53. Wagner G, Fuchs F. The volume of amniotic fluid in the first half of human
pregnancy. J Obstet Gynaecol Br Emp 1962; 69:131–136.
54. Magann EF, Bass D, Chauhan SP, Young RA, Whitworth, NS, Morrison
JC. Amniotic fluid volume in normal singleton pregnancies. Obstet Gynecol 1997; 90:524–528.
55. Richards FJ. A flexible growth function for empirical use. J Exp Botany
1959; 10:290–300.
56. Richards FJ. The quantitative analysis of growth. In: Stewart FC (ed).
Plant Physiology. Vol V. Analysis of Growth: Behavior of Plants and Their
Organs. New York, NY: Academic Press; 1969:3–76.
57. Seber GAF, Wild CJ. Nonlinear Regression. New York, NY: John Wiley &
Sons; 1989.
58. Machado MH, Cecatti JC, Krupa F, Faundes A. Curve of amniotic fluid
index measurements in low-risk pregnancy. Acta Obstet Gynecol Scand
2007; 86:37–41.
59. Lei H, Wen SW, Normal amniotic fluid index by gestational week in a
Chinese population. Central-South China Fetal Growth Study Group.
Obstet Gynecol 1998; 92:237–240.
60. Manning FA, Platt LD, Sipos L. Antepartum fetal evaluation: development of a fetal biophysical profile. Am J Obstet Gynecol 1980; 136:787–
795.
61. Hallak M, Kirshon B, O’Brien Smith E, Evans MI, Cotton DB. Subjective
ultrasonographic assessment of amniotic fluid depth: comparison with
the amniotic fluid index. Fetal Diagn Ther 1993; 8:256–260.
62. Chauhan SP, Magann EF, Perry KG Jr, Morrison JC. Intrapartum amniotic fluid index and two-diameter pocket are poor predictors of adverse
neonatal outcome. J Perinatol 1997; 17:221–224.
63. Moore TR, Brace RA. Amniotic fluid index (AFI) in the term ovine pregnancy: a predictable relationship between AFI and amniotic fluid volume
[abstract 286]. Paper presented at: Annual Meeting of the Society for Gynecological Investigation; Philadelphia, PA; March 1988.
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Page 1585
Magann et al—Amniotic Fluid Volume Dynamics and Clinical Correlation
64. Magann EF, Whitworth NS, Files JC, Terrone DA, Chauhan SP, Morrison JC. Dye-dilution techniques using aminohippurate sodium: do they
accurately reflect amniotic fluid volume? J Matern Fetal Neonatal Med
2002; 11:167–170.
65. Sepulveda W, Flack NJ, Fisk NM. Direct volume measurement at
midtrimester amnioinfusion in relation to ultrasonographic indexes of
amniotic fluid volume. Am J Obstet Gynecol 1994; 170:1160–1163.
66. Croom CS, Banias BB, Ramos-Santos E, Devoe LD, Bezhadian A, Hiett
AK. Do semiquantitative amniotic fluid indexes reflect actual volume?
Am J Obstet Gynecol 1992; 167:995–999.
67. Chauhan SP, Magann EF, Morrison JC, Whitworth NS, Hendrix NW,
Devoe LD. Ultrasonographic assessment of amniotic fluid does not reflect
actual amniotic fluid volume. Am J Obstet Gynecol 1997; 177:291–296.
68. Magann EF, Nevils BG, Chauhan SP, Whitworth NS, Klausen JH, Morrison JC. Low amniotic fluid volume is poorly identified in singleton and
twin pregnancies using the 2 × 2 cm pocket technique of the biophysical
profile. South Med J 1999; 92:802–805.
69. Bianco A, Rosen T, Kuczynski E, Tetrokalashvili M, Lockwood CJ. Measurement of the amniotic fluid index with and without color Doppler. J
Perinat Med 1999; 27:245–249.
70. Magann EF, Chauhan SP, Barrilleaux S, Whitworth NS, McCurley S,
Martin JN Jr. Ultrasound estimate of amniotic fluid volume: color
Doppler overdiagnosis of oligohydramnios. Obstet Gyncol 2001; 98:71–
74.
71. Magann EF, Chauhan SP, Whitworth NS, Isler C, Wiggs C, Morrison
JC. Subjective versus objective evaluation of amniotic fluid volume of
pregnancies of less than 24 weeks’ gestation: how can we be accurate? J Ultrasound Med 2001; 20:191–195.
72. Magann EF, Chauhan SP, Martin JN Jr. Is amniotic fluid volume status
predictive of fetal acidosis at delivery? Aust NZ J Obstet Gynaecol 2003;
43:129–133.
73. Magann EF, Doherty DA, Chauhan SP, Lanneau GS, Morrison JC. Dyedetermined amniotic fluid volume and intrapartum/neonatal outcome.
J Perinatol 2004; 24:423–428.
74. Shmoys SM, Sivkin M, Dery C, Monheit AG, Baker DA. Amniotic fluid
index: an appropriate predictor of perinatal outcome. Am J Perinatol 1990;
7:266–269.
75. Zhang J, Troendle J, Meikle S, Klebanoff MA, Rayburn WF. Isolated oligohydramnios is not associated with adverse perinatal outcomes. BJOG
2004; 111:220–225.
76. Magann EF, Chauhan SP, Kinsella MJ, McNamara MF, Whitworth NS,
Morrison JC. Antenatal testing among 1001 patients at high risk: the role
of ultrasonographic estimate of amniotic fluid volume. Am J Obstet Gynecol 1999; 180:1330–1336.
77. Barrilleaux PS, Magann EF, Chauhan SP, York BM, Philibert L, Lewis DF.
Amniotic fluid index as a predictor of adverse perinatal outcome in the
HELLP syndrome. J Reprod Med 2007; 52:293–298.
78. Ott WJ. Reevaluation of the relationship between amniotic fluid volume
and perinatal outcome. Am J Obstet Gynecol 2005; 192:1803–1809.
79. Magann EF, Kinsella MJ, Chauhan SP, McNamara MF, Gehring BW,
Morrison JC. Does an amniotic fluid index of </=5 cm necessitate delivJ Ultrasound Med 2011; 30:1573–1585
80.
81.
82.
83.
84.
85.
86.
87.
ery in high-risk pregnancies? A case-control study. Am J Obstet Gynecol
1999; 180:1354–1359.
Chauhan SP, Sanderson M, Hendrix NW, Magann EF, Devoe LD. Perinatal outcome and amniotic fluid index in the antepartum and intrapartum periods: a meta-analysis. Am J Obstet Gynecol 1999;
181:1473–1478.
Moore TR. Superiority of the four-quadrant sum over the single-deepest-pocket technique in ultrasonographic identification of abnormal amniotic fluid volumes. Am J Obstet Gynecol 1990; 163:762–767.
Magann EF, Chauhan SP, Barrilleaux PS, Whitworth NS, Martin JN. Amniotic fluid index and single deepest pocket: weak indicators of abnormal
amniotic volumes Obstet Gynecol 2000; 96:737–740.
Alfirevic Z, Luckas M, Walkinshaw SA, McFarlane M, Curran R. A randomised comparison between amniotic fluid index and maximum pool
depth in the monitoring of post-term pregnancy. Br J Obstet Gynaecol
1997; 104:207–211.
Chauhan SP, Doherty DD, Magann EF, Cahanding F, Moreno F,
Klausen JH. Amniotic fluid index vs single deepest pocket technique during modified biophysical profile: a randomized clinical trial. Am J Obstet Gynecol 2004; 191:661–668.
Moses J, Doherty DA, Magann EF, Chauhan SP, Morrison JC. A randomized clinical trial of the intrapartum assessment of amniotic fluid volume: amniotic fluid index versus the single deepest pocket technique. Am
J Obstet Gynecol 2004; 190:1564–1570.
Magann EF, Doherty DA, Field K, Chauhan SP, Muffley PE, Morrison JC.
Biophysical profile with amniotic fluid volume assessments. Obstet Gynecol 2004; 104:5–10.
Nabhan AF, Abdelmoula YA. Amniotic fluid index versus single deepest
vertical pocket as a screening test for preventing adverse pregnancy outcome. Cochrane Database Syst Rev 2008; 3:CD006593.
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