TECHNICAL UPDATE No. 340, January 2017
Amniotic Fluid: Technical Update on Physiology and Measurement This Technical Update has been prepared by the Diagnostic Imaging committee, reviewed by the Society of Obstetricians and Gynaecologists of Canada (SOGC) Guideline Management and Oversight Committee and approved by the Board of the SOGC.
Abstract Objective: 1. To provide an update on the use of ultrasound to evaluate amniotic fluid volume.
PRINCIPAL AUTHORS
2. To provide an update on amniotic fluid physiology.
Kenneth I. Lim, MD, Vancouver BC
3. To promote evidence based assessment techniques and definitions for amniotic fluid volume.
Kimberly Butt, MD, Fredericton NB Kentia Naud, MD, Edmonton AB
Outcomes:
Mila Smithies, MD, Halifax NS
1. Reduced interventions as a result of the diagnosis of oligohydramnios without increasing adverse outcomes.
DIAGNOSTIC IMAGING COMMITTEE
2. By understanding the limitations of amniotic fluid assessment, promote more efficient use of ultrasound assessment.
Kimberly Butt, MD, Fredericton NB Yvonne Cargill, MD, Ottawa ON Nanette Denis, RDMS, Saskatoon SK Johanne Dubé, MD, Mont-Royal QC Phyllis Glanc, MD, Toronto ON Kenneth I. Lim (co-chair) MD, Vancouver BC Lucie Morin (co-chair), MD, Outremont QC Kentia Naud, MD, Edmonton AB Mila Smithies, MD, Halifax ON Disclosure statements have been received from all members of the committee(s).
http://dx.doi.org/10.1016/j.jogc.2016.09.012
J Obstet Gynaecol Can 2017;39(1):52e58 Copyright ª 2017 The Society of Obstetricians and Gynaecologists of Canada/La Société des obstétriciens et gynécologues du Canada. Published by Elsevier Inc. All rights reserved.
Evidence: A MEDLINE and KFINDER search was used to identify relevant articles, with review of bibliography identified article including Cochrane reviews and recent review articles. Values: The evidence collected was reviewed by the Diagnostic Imaging Committee of the Society of Obstetricians and Gynecologists of Canada. The recommendations were made according to the guidelines developed by The Canadian Task Force on Preventative Health Care (Table 1). Benefits, Harms and Costs: Amniotic fluid assessment by ultrasound has become an integral part of fetal assessment in modern obstetrics. Abnormalities of fluid volume result in obstetrical intervention and further investigations. In Canada, there are no standard definitions of fluid volume estimation, nor a standard approach to assessing fluid. Multiple randomized trials have suggested that using a Single Pocket Estimation technique (rather than the multi pocket assessment approach known as the amniotic fluid index), will result in fewer obstetrical interventions without any increase in adverse outcomes. Recent literature suggests that there are detectable, modest changes in amniotic fluid that can occur within an hour or two of normal physiological maneuvers. This may account for the variability and inconsistent results from repeated assessments within a short period of time which can lead to confusion and generate further testing. This article hopes to describe the limitations of amniotic fluid assessment, promote a standard method of amniotic fluid assessment, and propose a common set of definitions to be used to describe amniotic fluid volume.
This document reflects emerging clinical and scientific advances on the date issued and is subject to change. The information should not be construed as dictating an exclusive course of treatment or procedure to be followed. Local institutions can dictate amendments to these opinions. They should be well documented if modified at the local level. None of these contents may be reproduced in any form without prior written permission of the publisher.
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Amniotic Fluid: Technical Update on Physiology and Measurement
Table. Key to evidence statements and grading of recommendations, using the ranking of the Canadian Task Force on Preventative Health Care Quality of evidence assessment* I: Evidence obtained from at least one properly randomized controlled trial II-1: Evidence from well-designed controlled trials without randomization II-2: Evidence from well-designed cohort (prospective or retrospective) or case-control studies, preferably from more than one centre or research group II-3: Evidence obtained from comparisons between times or places with or without the intervention. Dramatic results in uncontrolled experiments (such as the results of treatment with penicillin in the 1940s) could also be included in the category III: Opinions of respected authorities, based on clinical experience, descriptive studies, or reports of expert committees
Classification of recommendations† A. There is good evidence to recommend the clinical preventive action B. There is fair evidence to recommend the clinical preventive action C. The existing evidence is conflicting and does not allow to make a recommendation for or against use of the clinical preventive action; however, other factors may influence decision making D. There is fair evidence to recommend against the clinical preventive action E. There is good evidence to recommend against the clinical preventive action L. There is insufficient evidence (in quantity or quality) to make a recommendation; however, other factors may influence decision-making
*The quality of evidence reported in these guidelines has been adapted from The Evaluation of Evidence criteria described in the Canadian Task Force on Preventive Health Care. † Recommendations included in these guidelines have been adapted from the Classification of recommendations criteria described in The Canadian Task Force on Preventive Health Care.
Summary Statements 1. Changes in amniotic fluid volume are usually gradual, however modest shifts can occur within hours due to hydration, maternal positioning, and/or activity. Water channels such as aquaporins likely facilitate these rapid changes. (I and II-2) 2. Accurate quantification of amniotic fluid volumes using current ultrasound technology remains challenging. (II-2) 3. Various techniques for single pocket estimation of amniotic fluid are described in the literature. Most of these descriptions are open to interpretation, and no particular method has been shown to be superior to the other in direct comparison. (III) 4. Using the single pocket estimation method of amniotic fluid assessment in the third trimester to diagnose oligohydramnios, rather than the amniotic fluid index method, will result in fewer interventions without increasing adverse perinatal outcomes. (I) 5. Polyhydramnios as defined using amniotic fluid index is associated with a variety of adverse outcomes. More studies are needed looking at outcomes of polyhydramnios using the single pocket estimation definitions of polyhydramnios. (II-2) 6. There is insufficient literature to determine which method of amniotic fluid assessment is more reproducible than the other. (II-1)
ABBREVIATIONS AFI
amniotic fluid index
AFV
amniotic fluid volume
BPP
biophysical profile
CS
Caesarean section
RCT
randomized controlled trial
SDP
single deepest pocket
SOGC
Society of Obstetricians and Gynaecologists of Canada
SPE
single pocket estimation
7. It is proposed that the Chamberlain classification of amniotic fluid be used to define oligohydramnios (single deepest pocket [SDP] smaller than 2 cm in depth 1 cm wide) and polyhydramnios (SDP greater than 8 cm in depth 1 cm wide) for the initial assessment of amniotic fluid during routine obstetrical scanning. (I) Recommendation: 1. It is recommended that the initial, general evaluation of amniotic fluid volume during routine obstetrical ultrasound be a single pocket estimation. The Chamberlain method of amniotic fluid assessment is the preferred method for estimation. (I-A)
INTRODUCTION
T
he assessment of AFV has been an integral component of obstetrical scanning and fetal health surveillance for many years. Abnormalities of amniotic fluid are associated with a variety of adverse maternal, fetal, and obstetrical conditions. Modern obstetrical management relies significantly on assessment of amniotic fluid as a measure of fetal well-being.
However, amniotic fluid assessment by two-dimensional ultrasound is at best semi-quantitative. It is not a true quantitative measurement and is probably more qualitative than quantitative. The volume and shape of the amniotic fluid compartment is very dynamic due to fetal and maternal factors, which introduces a subjective component to its measurement. It can be difficult to duplicate and obtain accurate assessments of the volume of amniotic fluid, especially at the extremes. The SOGC guideline on fetal surveillance (2007) provides an overview of the use of amniotic fluid estimation in fetal
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surveillance.1 It describes both the Amniotic Fluid Index (AFI) and Single Pocket Estimation (SPE) techniques of measurement and suggests that SPE is preferable. However, no specific recommendations relating to amniotic fluid assessment were included in that guideline. Across the country, amniotic fluid is assessed using various methods, in isolation or in combination, without uniformly agreed upon definitions. There is currently no Canadian consensus on how to best measure and document/describe amniotic fluid volume. The intent of this technical update is to review the most recent relevant literature and to make recommendations on amniotic fluid assessment during obstetrical ultrasound. A future, separate publication will cover the subject in more detail. Physiology
The volume of amniotic fluid relies on a balance between production and uptake.2,3 In the second half of pregnancy, amniotic fluid volume (AFV) is mostly a balance between fetal urine output and fetal swallowing. Prior to that, maternal plasma and solutes, driven by hydrostatic and osmotic forces, form the bulk of the fluid in the amniotic space.4 Therefore, one cannot attribute AFV solely on fetal renal function in the first half of pregnancy. Later in gestation, additional sources of fetal contribution to amniotic fluid include lung and gastrointestinal secretions. Estimated levels of output from all fetal components suggest that only a small fraction of the AFV is being turned over on an hourly basis, which led to the belief that AFV does not change rapidly.2,3 Under conditions of utero-placental insufficiency, the fetus regionalizes blood flow to critical areas such as the heart and brain, at the expense of renal perfusion. Decreased blood flow to the kidneys results in decreased renal output, leading to oligohydramnios. Given the above, a reduction in amniotic fluid to the point of oligohydramnios representing fetal compromise may take a few days to fall below a level where ultrasound may detect it. However, a more modern concept recognizes that amniotic fluid is dynamic and can rapidly change due to normal maternal physiological processes (hydration, activity/rest, position, etc.). There is likely a limit to how much amniotic fluid can be affected by these factors, but this modifiable component, as assessed by AFI, is as much as 45 mm.5,6 due to the dynamic nature of amniotic fluid, and the resulting imprecision in its measurement, this is unlikely to make a difference in most situations; however, it may alter the diagnosis when closer to the upper and lower thresholds of normal.
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Ulker demonstrated that detectable changes in AFI (and fetal urine output) can occur within an hour or so of initiation of a maneuver such as hydration, rest, or maternal positioning.5,7e9 These findings may help explain the inconsistency of results when tests are repeated within hours of each other or performed by different operators. Furthermore, it is unclear whether manipulation of these modifiable factors affects fetal outcomes or changes the diagnostic value of amniotic fluid assessment. These rapid fluid shifts may be attributable to the intramembranous and transmembranous pathways that allow solutes and free water to move back and forth between maternal and fetal compartments. Free water channels known as aquaporins are up-regulated when needed, such as in idiopathic polyhydramnios,10e12 to help modulate the amount of amniotic fluid. It is probable that this “rapid transient” component is applicable to only a portion of the total AFV. Ulker’s work suggests that AFV behaves like a saturation curve in response to hydration and rest.5 It would be difficult to control all of the physiological factors that may affect the AFV in the typical diagnostic ultrasound lab. While simple to ensure maternal hydration, positioning women in the left lateral position for a sufficient duration would be more difficult, given that patients are scanned in a supine (commonly wedged) position. Physiologically, it is unknown if rest in the supine position, as opposed to left lateral, would increase or decrease AFV (presumably due to uterine compression of vena cava and/ or aorta leading to decreased placental perfusion). It is suggested that women be well hydrated prior to the ultrasound exam to ensure that maternal hydration is not a factor in the diagnosis of oligohydramnios. Summary Statements
1. Changes in amniotic fluid volume are usually gradual, however modest shifts can occur within hours due to hydration, maternal positioning, and/or activity. Water channels such as aquaporins likely facilitate these rapid changes. (I and II-2)
Technical Aspects
The volume of amniotic fluid that surrounds a fetus is a complex 3-dimensional form that is difficult to quantify with single axis vectors. Methods that employ summation of parallel multi-planar slices are cumbersome and time consuming, limiting their regular use. The dye dilution
Amniotic Fluid: Technical Update on Physiology and Measurement
technique is far too invasive and complex to be considered on a wide scale, notwithstanding the potential toxicities to the fetus with the use of a dye or measurable solutes. Thus, we are left with either qualitative (visual estimation) or semi-quantitative methods of amniotic fluid determination. The semi-quantitative methods can be loosely described as multi-pocket (AFI) or single pocket estimation (SPE) based on the largest pocket of fluid found on ultrasound. There are many different methods of SPE, which include different pocket dimensions: 2 2,13 2 1,14,15 2-dimensional product,16 or a single vertical depth measurement of the largest pocket.17 The technical methods of obtaining SPE are difficult to describe since the literature descriptions are very old or of insufficient detail. Generally, the maternal position is not described for SPE, nor is the transducer orientation. For example, Chamberlain’s method specifies that the pocket width must be at least 1 cm and at least 2 cm in the depth axis, which is at right angles to the uterus. Some operators look for any 2 cm 1 cm pocket regardless of transducer angle, orientation, or plane. Sande describes his technique as “ultrasound probe being held vertical to the uterine contour onto the abdomen and parallel to the maternal sagittal plane.”17 This does not appear to match the Chamberlain definition, particularly since the minimum width of the pocket is not included. The commonly used biophysical profile (BPP) 2 2 pocket does not specify transducer plane nor orientation. Kehl describes a 2 1 pocket in which the long axis is vertical.15 There are no outcome studies that directly compare the various methods of SPE. A number of papers18e21 compared determining AFI with and without using color Doppler. In the past, the literature showing a difference in measurements was likely a result of the inability to see the umbilical cord, which is unlikely today using modern ultrasound machines. Summary Statements
2. Accurate quantification of amniotic fluid volumes using current ultrasound technology remains challenging. (II-2) 3. Various techniques for single pocket estimation of amniotic fluid are described in the literature. Most of these descriptions are open to interpretation, and no particular method has been shown to be superior to the other in direct comparison. (III) Terminology
The terminology used to describe AFV assessment is varied and inconsistent, adding to the confusion when
assessing the literature. For example, Chamberlain’s paper has been referenced using the following terms: single deepest pocket (SDP),15,18 maximum vertical pocket,22 maximum pool depth,23 and single deepest vertical pocket.24 Sande uses the terms “single deepest vertical pool” or “maximum vertical pocket” to describe his.17 For this technical update, it was felt that using the term “single deepest pocket” was the one most often ascribed to Chamberlain and removes the word “vertical,” which suggests that the ultrasound plane has to be vertical or perpendicular to the floor, which is not included in Chamberlain’s description. Recent and Major Literature Review
The Nabhan Cochrane meta-analysis included five randomized trials comparing AFI (oligo definition of less than 5 cm) versus SPE (2 cm 1 cm pocket).25 No differences in pH <7.0, low Apgar scores, neonatal intensive-care unit admission, non-reassuring fetal heart rate tracing, meconium, or CS rates were seen. The use of AFI, however, resulted in significant differences in diagnosis of oligohydramnios and rate of induction of labour and CS for fetal distress. It should be noted that three of the five randomized control trials (RCTs)24e26 referenced Chamberlain directly whereas the fourth27 can be ascribed to Chamberlain. A recently published randomized trial is not yet incorporated in the most recent meta-analysis.15 It supports the findings of the Nabhan meta-analysis suggesting that SDP be used over AFI. However, the AFI group had fewer gestational diabetics and patients with previous CS than the SDP group, and the studied population was a mixture of low and high risk patients (15%), although post dates were not considered a high risk indication. A significantly higher rate of abnormal blood gases found in the group assigned to SDP was considered clinically non-significant as base excess and low Apgar scores were not different between the two groups. Moore has argued that the RCTs comparing AFI to SDP are not based on technique but definitions of oligohydramnios for the two.2 He points out the normal curve percentile thresholds for diagnosis of oligohydramnios between AFI and SDP (using AFI <5 cm, SDP <2 cm) are different, so the RCTs compared different percentile thresholds. He suggests the definition of oligo using AFI should be reduced to 3.0 cm. However, this threshold has not been studied, and so it would be difficult to bring to clinical practice without sufficient supporting evidence as to its safety relative to the original <5.0 cm. Morris performed a meta-analysis and systematic review of the literature looking at perinatal outcomes of
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oligohydramnios and comparing results of studies using SPE versus AFI.28 One conclusion was that both AFI and SPE estimations have very similar associations to adverse outcomes, and he could not find a statistical reason to choose one over the other. The analysis for outcomes associated with polyhydramnios is limited to papers using AFI only, and so no comparison can be made with regards to outcomes of polyhydramnios comparing definitions by AFI and SPE. Sande et al. recently published a study looking at inter- and intra-observer limits of agreement for both AFI and their definition of SPE.17 They found that the limits of variation for both were quite wide. Williams et al. found that the SPE method they used had poorer reproducibility than AFI.22 Therefore, the studies on reproducibility of the different techniques are inconsistent. Some have noted that all of the randomized trials were conducted in patients at later gestational ages, typically from mid-third trimester onwards, with the majority of data at or beyond term. Whether the findings in those studies can be extrapolated to preterm pregnancies, especially before 32 weeks, remains to be seen. With regards to polyhydramnios, the vast majority of the literature uses AFI as the assessment technique. Chamberlain’s original study using his method of SPE for defining polyhydramnios, retrospectively found that corrected perinatal mortality is modestly increased using that definition.14 There are no prospective studies of outcomes of polyhydramnios using an SPE definition. Therefore, in some situations, the continued use of the AFI to help define and/or clinically manage polyhydramnios may be appropriate until such time as more data is available. Summary Statements
4. Using the single pocket estimation method of amniotic fluid assessment in the third trimester to diagnose oligohydramnios, rather than the amniotic fluid index method, will result in fewer interventions without increasing adverse perinatal outcomes. (I) 5. Polyhydramnios as defined using amniotic fluid index is associated with a variety of adverse outcomes. More studies are needed looking at outcomes of polyhydramnios using the single pocket estimation definitions of polyhydramnios. (II-2) 6. There is insufficient literature to determine which method of amniotic fluid assessment is more reproducible than the other. (II-1)
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Definitions
Originally, Chamberlain defined levels of amniotic fluid according to the largest pocket of fluid having depth as decreased (<1 cm), marginal (1e2 cm), normal (>2 cm, less than or equal to 8 cm), and polyhydramnios (>8 cm).14 The Cochrane meta-analysis RCT used depth measurements between 1.8 and 2.0 cm as the lower threshold for normal. The following definitions are proposed for the initial assessment of amniotic fluid during general, routine obstetrical scanning. The largest pocket of fluid found is referred to as the SDP. Oligohydramnios: SDP smaller than 2 cm in depth by 1 cm wide Normal: SDP 2e8 cm in depth (and at least 1 cm in width) Polyhydramnios: SDP of fluid greater than 8 cm depth (and at least 1 cm in width) Further subdivisions for clinical use (e.g., severe oligohydramnios, severe polyhydramnios) may be possible, but at present, there is insufficient literature to determine what those threshold levels should be using SPE. As more data becomes available, individual centers may need to modify the definition of polyhydramnios. Based on Magann’s published normal curves, thresholds of 2 and 8 cm would be well below and well above the 5th percentile and 95th percentile, respectively, across both the second and third trimesters so gestational age adjustments are not needed. The use of blended methods of amniotic fluid assessment for initial assessment of amniotic fluid is discouraged to avoid confusion and to maintain simplicity. However, as discussed earlier, AFI may still be used to help define/ stratify polyhydramnios for referral and/or clinical management. Amniotic fluid assessment during BPP deserves special mention. All methods of fluid assessment are ascribed in the literature to BPP (vertical depth, SDP dimensions of 2 1, 2 2, 1 1, and AFI), with the original being a 1 cm 1 cm pocket.13 There are few studies which compare methods of fluid assessment during BPP. Chauhan, in his randomized trial, used the Chamberlain 2 cm 1 cm definition and showed it to be preferable over AFI.18 A SPE of fluid during BPP is advocated, but there is no clear evidence one is superior to the other.
Amniotic Fluid: Technical Update on Physiology and Measurement
Summary Statement
7. It is proposed that the Chamberlain classification of amniotic fluid be used to define oligohydramnios (single deepest pocket [SDP] less than 2 cm in depth 1 cm wide) and polyhydramnios (SDP greater than 8 cm in depth 1 cm wide) for the initial assessment of amniotic fluid during routine obstetrical scanning. (I) Future Direction
It is clear that there needs to be more contemporary studies looking at the methodology of amniotic fluid assessment, comparing measurement techniques and correlating outcomes with different levels of AFV. In particular, SPE thresholds for polyhydramnios and its clinical associations are lacking. More in depth understanding of the physiological factors that influence AFV is required. CONCLUSION
This technical update reflects an attempt to assess the current available literature, noting its limitations, to optimize the use of ultrasound in the measurement of amniotic fluid. The available evidence indicates that using the AFI to diagnose oligohydramnios leads to more interventions without any significant improvement in outcomes. Neither is superior based on association of outcomes or reproducibility. We propose that a single pocket technique be used to estimate AFV and specifically advocate the Chamberlain method. Other methods of SPE may be as valid but do not have the preponderance of evidence that the Chamberlain method does. The Chamberlain definition is somewhat open to interpretation. Adaption of other definitions, such as Kehl’s, may also be considered as they have evidence to support its use. Recommendation
8. It is recommended that the initial, general evaluation of amniotic fluid volume during routine obstetrical ultrasound be a single pocket estimation. The Chamberlain method of amniotic fluid assessment is the preferred method for estimation. (I-A)
REFERENCES 1. Liston R, Sawchuck D, Young D. Society of Obstetricians and Gynaecologists of Canada; British Columbia Perinatal Health Program. Fetal health surveillance: antepartum and intrapartum consensus guideline. J Obstet Gynaecol Can 2007;29:S3e56.
2. Moore TR. The role of amniotic fluid assessment in evaluating fetal wellbeing. Clin Perinatol 2011;38:33e46. v. 3. Magann EF, Sandlin AT, Ounpraseuth ST. Amniotic fluid and the clinical relevance of the sonographically estimated amniotic fluid volume: oligohydramnios. J Ultrasound Med 2011;30:1573e85. 4. Underwood MA, Gilbert WM, Sherman MP. Amniotic fluid: not just fetal urine anymore. J Perinatol 2005;25:341e8. 5. Ulker K, Cicek M. Effect of maternal hydration on the amniotic fluid volume during maternal rest in the left lateral decubitus position: a randomized prospective study. J Ultrasound Med 2013;32:955e61. 6. Kilpatrick SJ, Safford KL. Maternal hydration increases amniotic fluid index in women with normal amniotic fluid. Obstet Gynecol 1993;81:49e52. 7. Ulker K, Cecen K, Temur I, Gul A, Karaca M. Effects of the maternal position and rest on the fetal urine production rate: a prospective study conducted by 3-dimensional sonography using the rotational technique (virtual organ computer-aided analysis). J Ultrasound Med 2011;30:481e6. 8. Ulker K, Gul A, Cicek M. Correlation between the duration of maternal rest in the left lateral decubitus position and the amniotic fluid volume increase. J Ultrasound Med 2012;31:705e9. 9. Ulker K, Temur I, Karaca M, Ersoz M, Volkan I, Gul A. Effects of maternal left lateral position and rest on amniotic fluid index: a prospective clinical study. J Reprod Med 2012;57:270e6. 10. Zhu X, Jiang S, Hu Y, Zheng X, Zou S, Wang Y, et al. The expression of aquaporin 8 and aquaporin 9 in fetal membranes and placenta in term pregnancies complicated by idiopathic polyhydramnios. Early Hum Dev 2010;86:657e63. 11. Damiano AE. Review: water channel proteins in the human placenta and fetal membranes. Placenta 2011;(32 Suppl 2):S207e11. 12. Mann SE, Dvorak N, Gilbert H, Taylor RN. Steady-state levels of aquaporin 1 mRNA expression are increased in idiopathic polyhydramnios. Am J Obstet Gynecol 2006;194:884e7. 13. Manning FA, Platt LD, Sipos L. Antepartum fetal evaluation: development of a fetal biophysical profile. Am J Obstet Gynecol 1980;136:787e95. 14. 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 outcome. Am J Obstet Gynecol 1984;150:245e9. 15. Kehl S, Schelkle A, Thomas A, Puhl A, Meqdad K, Tuschy B, et al. Single deepest vertical pocket or amniotic fluid index as evaluation test for predicting adverse pregnancy outcome (SAFE trial): a multicenter, openlabel, randomized controlled trial. Ultrasound Obstet Gynecol 2016;47:674e9. 16. 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;182:1581e8. 17. Sande JA, Ioannou C, Sarris I, Ohuma EO, Papageorghiou AT. Reproducibility of measuring amniotic fluid index and single deepest vertical pool throughout gestation. Prenat Diagn 2015;35:434e9. 18. 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;191:661e7. discussion 7e8. 19. Magann EF, Chauhan SP, Barrilleaux PS, Whitworth NS, McCurley S, Martin JN. Ultrasound estimate of amniotic fluid volume: color Doppler overdiagnosis of oligohydramnios. Obstet Gynecol 2001;98:71e4. 20. 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;27:245e9. 21. Zlatnik MG, Olson G, Bukowski R, Saade GR. Amniotic fluid index measured with the aid of color flow Doppler. J Matern Fetal Neonatal Med 2003;13:242e5.
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22. Williams K, Wittmann B, Dansereau J. Intraobserver reliability of amniotic fluid volume estimation by two techniques: amniotic fluid index vs. maximum vertical pocket. Ultrasound Obstet Gynecol 1993;3:346e9. 23. Nwosu E, Welch C, Walkinshaw S. Measurement of amniotic fluid volume using maximum pool depth. Cont Reviews in Obs and Gynec 1996;6:25e30. 24. 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;190:1564e9. discussion 9e70.
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25. 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. 26. Magann EF, Doherty DA, Field K, Chauhan SP, Muffley PE, Morrison JC. Biophysical profile with amniotic fluid volume assessments. Obstet Gynecol 2004;104:5e10. 27. 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;104:207e11. 28. Morris RK, Meller CH, Tamblyn J, Malin GM, Riley RD, Kilby MD, et al. Association and prediction of amniotic fluid measurements for adverse pregnancy outcome: systematic review and meta-analysis. BJOG 2014;121:686e99.