[Obstetrical ultrasound: can the fetus hear the wave and feel the heat?]. / Ultraschall in der Geburtshilfe: Kann der Fötus die Ultraschallwelle hören und die Hitze spüren?

"Fetuses can hear ultrasound and the sound is as loud as a subway train entering a station." This statement originates in a single report in a non-peer reviewed journal, despite its name 1, of a presentation at a scientific meeting by researchers who reported measuring the sound intensity in the uterus of pregnant women and being able to demonstrate the above. This was later published in a peer-review journal 2 probably not very widely read by clinicians or the general public. From time to time, the popular press or various pregnancy-related websites repeat the assertion or a worried pregnant patient inquires about the truthfulness of this statement. A second, oft-quoted concern is that ultrasound leads to heating of the amniotic fluid. These two assertions may be very concerning to expectant parents and merit scientific scrutiny. In this editorial, we shall examine the known facts about the physical properties of ultrasound as they relate to these two issues. Diagnostic ultrasound employs a pulsed sound wave with positive and negative pressures and the Mayo team, quoted in the New Scientist, predicted that the pulsing would translate into a "tapping" effect 1. According to their report, they placed a tiny hydrophone inside a woman's uterus while she was undergoing an ultrasound examination. They stated that they picked up a hum at around the frequency of the pulsing generated when the ultrasound is switched on and off. The sound was similar to the highest notes on a piano. They also indicated that when the ultrasound probe was pointed right at the hydrophone, it registered a level of 100 decibels, as loud as a subway train coming into a station. Sound levels in decibels are defined for audible frequencies with the reference level being the threshold for hearing at a given frequency. Although the operating frequencies used in sonography are inaudible, it is possible for the pulsing rate (pulse repetition frequency, PRF) to be heard, thus falling in the audible range. A previous report had hinted at similar phenomena 3.Ultrasound is a pressure wave with a frequency beyond (ultra) that detectable in the human auditory system. The human ear can discern sound at roughly 20 - 20 000 cycles (hertz) per second. The frequencies of diagnostic ultrasound are roughly 1 - 10 megahertz (MHz) or 1 000 000 to 10 000 000 cycles per second. It is a form of energy and, as such, may have effects in tissues it traverses. Any consequences occurring in living tissues secondary to an external influence are called biological effects or bioeffects. This term does not imply damage or harm. The two major mechanisms for bioeffects are thermal and non-thermal. Thermal effects are secondary to ultrasound energy being converted into heat in the tissue (indirect effect of ultrasound) and non-thermal effects are secondary to the alternating positive and negative pressures generated by the wave (direct effect). The definition of moderately loud sound is 60 - 70 dB (2 × 10-3-2 × 10-2 Pa), defined as high urban ambient sound, normal conversation at 1 m, or living room music 4. In comparison, quiet conversation is 40 dB, a railway diesel engine passing at 45 mph at 100 feet is 80 - 85 dB and a rock band is 110 dB 4. There have been a few publications describing harm to fetuses exposed to elevated levels of ambient noise, particularly industrial noise 567, specifically in the aircraft and textile industries, but while there have been reports of impaired hearing in infants who were exposed to ultrasound in the womb, several rigorous studies have disproved that notion 891011. Furthermore, a study of fetuses exposed in utero to vibroacoustic stimulation 12 and a recent study of fetuses exposed to noise generated during an MR exam of the pregnant women 13 showed no ill effect on the auditory system. There have been some reports of being able to hear a "hum" during transcranial ultrasound. This may be the pulse-repetition frequency (PRF), but, if so, it would be described as a higher pitch, and probably not a "hum". To our knowledge, this phenomenon has not been investigated. Although the report mentioned above suggested that diagnostic ultrasound is detectable at measurable levels in the uterus, there is no independently confirmed, peer-reviewed, published evidence that the fetus actually hears the PRF, responds to it or is harmed by it."The fetus cannot regulate its own body temperature, so amniotic fluid can reach very high temperatures over long periods" 14. Does this statement reflect a real risk? What does it mean if this statement is scientifically true? The fear is, of course, that this will raise the temperature of the fetus. Thermally induced teratogenesis has been demonstrated in many animal studies, as well as several controlled human studies 1516. A temperature increase of 1.5 °C above the normal value has been suggested as a universal threshold 17. It is important to note that diagnostic ultrasound was not the source of the temperature elevation in any of these studies. Some believe that there are temperature thresholds for hyperthermia-induced birth defects (hence the ALARA [as low as reasonably achievable] principle), but there is some evidence that any positive temperature differential for any period of time has some effect, in other words there may be no thermal threshold for hyperthermia-induced birth defects 18. In experimental animals the most common defects are microcephaly with associated functional and behavioral problems 17, microphthalmia and cataracts. There are reports on the effects of hyperthermia and measurements of in vivo temperature induced by pulsed ultrasound but not in humans 192021. Temperature increases of 1 °C are easily reached in routine scanning 22. Elevation of up to 1.5 °C can be obtained in the first trimester and up to 4 °C in the second and third trimesters, particularly with the use of pulsed Doppler 23. When the ultrasound wave travels through tissue, its intensity diminishes with distance (attenuation). In completely homogeneous materials, the signal amplitude is reduced only by beam divergence and absorption (conversion of sound to heat). However, biologic tissues are non-homogeneous and further weakening occurs due to scattering. The issue of temperature increase in the amniotic fluid is based on the fact that the energy of the ultrasound waves is partially converted to heat in the tissue traversed by the waves. Tissues with a high absorption coefficient (such as bone) will produce a high conversion rate while the conversion will be lower in tissues with low absorption. Fluids have very low absorption characteristics and, therefore, the risk of temperature elevation in the amniotic fluid is minimal. The only available study on the topic did not demonstrate any increase in temperature in the amniotic fluid when performing diagnostic ultrasound, both in grayscale anatomic imaging (sonography) and Doppler ultrasound 24. ConclusionWhile ultrasound is a sound wave which can produce mechanical effects and temperature elevation in tissues that it traverses, the risk to human fetuses when using diagnostic ultrasound appears to be minimal if certain rules are followed, such as performing a scan when medically indicated, and observing the ALARA principle (using the lowest output power consistent with acquiring the necessary diagnostic information and keeping the exposure time as low as possible for accurate diagnosis).

Ultrasonic attenuation estimation of the pregnant cervix: a preliminary report.

OBJECTIVE: Estimates of ultrasonic attenuation (the loss of energy as an ultrasonic wave propagates through tissue) have been used to evaluate the structure and function of tissues in health and disease. The purpose of this research was to develop a method to estimate ultrasonic cervical attenuation during human pregnancy using a clinical ultrasound system. METHODS: Forty women underwent a cervical scan once during pregnancy with the Zonare z.one clinical ultrasound system using a 4-9-MHz endovaginal transducer. This ultrasound system provides access to radiofrequency (RF) image data for processing and analysis. In addition, a scan of a tissue-mimicking phantom with a known attenuation coefficient was acquired and used as a reference. The same settings and transducer used in the clinical scan were used in the reference scan. Digital data of the beam-formed image were saved in Digital Imaging and Communications in Medicine (DICOM) format on a flash drive and converted to RF data on a personal computer using a Matlab program supplied by Zonare. Attenuation estimates were obtained using an algorithm that was independently validated using tissue-mimicking ultrasonic phantoms. RESULTS: RF data were acquired and analyzed to estimate attenuation of the human pregnant cervix. Regression analysis revealed that attenuation was: a predictor of the interval from ultrasound examination to delivery (beta = 0.43, P = 0.01); not a predictor of gestational age at time of examination (beta = - 0.23, P = 0.15); and not a predictor of cervical length (beta = 0.077, P = 0.65). CONCLUSIONS: Ultrasonic attenuation estimates have the potential to be an early and objective non-invasive method to detect interval between examination and delivery. We hypothesize that a larger sample size and a longitudinal study design will be needed to detect gestational age-associated changes in cervical attenuation.

Ultrasound of the placenta: a systematic approach. Part II: functional assessment (Doppler).

Doppler velocimetry is the ideal clinical tool to assess placental performance in high-risk pregnancies. It also has value in predicting later complications and outcome in pregnancies which appear uncomplicated. All three circulations (fetal, placental and maternal) may be interrogated by Doppler technology. In the following review, we present basic physics aspects of Doppler and discuss mainly Doppler investigation of the fetal-placental circulation (umbilical artery, intraplacental circulation) as well as the uterine arteries. The assessment of umbilical blood flow provides information on blood perfusion of the fetal-placental unit. The diastolic blood flow velocity component in umbilical artery increases with advancing gestation. In pregnancies complicated by placental dysfunction, there may be a reduction in the number of functional villi and/or small blood vessels with, as a result, increased impedance, reflected, mainly, by a decrease in end-diastolic velocity. When the resistance increases even more, there is no diastolic forward velocity (absent end-diastolic velocity). Further increase in the resistance causes reversed end-diastolic velocity, which is considered a late step in the cascade of events leading to intrauterine fetal demise. Doppler assessment of the umbilical arteries was found to improve outcome of high-risk pregnancies, and reduce hospital admissions. On the contrary, routine Doppler ultrasound in low risk or unselected populations does not seem to confer benefit on mother or newborn. Uterine artery Doppler is a useful test in predicting pregnancies at high risk of developing complications related to uteroplacental insufficiency. It identifies women who may benefit from increased antenatal surveillance or prophylactic therapy. Three-dimensional power Doppler sonography can provide new insights into placental pathophysiology.

Ultrasound of the placenta: a systematic approach. Part I: Imaging.

Diagnostic ultrasound has been in use in clinical obstetrics for close to half-a-century. However, in the literature, examination of the placenta appears to be treated with less attention than the fetus or the pregnant uterus. This is somewhat unexpected, given the obvious major functions this organ performs during the entire pregnancy. Examination of the placenta plays a foremost role in the assessment of normal and abnormal pregnancies. A methodical sonographic evaluation of the placenta should include: location, visual estimation of the size (and, if appearing abnormal, measurement of thickness and/or volume), implantation, morphology, anatomy, as well as a search for anomalies, such as additional lobes and tumors. Additional assessment for multiple gestations consists of examining the intervening membranes (if present). The current review considers the various placental characteristics, as they can be evaluated by ultrasound, and the clinical significance of abnormalities of these features. Numerous and varied pathologies of the placenta can be detected by routine ultrasound. It is incumbent on the clinician performing obstetrical ultrasound to examine the placenta in details and in a methodical fashion because of the far reaching clinical significance and potentially avoidable severe consequences of many of these abnormalities.

In utero imaging of the placenta: importance for diseases of pregnancy.

Maurice Panigel demonstrated by X-rays, almost 40 years ago, placental maternal blood jets in non-human primates. Although to researchers the importance of the placenta is evident, in clinical obstetrical imaging, the fetus takes precedence. The placenta is imaged almost as an after thought and mostly to determine its location in the uterus. In animal species, the placenta was imaged with techniques which would be considered too invasive (or too costly for routine use) in humans, many pioneered by Panigel: radioangiography, radioisotopes scintigraphy, thermography, magnetic resonance imaging (MRI) and spectroscopy, positive emission tomography (PET) and single photon emission computed tomography (SPECT). Ultrasound allows for detailed, and, as far as is known, safe analyses of not only placental structure in the human but also its function. Earlier, only 2-dimensional grey-scale was available and more than 20 years ago, placental grading was popular. Later, colour imaging and spectral Doppler analysis of blood velocity both in the umbilical artery and within the placenta as well as the uterus and fetal vessels became essential and, more recently, the use of ultrasound contrast agents has been described, albeit not yet in a clinical setting. Three-dimensional ultrasound permits evaluation of the placenta in several planes, more precise depiction of internal vasculature as well as more accurate volume assessment. Several medical disorders of the pregnant woman or her fetus begin or end in the placenta, and ultrasound is the optimal investigation method. Obvious examples include pre-eclampsia and other forms of hypertension in pregnancy, less than optimal fetal growth (i.e. intrauterine growth restriction), triploidy (and its placental manifestation: partial mole), non-immune hydrops as well as several infectious processes. Ultrasound is also particularly suited to evaluate specific placental conditions, such as abnormal placentation (placenta previa and accrete for instance), gestational trophoblastic disease and placental tumors (e.g. chorioangioma).

A comparison between acoustic output indices in 2D and 3D/4D ultrasound in obstetrics.

OBJECTIVE: Three-dimensional (3D) ultrasound is gaining popularity in prenatal diagnosis. While there are no studies regarding the safety of 3D ultrasound, it is now widely performed in non-medical facilities, for non-diagnostic purposes. The present study was aimed at comparing the acoustic output, as expressed by thermal index (TI) and mechanical index (MI), of conventional two-dimensional (2D) and 3D/4D ultrasound during pregnancy. METHODS: A prospective, observational study was conducted, using three different commercially available machines (iU22, Philips Medical Systems; Prosound Alfa-10, Aloka; and Voluson 730 Expert, General Electric). Patients undergoing additional 3D/4D ultrasound examinations were recruited from those scheduled for fetal anatomy and follow-up exams. Fetuses with anomalies were excluded from the analysis. Data were collected regarding duration of the exam, and each MI and TI during 2D and 3D/4D ultrasound exams. RESULTS: A total of 40 ultrasound examinations were evaluated. Mean gestational age was 31.1 +/- 5.8 weeks, and mean duration of the exam was 20.1 +/- 9.9 min. Mean TIs during the 3D (0.27 +/- 0.1) and 4D examinations (0.24 +/- 0.1) were comparable with the TI during B-mode scanning (0.28 +/- 0.1, P = 0.343). The MIs during the 3D volume acquisitions were significantly lower than those in the 2D B-mode ultrasound studies (0.89 +/- 0.2 vs. 1.12 +/- 0.1, P = 0.018). The 3D volume acquisitions added 2.0 +/- 1.8 min of actual ultrasound scanning time (i.e. not including data processing and manipulation, or 3D displays, which are all post-processing steps). The 4D added 2.2 +/- 1.2 min. CONCLUSIONS: Acoustic exposure levels during 3D/4D ultrasound examination, as expressed by TI, are comparable with those of 2D B-mode ultrasound. However, it is very difficult to evaluate the additional scanning time needed to choose an adequate scanning plane and to acquire a diagnostic 3D volume.

Hyperthermic teratogenicity, thermal dose and diagnostic ultrasound during pregnancy: implications of new standards on tissue heating.

Hyperthermia is a recognized teratogen in mammalian laboratory animals and is a suspected teratogen for humans. The purpose of this synopsis is to reanalyse existing data on hyperthermia-induced teratogenic effects in experimental mammalian systems in terms of a thermal dose (temperature:time) concept, and then to illustrate the utility of this concept to human situations involving potential thermal increments to post-implantation embryos and foetuses. For example, the threshold temperature elevation for hyperthermia-induced teratogenic effects in experimental mammals is estimated (but not rigorously tested) to be approximately 1.5 degrees C above core values for exposures of long duration, possibly with a thermal dose of approximately 5 min duration or more at 4 degrees C. This level of tissue temperature increment is within the capability of some modern diagnostic ultrasound (DUS) devices sold within the USA and abroad. Epidemiological studies have not indicated any hazard from the use of DUS, but such studies are limited in sensitivity and were conducted with DUS devices whose acoustic outputs were relatively low compared to those presently available. After a regulatory change that allowed for substantially increased acoustic outputs, modern DUS devices were mandated to provide the user with on-screen information (the Thermal Index, or 'TI') about ultrasound-induced temperature increments in the target tissue. The TI is generally accurate to within a factor of 2, but the factor may be as high as 6 in certain obstetric settings. Thus, informed use of and attention to the TI is strongly advised, with this admonition gaining increased emphasis if the present regulations regarding allowable acoustic outputs of DUS devices were to be further relaxed or eliminated.

Comparative sensitivity of human fetal and adult erythrocytes to hemolysis by pulsed 1 MHz ultrasound.

Human fetal and adult erythrocytes differ significantly in mean corpuscular volume (MCV), the fetal cells being larger than adult cells and diminishing in MCV as gestational age (GA) increases. Previous studies have shown that the sensitivity of erythrocytes from different species to lysis by mechanically applied shear stress increases as MCV increases. The tested hypotheses in the present project were: 1. fetal erythrocytes would be more sensitive to sonolysis than adult erythrocytes because of the former's larger size, and 2. erythrocyte sonolytic sensitivity would scale with MCV. Fetal and adult erythrocytes were resuspended to 40% hematocrit in oxygenated isotonic saline solution and 500 microL aliquots were exposed for 60 s to 200 micros bursts of 1-MHz ultrasound (US) (peak pressures: approximately 4.8 MPa positive, approximately 2.7 MPa negative; duty factor = 0.01), either with or without 3.6 volume % Albunex (ALX) present. Background-corrected hemolysis was indistinguishable from zero in sham-exposed fetal or adult erythrocyte suspensions. Without ALX, mean background-corrected US-induced hemolysis was significantly greater than zero for fetal and adult cells (0.42 +/- 0.15% vs. 0.62 +/- 0.15), but fetal cell lysis was not significantly greater than adult cell lysis. With ALX, US-induced hemolytic yields increased approximately 80-fold (fetal: 50.53 +/- 2.14; adult: 46.40 +/- 1.85%), and were significantly higher for fetal than for adult cells. There was also a statistically significant correlation between MCV and US-induced background-corrected hemolysis. Thus, the two hypotheses were supported.

Sonographic investigation of flow patterns in the perfused human placenta and their modulation by vasoactive agents with enhanced visualization by the ultrasound contrast agent Albunex.

PURPOSE: Our objective was to demonstrate sonographically the flow distribution in the circulation of human placentae as well as the sensitivity of the human fetal capillary bed to vasoconstriction and dilatation. METHODS: Five human full-term placental lobules were maintained in vitro with fetal and maternal flow. Commercial ultrasound scanners were used for imaging. Albunex (1 ml bolus) was administered to the fetal "artery" to monitor patterns of flow. U46619 (1 ml, 10(-6) M; a thromboxane agonist and potent vasoconstrictor) and/or nitroglycerin (a potent vasodilator) were added to the fetal artery. RESULTS: Following the addition of U46619, mean "fetal pressures" rapidly rose from 23.2 +/- 0.8 to 118 +/- 2. 9 mm Hg (mean +/- standard error of mean; p < 0.001); venous flow rates decreased. As demonstrated by color Doppler imaging, flow markedly changed from a pattern of general distribution throughout the lobule to flow only near the chorionic plate. Color persistence was 94.4 +/- 6.5 seconds with Albunex after nitroglycerin and 39.8 +/- 3.4 seconds with Albunex after injection of U46619 (p < 0.001). Nitroglycerin had no effect when injected by itself but returned "constricted" flow to a "normal" pattern when injected after U46619. CONCLUSIONS: The contrast medium Albunex improved visualization of the fetal circulation throughout the lobule. Flow in the human placental capillary bed can be regionally manipulated throughout the placental lobule by vasomodulators and monitored by Albunex-enhanced sonographic examination.

Obstetric ultrasonography: a biophysical consideration of patient safety--the "rules" have changed.

We address the issue of health and safety in relation to exposure to diagnostic ultrasound, with particular emphasis given to obstetrics. In terms of fetal and maternal outcomes, the epidemiologic record of diagnostic ultrasound is exemplary but is primarily made on the basis of data derived from clinical devices whose outputs were relatively low compared with what is now allowable and available. The power outputs of clinical devices have been increasing over the past decade such that the potential for thermal and nonthermal insults is increased. For obstetric devices that use these higher outputs, the Food and Drug Administration now requires the presentation of 2 on-screen indexes, the thermal index and the mechanical index, in recognition of the 2 major mechanisms by which ultrasonography is known to affect cells and tissues. Greater responsibility for patient safety is now placed on the diagnostician; for the new indexes to be meaningful the diagnostician must be cognizant of the health and safety implications. The purpose of this article is to provide some guidance to the obstetrician in interpreting the indexes and to review the current status of ultrasonography biophysics in relation to the use of diagnostic ultrasound in obstetrics.

Incorporating sonographic cheek-to-cheek diameter, biparietal diameter and abdominal circumference improves weight estimation in the macrosomic fetus.

The objective of this study was to improve the accuracy of sonographic fetal weight estimation in macrosomic (> 4000 g) fetuses by combining the cheek-to-cheek diameter (CCD), an indicator of subcutaneous tissue mass, with the biparietal diameter (BPD) and abdominal circumference (AC) in generating a new weight formula. Three hundred well-dated, uncomplicated singleton pregnancies > 32 weeks' gestational age (GA) were analyzed. Sonographic fetal measurements obtained in every case included BPD, head circumference, AC, femur length and CCD. Sonographic estimation of fetal weight (EFW) was derived by using BPD and AC. Actual birth weights (BW) of fetuses delivered within 7 days of the last sonographic examination and weighing over 1500 g (n = 123) were compared to EFW. A formula was derived by correlating BPD, AC and CCD with BW in these 123 fetuses using multiple regression analysis. A second formula was derived from the data of 39 macrosomic fetuses. The two formulae were then tested for accuracy of prediction of fetal weight in 157 other fetuses delivered within 7 days and grouped by birth weight, 44 of them weighing > 4000 g. The new formula for macrosomic fetuses was: EFW (g) = 1065 + 84.5 BPD (cm) + 41.29 AC (cm) + 111.0 CCD (cm). In the macrosomic fetuses, a difference of < 10% between EFW and BW was demonstrated in 72.7% by the BPD-AC formula and 95.5% when incorporating CCD. In this group, the mean percentage error was significantly smaller: 4.14 vs. 7.97% (p = 0.0005). In the regression analysis, the contributions of BPD, AC and CCD to the variance in BW were 5.5%, 16%, and 18.3%, respectively (p = 0.008). In the non-macrosomic fetuses, CCD improved prediction of BW, but the trend did not reach statistical significance. Our results demonstrate that, in the macrosomic fetus, CCD explains more of the variance in BW than other parameters and incorporating it in the sonographic weight estimation greatly improves its accuracy.