|Year : 2015 | Volume
| Issue : 3 | Page : 98-107
Knowledge attitude and practices of ultrasound safety in pregnancy among healthcare providers in Riyadh, Saudi Arabia: a survey study
Ahmed T ElOlemy1, Mohammed S Almuwannis2, Majed S Alamiri3, Khudhair M Alkhudair3
1 Department of Public Health and Community Medicine, Faculty of Medicine, Tanta University, Tanta, Egypt
2 Department of Radiological Sciences, College of Applied Medical Sciences, Riyadh, Saudi Arabia
3 Medical Imaging Department, King Saud Medical City, Riyadh, Saudi Arabia
|Date of Submission||11-Dec-2014|
|Date of Acceptance||15-Mar-2015|
|Date of Web Publication||7-Aug-2015|
Ahmed T ElOlemy
Department of Public Health and Community Medicine, Faculty of Medicine, Tanta University, Building (B), N0 (11), AlKholafaa AlRashdeen buildings, High way Tanta Alex st., Kohafa, Tanta
The present study aimed to assess knowledge, attitudes, and practices of safety of ultrasound during pregnancy among healthcare providers in Riyadh, Saudi Arabia.
Materials and methods
This cross-sectional descriptive survey was conducted in Riyadh city, Saudi Arabia, between January and March, 2014. Six hospitals were selected randomly, one from each health sector in the kingdom. All Obstetrics and Gynecology physicians, Radiologists, General practitioners, family physicians, Sonographers, and nurse practitioners in the selected hospitals were the target of the study. They answered a questionnaire containing 30 items.
Fifty-two percent of 685 respondents who completed the survey were nurse practitioners, 11.5% were sonographers, and 36.6% were physicians, most of them radiologists (n = 110/251). Sixty percent disapproved of keepsake ultrasound examinations. 75.9 and 84.7% of the respondents were not familiar with the term thermal index (TI) and mechanical index (MI), respectively. Only 7% of respondents knew the answer to the specific question on the TI and MI correctly, and 24.5% knew that TI and MI are displayed on the sonographic monitor during the examinations. In terms of Doppler examination, 38.2% never performed a Doppler examination during the first trimester, in contrast to 19.3%, who always performed it.
There was poor knowledge of ultrasound safety in pregnancy among healthcare providers: physicians, sonographers, and nurse practitioners. This lack of knowledge is an alarm signal for the health authorities; thus, there is a need for training programs for all healthcare providers. Most participants rarely performed a Doppler examination during the first trimester and did not advise nonradiology doctors to scan.
Keywords: Doppler ultrasound; knowledge and practices; mechanical index; pregnancy; Saudi Arabia; thermal index; ultrasound safety
|How to cite this article:|
ElOlemy AT, Almuwannis MS, Alamiri MS, Alkhudair KM. Knowledge attitude and practices of ultrasound safety in pregnancy among healthcare providers in Riyadh, Saudi Arabia: a survey study. Tanta Med J 2015;43:98-107
|How to cite this URL:|
ElOlemy AT, Almuwannis MS, Alamiri MS, Alkhudair KM. Knowledge attitude and practices of ultrasound safety in pregnancy among healthcare providers in Riyadh, Saudi Arabia: a survey study. Tanta Med J [serial online] 2015 [cited 2018 Nov 19];43:98-107. Available from: http://www.tdj.eg.net/text.asp?2015/43/3/98/162445
| Introduction|| |
Ultrasound is an imaging modality that has important diagnostic value. It is used widely in prenatal diagnosis. It is commonly perceived as a safe diagnostic procedure that does not harm the developing fetus if used properly  . Meanwhile, it is important to keep in mind that diagnostic ultrasound transmits energy into the patient. It has the potential to exert certain bioeffects in the form of heating and cavitation  . These effects are inherent in the physical properties of the ultrasound transducers. Heating and cavitation are approximated by the thermal index (TI) for heating and the mechanical index (MI) for cavitation effects  .
The TI provides a rough guide of the magnitude of increase in temperature that might be produced after a long exposure , . A TI of 1.0 corresponds to a potential for increase of 1°C. A larger TI value represents a higher heating potential and hence a higher risk. A temperature increase less than 1.5°C likely does not present a risk to the embryo. A temperature increase of 1.5-2°C may lead to a developmental effect. A temperature increase greater than 4°C for 5 min can exert a risk of bioeffects on the embryo  .
The MI is a measure of pressure fluctuations within the ultrasound pulse. It is intended to offer the potential for the ultrasound to induce a nonthermal bioeffect, including cavitation in tissues. It is related to the intensity of the pulse  . Cavitation can be either inertial or transient, which may be capable of exerting biological effects, or noninertial, which is less likely to exert biological effects. As a general role, the MI should be kept as low as possible while obtaining the necessary diagnostic information  .
The output of ultrasound equipment for fetal applications was increased from 94 to 720 mW/cm 2 to increase its diagnostic value. At that time, 1992, the US Food and Drug Administration (FDA) established the Standard for Real-time Display of Thermal and Mechanical Indices on Diagnostic Ultrasound machines, named the output display standard (ODS)  . The ODS supplies on-screen numerical displays that provide information on TI and MI  . The as low as reasonably achievable (ALARA) principle was also recommended. As a general strategy, the on-screen TI and MI values should be monitored after scanner adjustments and kept ALARA  .
Knowledge of risks of common radiological procedures and how to express these risks to patients are competencies required by physicians and healthcare providers. Knowledge gaps of hospital physicians on radiation dose and risk are evident from published research. Also, patients are not fully informed of the radiation risks associated with radiological tests  .
Poor knowledge among hospital doctors of levels of radiation exposure, with most clinicians significantly underestimating the relative exposure associated with common radiological investigations, has been reported previously , . Meanwhile, some researches have reported a beneficial effect from radiation training, recording increased knowledge and awareness of radiation dose ,, .
The aim of this study was to assess the knowledge, attitudes, and practices of safety aspects of diagnostic ultrasound during pregnancy among healthcare providers in Riyadh, Saudi Arabia.
| Materials and methods|| |
A cross-sectional descriptive survey was conducted in Riyadh city, capital of Saudi Arabia, between January and March, 2014. Riyadh city has a population of 7 309 966 individuals according to estimated census 2013G. There are 46 governmental hospitals and 32 nongovernmental hospitals in Riyadh city, representing 17.8% of all hospitals of Saudi Arabia. From the 46 governmental hospitals, 36 are general ones and the rest are specialized, of which five hospitals are for women and children. The governmental hospitals are related to many sectors including the Ministry of Health, University hospitals, militarily hospitals, National Guard hospitals, and Security Forces hospitals. From each sector, a hospital was chosen randomly. The obstetric hospital in King Saud Medical City, King Khalid University Hospital, Riyadh Military Hospital, National Guard Hospital in Riyadh, Security Forces Hospital in Riyadh, respectively, and British-Saudi Hospital for Obstetrics and Gynecology (from specialized hospitals) were selected by a simple random sample. All obstetrics and gynecology physicians, radiologists, general practitioners, family physicians, sonographers, and nurse practitioners in the selected hospitals were the target of the study. Six hundred and eighty-five individuals participated in the study, yielded a response rate of 58%. This may be attributed to the heavy work load of healthcare providers in hospitals and lack of time to answer the questionnaire.
Data were collected by a self-administered questionnaire used previously and published in the study by Sheiner et al.  and approved by an Institutional Review Board. This questionnaire included 30 items. The following issues were addressed:
- Demographic data included age, sex, nationality, qualification, specialty, number of years in work, and place of work;
- Information on the average number of ultrasound examinations that participants performed daily, limitations in the number of ultrasound examinations that a 'low-risk' pregnant women should undergo during her pregnancy, and any adverse events to the fetus during ultrasound examinations;
- Whether ultrasound and Doppler ultrasound during the first, second, and third trimesters of pregnancy, perfectly safe without limitations, safe but should be used mainly when medically indicated, or should be used only for medical reasons;
- How often participants performed Doppler ultrasound during the first trimester, and their thoughts on keepsake ultrasound performed in a nonmedical facility;
- Familiarity with ultrasound bioeffects, TI and MI, their knowledge of these indices, and where TI and MI present during a clinical examination; and
- Their attitude toward who should scan and interpret scan images.
Questionnaires were distributed and collected within 15 min. Answering the questionnaire was considered as an informed consent.
Ethical considerations were addressed through approval of the ethical committee of hospitals that participated in the study. Data entry and statistical analysis were carried out using the SPSS statistical package for windows version 19 (SPSS Inc., Chicago, Illinois, USA). Data were analyzed using frequencies, percentages, mean, and SD. Statistical associations between sonographers, nurse practitioners, and physicians were tested using a 95% confidence interval for proportion.
| Results|| |
Out of 1180 health workers, 685 completed the survey, yielding a response rate of 58%. [Table 1] presents the demographic characteristics of the study participants. The mean age ± SD of the participants studied was 34.28 ± 9.81 years. Thirty-three percent of the participants were men (n = 227); 67.2% (n = 460) were Saudi. Fifty-two percent of participants were nurse practitioners (n = 355) and 36.6% (n = 251) were physicians, most of them radiologists (n = 110). Approximately 69% (n = 471) of respondents had less than 10 years of experience.
|Table 1: Demographic characteristics of the participants studied (n = 685)|
Click here to view
Knowledge levels of study participants of ultrasound safety in pregnancy are shown in [Table 2]. More than half (54%) of the respondents - mostly nurse practitioners (223/355) and sonographers (48/79) - believed that there should be limitations on the number of ultrasound examinations in low-risk pregnancies. Only 39.44% (99/251) of physicians have the same believe. About one-third of respondents, mostly physicians (116/251), believed that less than five scans are appropriate. More than three-fourths (76.9%) of respondents, mostly nurse practitioners (295/355) and physicians (177/251), stated that there are no adverse effects to the fetus during ultrasound examination. Sixty percent of respondents disapproved of keepsake ultrasound examinations. More than 70% (n = 491) of the participants, mostly sonographers (67/79) and physicians (201/251), did not know that an increase in temperature could potentially be teratogenic during the first trimester of pregnancy. There was a statistically significant association between occupation of respondents and different items on their knowledge of ultrasound safety of pregnancy (P < 0.05).
|Table 2: Knowledge of the participants studied of ultrasound safety in pregnancy in relation to respondents ' occupation|
Click here to view
Knowledge of ultrasound and Doppler ultrasound safety in the first, second, and third trimesters of pregnancy in relation to respondents' occupation is shown in [Table 3]. Physicians stated that ultrasound was safer than Doppler ultrasound at any time of pregnancy, whereas sonographers stated that ultrasound was safer only during the first trimester of pregnancy. However, nurse practitioners did not believe that there was any difference in safety between ultrasound and Doppler ultrasound at any time of pregnancy.
|Table 3: Knowledge of the participants studied of ultrasound and Doppler ultrasound safety in the fi rst, second, and third trimester of pregnancy in relation to respondents ' occupation|
Click here to view
Knowledge of TI and MI is presented in [Table 4] and [Figure 1], [Figure 2] and [Figure 3]. More than three-fourths (75.9 and 84.7%) of the respondents were not familiar with the term TI and MI, respectively, most of whom were nurse practitioners and sonographers. However, 7% of the respondents, mostly sonographers, knew the answer to the specific question of the TI and MI correctly. In addition, only 24.5% of the respondents - none of the sonographers - knew that TI and MI are displayed on the sonographic monitor during the examinations. There was a statistically significant association between the occupation of respondents and different items in terms of their knowledge of TI and MI (P = 0.000).
|Figure 2: Percentage of respondents who did not know the meaning of TI and M I of 1.|
Click here to view
|Figure 3: Frequency of respondents who did not know that TI and MI are displayed on the sonographic monitor during the examin ations.|
Click here to view
|Table 4: Knowledge of the participants studied of the thermal index and the mechanical index in relation to respondents ' occupation|
Click here to view
Attitudes and practices
Practices of ultrasound safety in pregnancy and attitudes of the study participants in terms of who should scan and interpret scan images are shown in [Table 5]. The mean number of ultrasound examinations performed by the study respondents per day was 13.37 ± 7.49 SD. In terms of Doppler examination, 38.2% of the participants never performed a Doppler examination during the first trimester, in contrast to 19.3%, who always did. With respect to who should scan and interpret scan images, 53.9 and 59.0% of the participants reported that radiographers and prepart 1 radiology resident, respectively, should perform scanning. However, 45.4% stated that radiographers should not interpret scan images. About three-fourths (72%) of the participants stated that nonradiology doctors should not perform scanning.
|Table 5: Practices of ultrasound safety in pregnancy and attitudes of study respondents of who should scan and interpret scan images (n = 685)|
Click here to view
| Discussion|| |
Approximately 250 million fetal ultrasound examinations are performed per year in the USA  . Fetal ultrasound is considered to be safe. There is no evidence that diagnostic ultrasound may be harmful. To date, no adverse effects on the fetus have been reported at diagnostic levels in laboratory studies. Subtle or transient effects are not well understood. Otherwise, ultrasound exposure can produce bioeffects  . Because of wide clinical practice, the knowledge of potential bioeffects in tissues is mandatory  . Studies from Norway and Sweden have raised the possibility that fetal exposure to diagnostic ultrasound may exert effects on subsequent handedness  .
Sheiner et al.  , in the USA reported that the mean number of ultrasound examinations per day was 7.8 ± 6.0, and 18% of the participants routinely performed Doppler ultrasound examinations during the first trimester. This is nearly half that reported in the present study, where the mean number of ultrasound examinations was 13.37 ± 7.49.0 and 19.3% always performed a Doppler examination during the first trimester and 32.6% performed a Doppler examination sometimes.
Healthcare providers in our study were divided on the issue of limiting the number of ultrasound examinations that a 'low-risk' pregnant woman should undergo during her pregnancy. This is the same picture in the USA  . However, a lower percent (36%) of the ultrasound end users in Israel believed that the number of ultrasounds performed in low-risk pregnancy should be limited  .
More than 35% of the respondents actually approved of keepsake ultrasound examinations without any clinical indication (souvenir photos of the unborn child performed in a nonmedical facility). These procedures are generally performed by physicians significantly more than sonographers and nurse practitioners. These results were similar to those of Sheiner et al.  , who reported that more than 30% of the ultrasound professionals actually approved of keepsake ultrasound examinations, but it was generally performed by sonographers and this is in contrast to our results. The American Institute of Ultrasound in Medicine reported that this diagnostic procedure should be used prudently and should be performed only when there is a valid medical indication  . The promotion, selling, or leasing of ultrasound equipment for making 'keepsake fetal videos' is considered by the US FDA to be an unapproved use of a medical device. Use of a diagnostic ultrasound system for these purposes, without a physician's order, may be in violation of state laws or regulations  . Otherwise, Wax et al.  , pointed out that although most end users do not favor nonmedically indicated examinations, they do not believe that sonographers performing these examinations should be reported or punished. Nelson et al.  , stated that it should only be performed by trained, competent personnel. The lowest possible ultrasonic exposure setting should be used to obtain the necessary diagnostic information according to the ALARA principle  .
Professional ultrasound end users in the USA showed poor knowledge of safety issues. Most did not answer the TI question correctly and even fewer answered the MI question correctly. Only 21% knew where to find the TI and MI during an ultrasound examination  . Similar to their American counterparts, Only 22% of European professionals using ultrasound for fetal examinations could explain what the TI was and only 11% could provide a correct explanation for the MI. Only 28% correctly indicated where, on their own machines, they could find the information on the acoustic indices  . Sharon et al.  , reported that 44.1% were familiar with the term TI, whereas only 22.4% answered the related question correctly; 26.6% were familiar with the term MI, but only 4.9% described it correctly. More than 80% of the end users did not know where to find the acoustic indices while performing the examination  . Unfortunately, our study does not show a better picture.
Manufacturers are obliged to provide information on safety indices (i.e. the TI and MI values), but the responsibility for the ultrasound output energy is, ultimately, that of the end users: sonographers, radiologists, obstetricians, gynecologists, and others  . Healthcare providers should be familiar with the output energy, how to control it, and, accordingly, how to use the machine in a safe manner. Nevertheless, if they are not familiar with the acoustic indices or where to find them, one can assume that they will not be able to control them.
Few studies have evaluated the levels of TI and MI and the exposure time during standard obstetric ultrasound examinations ,,, . These studies have shown that the TI values occasionally exceed 2.0 when color or spectral pulsed wave Doppler modes are applied. This is despite the fact that in most obstetric examinations, fully satisfactory images and/or Doppler signals can be obtained at low levels of TI and MI ,, . 3D ultrasound does not introduce additional safety considerations. 4D ultrasound with continuous exposure offers the potential to prolong examination times  . Spectral pulsed Doppler and Color Doppler modes can reach higher levels than B mode ultrasound; thus, they should be avoided in the first trimester of pregnancy because of potential for tissue heating  . Importantly, most data indicating a lack of adverse effects on human fetuses are based on older studies using lower intensities  . Respondents in the present study agreed that ultrasound is safer than Doppler ultrasound.
Damage has been observed in tissues with gas pockets at MI more than 0.3. Unnecessary exposure to neonatal lung should be avoided. MI should be maintained as low as possible. MI provides a rough guide to sonographers on nonthermal hazards  .
In 1976, the US FDA began regulating the output levels of machines to no more than a 94 mW/cm 2 spatial-peak temporal-average intensity for fetal use. In 1992, under pressure from manufacturers and end users, the FDA changed this limit to 720 mW/cm 2 , but mandated that machines capable of producing higher outputs display to the diagnostician some indication of the likelihood of ultrasound-induced bioeffects (ODS)  . This ODS consists of the TI and the MI, a document produced jointly by the American Institute of Ultrasound in Medicine and the National Electrical Manufacturers Association (1992)  . The purpose of the ODS was to provide the capability for end users of diagnostic ultrasound to operate their machines at higher levels to increase diagnostic capabilities. The ODS did not specify any upper limits  . Marsal  , concluded that the ODS failed to provide a practical useful platform during obstetric examinations. The ALARA principle was also recommended  .
The Safety Group of the British Medical Ultrasound Society established Guidelines for the safe use of diagnostic ultrasound equipment. These Guidelines cover the following issues: medical endorsement, operator training, awareness of machine factors influencing hazard, initial power setting, exposure time, stationary probe, probe self-heating, pre-existing temperature increase, sensitive tissues, pulsed Doppler, thermal and mechanical indices, and non-diagnostic uses of diagnostic ultrasound equipment  . The ultrasound operator must control the factors that influence ultrasound exposure.
The strengths of this study are that it focused on an important issue worldwide; in addition, this is the first study on this issue in the kingdom. Among the limitations of this study is that it covers only healthcare providers in Riyadh city, with limited generalization of results and a relatively low response rate.
| Conclusion|| |
There was poor level of knowledge of safety issues among healthcare providers. This lack of knowledge is an alarm signal for the health authorities, and indicates that there is a need to establish training programs for all healthcare providers. Further efforts in the realm of education and training are needed to improve healthcare providers' knowledge of the acoustic output of the machines and safety issues. Healthcare providers should basically understand the basic physics, chemistry, and biology of radiation to effectively impart and communicate facts about radiation as well as promote and practice appropriate protection measures. Moreover, an effective medical education model should be developed in medical schools and health training institutions to address the knowledge gap currently observed in clinical practice. A major curriculum revision of both undergraduate and graduate medical education on the awareness of ultrasound safety is mandatory to improve this gap. Most participants rarely performed a Doppler examination during the first trimester and did not advice nonradiology doctors to scan.
Human rights statements and informed consent
All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and according to the Helsinki Declaration of 1975, as revised in 2008. Informed consent was obtained from all participants before inclusion in the study.
| Acknowledgements|| |
The authors thank the College of Applied Medical Sciences Research Center and the Deanship of Scientific Research at King Saud University for supporting this research.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Newnham JP, Doherty DA, Kendall GE, Zubrick SR, Landau LL, Stanley FJ. Effects of repeated prenatal ultrasound examinations on childhood outcome up to 8 years of age: follow-up of a randomised controlled trial. Lancet 2004; 364:2038-2044.
American Institute of Ultrasound in Medicine. Mechanical bio-effects from diagnostic ultrasound: AIUM Consensus Statements. Section 8. J Ultrasound Med 2000; 19:149-153.
National Council on Radiation Protection and Measurements (NCRP). Exposure criteria for medical diagnostic ultrasound, II: criteria based on all known mechanisms
. Bethesda, MD: NCRP; 2002. NCRP report 140.
O'Brien WD Jr, Deng CX, Harris GR, Herman BA, Merritt CR, Sanghvi N, Zachary JF The risk of exposure to diagnostic ultrasound in postnatal subjects: thermal effects. J Ultrasound Med 2008; 27:517-535; quiz 537-40.
Abramowicz JS, Barnett SB, Duck FA, Edmonds PD, Hynynen KH, Ziskin MC. Fetal thermal effects of diagnostic ultrasound. J Ultrasound Med 2008; 27:541-559; quiz 560-3.
Barnett SB (ed). World Federation for Ultrasound in Medicine and Biology Symposium on Safety of Ultrasound in Medicine. Recommendation on the safe use of ultrasound. Ultrasound Med Biol 1998; 24:xv-xvi.
O'Brien WD, Siddiqi TA. Obstetric sonography: the output display standard and ultrasound bio-effects. In: Fleischer AC, Manning FA, Jeanty P, Romero R (editors) Sonography in Obstetrics and Gynecology: Principles and Practice
. 6th ed. New York, NY: McGraw-Hill; 2001. 29-48.
Abramowicz JS, Kossoff G, Marsál K, Ter Haar G. Literature review by the ISUOG bioeffects and safety committee. Ultrasound Obstet Gynecol 2002; 19:318-319.
Abbott JG. Rationale and derivation of MI and TI - a review. Ultrasound Med Biol 1999; 25:431-441.
Abramowicz JS, Kossoff G, Marsal K, Ter Haar G. Safety Statement, 2000 (reconfirmed 2003). International Society of Ultrasound in Obstetrics and Gynecology (ISUOG). Ultrasound Obstet Gynecol 2003; 21:100.
Miller MW, Brayman AA, Abramowicz JS. Obstetric ultrasonography: a biophysical consideration of patient safety - the 'rules' have changed. Am J Obstet Gynecol 1998; 179:241-254.
Krille L, Hammer GP, Merzenich H, Zeeb H. Systematic review on physician's knowledge about radiation doses and radiation risks of computed tomography. Eur J Radiol 2010; 76:36-41.
Shiralkar S, Rennie A, Snow M, Galland RB, Lewis MH, Gower-Thomas K, et al
. Doctors' knowledge of radiation exposure: questionnaire study. BMJ 2003; 327:371-372.
Bosanquet DC, Green G, Bosanquet AJ, Galland RB, Gower-Thomas K, Lewis MH. Doctors' knowledge of radiation - a two-centre study and historical comparison. Clin Radiol 2011; 66:748-751.
Jacob K, Vivian G, Steel JR. X-ray dose training: are we exposed to enough? Clin Radiol 2004; 59:928-934.
Soye JA, Paterson A. A survey of awareness of radiation dose among health professionals in Northern Ireland. Br J Radiol 2008; 81:725-729.
Sheiner E, Shoham-Vardi I, Abramowicz JS. What do clinical users know regarding safety of ultrasound during pregnancy? J Ultrasound Med 2007; 26:319-325; quiz 326-7.
Nelson TR, Fowlkes B, Abramowicz Duque A. Ultrasound Biosafety Considerations for the Practici Son ra her/Sonol ist. JUM 2008; 2:167-78.
Pavlova E, Ivanov S. Potential bioeffects in interaction between ultrasound and tissue - safety of diagnostic ultrasound. Akush Ginekol (Sofiia) 2013; 52:29-32.
American Institute of Ultrasound in Medicine. Bio-effects literature reviews. J Ultrasound Med 2004; 23:1535-1542.
Sharon N, Shoham-Vardi I, Aricha-Tamir B, Abramowicz JS, Sheiner E. What do ultrasound performers in Israel know regarding safety of ultrasound, in comparison to the end users in the United States? Harefuah 2012; 151:146-149. 190
American Institute of Ultrasound in Medicine. AIUM practice guideline for the performance of obstetric ultrasound examinations. J Ultrasound Med 2013; 32:1083-1101.
Wax JR, Cartin A, Pinette MG, Blackstone J. Nonmedical fetal ultrasound: knowledge and opinions of Maine obstetricians and radiologists. J Ultrasound Med 2006; 25:331-335.
Marsál K. The output display standard: has it missed its target? Ultrasound Obstet Gynecol 2005; 25:211-214.
Sheiner E, Freeman J, Abramowicz JS. Acoustic output as measured by mechanical and thermal indices during routine obstetric ultrasound examinations. J Ultrasound Med 2005; 24:1665-1670.
Deane C, Lees C. Doppler obstetric ultrasound: a graphical display of temporal changes in safety indices. Ultrasound Obstet Gynecol 2000; 15:418-423.
Sheiner E, Shoham-Vardi I, Pombar X, Hussey MJ, Strassner HT, Abramowicz JS. An increased thermal index can be achieved when performing Doppler studies in obstetric sonography. J Ultrasound Med 2007; 26:71-76.
Barnett SB, Maulik D, International Perinatal Doppler Society. Guidelines and recommendations for safe use of Doppler ultrasound in perinatal applications. J Matern Fetal Med 2001; 10:75-84.
Gail R, Jacques S, Iwaki A, David HE, Marvin CZ, Karel M. Do we need to restrict the use of Doppler ultrasound in the first trimester of pregnancy? Ultrasound Med Biol 2013; 39:374-380.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]