Abstract
An 18-year-old single mother presented for counseling following the diagnosis of a hypoplastic left heart syndrome in the fetus. Despite being encouraged by her family members to terminate the pregnancy, the clinicians involved endeavored to provide information in a non-directive manner in accordance with widely accepted norms for antenatal counseling. Following the consultation, however, the clinicians wondered whether they should have provided more directive advice. In this report, we review the ethics of counseling following the diagnosis of a severe fetal cardiac abnormality. We assess the general and specific arguments in favor of providing directive advice, at least in some circumstances. There may be legitimate concerns about harms to the fetus, to the mother, or to the wider community from continuing a pregnancy. While these arguments yield rare exceptions to the generally accepted practice that antenatal counseling should not be directive, they may still not apply to the more severe forms of congenital cardiac abnormalities.
Case report
Ms. A, an 18-year-old primigravida with no family history of congenital heart disease, was referred to a multidisciplinary fetal cardiac unit at a tertiary center at 23 weeks’ gestation because of a fetal cardiac abnormality. She attended with her mother and aunt, her partner having left her.
A detailed fetal cardiac ultrasound confirmed the diagnosis of a hypoplastic left heart syndrome (HLHS), characterized by underdevelopment of the left-sided structures of the heart, including the left atrium, mitral valve, left ventricle, and the ascending aorta. Fetal intervention was not feasible. Ms. A and her mother were informed in simple terms that following delivery, major surgery would be required. That would be followed by at least two further operations in infancy and early childhood, and a possible need for later cardiac transplantation if the single right ventricle was to fail. The overall surgical mortality is of the order of 20–40%. Specific learning problems are not uncommon, although most surviving children do not have serious physical or cognitive impairment.
This information was presented to Ms. A in simple terms and as completely as possible. Diagrams were drawn to explain the abnormality and its anticipated management. Ample opportunity was given for any questions to be answered and to allow each of those present to express their views. Ms. A herself remained quiet but seemed resolved to continue with the pregnancy. Her mother remarked forcefully that her daughter had, “No education, no job, and no place to live,” and should not continue with the pregnancy. The aunt repeatedly asked about the possibility of intellectual disability affecting the child.
Amniocentesis was recommended to exclude an associated chromosomal abnormality, but was declined. A further appointment was offered to review the diagnosis and answer any additional questions prior to a decision being made. That offer was not taken up.
Four days later, Ms. A rang to say that she had decided to continue with the pregnancy and would be returning for a follow-up scan in 6 weeks. The clinicians involved wondered if they should have been more directive, following Ms. A’s mother, in recommending termination.
Antenatal counseling
The antenatal diagnosis of fetal abnormalities is becoming increasingly accurate with advances in ultrasound imaging technology [20, 32]. The midtrimester ultrasound scan assesses gestational age, fetal growth, placental location, amniotic fluid volume, maternal pelvic anatomy, and fetal anatomy [2]. In Australia, routine midtrimester ultrasound is accepted. It is estimated that >95% of Victorian women undergo obstetric ultrasound [44]. Reasonably good resolution of the fetal heart may be obtained by 12 to 13 weeks’ gestation [35], but with increasing accuracy of diagnosis by 16 to 18 weeks [43]. While little can be done in most cases to alter the course of the abnormality, detailed counseling, describing the need for interventions and their likely postnatal outcomes, can be provided to help the patient and her partner reach an understanding of the abnormality [18]. Lesions range from a hemodynamically insignificant ventricular septal defect to that of a univentricular heart requiring multiple operations for survival. Such counseling, often done in a setting of great emotional distress [19], may provide the parents who are able to make a decision with the option of termination. In Victoria, in the Commonwealth of Australia, abortion was decriminalized in 2008. Termination of pregnancy may be performed at the request of a mother before 24 weeks’ gestation [23]. A request for termination later on in the pregnancy needs to be presented to a Hospital Pregnancy Termination Review Committee for their consideration and final decision. If the pregnancy is continued, then such counseling, in addition to helping the parents come to terms with the infant’s serious abnormality, allows for the planning of the rest of the pregnancy, together with advice as to where the infant would be best delivered so as to receive tertiary intensive care if needed [19]. Such care would be provided in an anticipatory manner and has been found to generally improve the outcomes of affected infants [4, 34].
The approach of non-directive counseling following the diagnosis of a complex cardiac abnormality, with the provision of detailed information in a concise and understandable manner, is generally expected as the accepted standard of care in most Australian centers [18] and elsewhere [1, 42]. In this approach, patients make an autonomous decision with respect to the course of their pregnancy, i.e., whether to terminate the pregnancy. Physicians are expected to make no attempt to influence decisions either way. Reasons cited in support of non-directiveness include that it enhances client autonomy [9], avoids association with the eugenic movement [28] or controversies relating to abortion, and facilitates transfer of information to the patient [5].
However, it may be asked whether clinicians should always follow that model or whether they should take a more active role and provide directive counseling as is the case in some other parts of the world, for example, in China [15]. We have previously suggested that unlike counseling done following the birth of an infant where every effort may be made to ensure survival and a good outcome, fetal counseling need highlight adverse outcomes as the parent(s) may have the option of termination [14, 16]. In the case of Ms. A, the clinicians stopped short of providing a recommendation for her, despite the requests of her mother. Yet, in retrospect, they wondered whether the patient would have benefited from such advice. Could directive counseling have a role following the diagnosis of severe fetal cardiac abnormalities?
Hypoplastic left heart syndrome
Hypoplastic left heart is considered by some to be the most severe form of congenital heart abnormality, and is not compatible with life without major surgical interventions in the newborn period. It is still associated with a significant mortality ranging from 10% to 40%. HLHS usually arises spontaneously, but in a small proportion it may evolve during the pregnancy. There may be an association with a chromosomal abnormality. The usual first-stage surgical approach involves a Norwood procedure whereby the proximal main pulmonary artery is connected to an augmented ascending aorta and aortic arch while the distal pulmonary arteries are supplied by a modified Blalock-Taussig shunt connecting the right subclavian artery to the right pulmonary artery through a Goretex tube [22], or alternatively inserting a non-valved conduit between the right ventricle and distal pulmonary artery trunk (Sano modification) [30].
After the initial operation, prolonged hospitalization and intensive care is often required over a period of 3 months before a second operation is undertaken, namely a modified Glen, connecting the superior vena cava to the right pulmonary artery [26]. Primary cardiac transplant in the newborn is not generally available in Melbourne. The Norwood procedure carries a local mortality of 15–35% depending on the details of the cardiac anatomy, while the bidirectional Glen has a local mortality of 1–2%. If all goes well, a third operation is carried out usually between the age of 3 and 5 years, inserting an extracardiac conduit between the inferior vena cava and the right pulmonary artery, which carries a mortality of 1–2% [26].
An increasing number of operated children are now reaching early adult life. Their exercise tolerance is reasonable but their long-term outlook depends on the function of the right ventricle [11]. If that begins to fail, as is not uncommon, then the only option is to consider a cardiac transplant with all its attendant problems [6].
In the light of the significant risk of mortality and morbidity, and the burden of treatment for the infants, some consider palliative (non-operative) perinatal care as a legitimate management option [10].
Arguments in favor of directive counseling
There are several general arguments against strict neutrality and non-directiveness in antenatal counseling. The first of these is that in most other circumstances in medicine counseling is directive, and this is not thought to be inappropriate. Patients expect and seek advice from their physician for both minor and major health issues. Why should this be any different [3, 5]? Second, when they are receiving antenatal counseling, patients appear to often want to know what the counselor’s view is about alternative courses of action. Why refuse to provide advice that the patient is seeking? [3] Third, some question whether non-directive counseling is, in fact, achievable in practice [31, 40]. The way that information is presented, the choice of information, and the tone in which it is given all potentially reflect the values of the counselor. Empirical studies, however, suggest that implicit (and sometimes explicit) guidance is the exception rather than the rule [21].
There were also several specific factors in this case that led the clinicians to wonder whether directive counseling might have been justified. First, the risk of death is significant for infants with a hypoplastic left heart even in the best hands, and the burdens of treatment are substantial. Some infants, despite surviving the initial operation, die after weeks or months of intensive care. These infants undergo a large number of highly invasive and painful procedures. While the risk of a major cerebral insult is small, there is mounting evidence to suggest that because of the nature of the abnormality, the growing fetal brain will be subjected to slightly lower oxygen saturations that may contribute to specific learning disabilities in the young child [29]. A proportion of survivors have major developmental disabilities [29, 37]. Children face yet more surgery if they are to survive into adulthood. A further consideration is the potential harm to the family from the offspring’s repeated hospitalizations, surgery, etc., a factor many consider as a good enough reason to terminate. There is the burden of major dislocation for those families who decide to continue with the pregnancy and require surgical treatment in a capital city far from their home. Finally, a further concern is the potential cost to the community in general, in this case conservatively estimated at a quarter million dollars for the first 3 months paid by the tax payers [33]. That cost was a factor that contributed to two of the Australian centers that had previously carried out surgery for HLHS suspending their programs, with Sydney restarting only recently.
Arguments against directive counseling
There were three specific arguments in favor of more directive counseling for this mother. On closer scrutiny, however, there are problems with each of these.
Harm to the fetus/infant
Is it a harm for a fetus to have a pregnancy continued? There are some very severe conditions where infants benefit little or not at all from a very brief life, and may suffer significantly, perhaps, for example, the most severe forms of epidermolysis bullosa or osteogenesis imperfecta. In such circumstances, it would potentially be better for the fetus not to have the pregnancy continue, and it would be arguably appropriate for physicians to counsel in favor of termination. However, even for conditions that are often described as perinatally lethal, such as trisomy 18, some question whether fetuses are actually harmed by surviving to be born [38]. What about HLHS? Some infants die in the newborn period. However, a larger number survive early surgery (albeit at times after prolonged hospitalization) and are discharged home. The majority of school-age children surviving surgery for HLHS have IQs in the normal range, and their overall health is rated by parents as good [12]. Generally, the quality of life even for severe lesions such as a HLHS following a palliative Fontan procedure is generally good, even if somewhat less than the general population [31, 36]. Further medical advances over the years may allow the survivors an even better long-term survival. A recommendation to terminate for the sake of the fetus himself or herself would be hard to sustain in HLHS.
Harm to the mother
What about the mother? There are a range of potential harms to a mother from continuing a pregnancy. In some situations, there are medical risks, for example, where she has a serious or life-threatening condition that may be complicated by continuing a pregnancy such as pulmonary hypertension. It would be arguably reasonable for counseling to be directive where continuing a pregnancy imposes a risk of maternal death or other serious harm. In other circumstances, there are personal risks to a mother, for example, risks to employment, her finances, or personal relationships. In addition, there are increased risks of physical and psychological illness among parents of children with serious illness or impairment, and higher rates of separation [25, 27]. Even in countries with well-funded public health systems, there are considerable direct and indirect financial costs to the caregivers [8]. There is also concern of the effect of caring for a potentially disabled child on the mother, her partner, and the other siblings [7, 17].
For most cases of prenatally diagnosed HLHS, however, there are no significant physical or medical risks to the mother. Thus, the justification for a recommendation would have to be personal risks to the individual parent. These are likely to underlie the recommendations of Ms. A’s mother that she undergo a termination. However, there are several problems with this reasoning for the attending clinician. It is difficult for doctors to predict how the birth of a child will affect a mother. The personal and social consequences for family members are not necessarily correlated with the severity of the underlying illness. While counselors appear to be often more directive for patients from a lower socio-economic background than for those who are more well-to-do [21], doctors do not have particular expertise in predicting the social consequences of caregiving. We might also worry that allowing doctors to counsel on the basis of predicted personal risk would lead to directiveness in a much broader range of cases, for example, teenage mothers, or those who are unemployed, or socially disadvantaged. Advice of this nature might be particularly sensitive to bias and stereotyping.
Harm to others
Finally, there is the question of costs for society if a mother continues her pregnancy. These include acute and long-term medical costs [33], as well as the costs of assisted education and social support across a lifetime. Prenatal testing is a way of reducing these costs. From the point of view of society, it may be preferable if a mother was to terminate a pregnancy and (assuming she is able to) conceive another child with a lower chance of substantial health and long-term care costs [39].
However, treatment for HLHS, at least in a “wealthy” country such as Australia, is arguably cost-effective. Although early treatment is intensive and expensive, these costs are similar to those of treatments funded for life-threatening conditions in industrialized countries, including solid-organ transplantation [41]. If aggressive treatment for HLHS was not available or affordable, it would potentially be preferable for parents to terminate their pregnancy rather than continuing to term, and it may be justifiable for doctors to advise this following an antenatal diagnosis, as is the norm in some parts of the world [15].
Finally, there is a more general worry about including future care costs as the basis for directiveness in antenatal counseling, as this appears to veer much closer to a form of eugenics, where the benefits or costs to others inform or constrain parents’ choices about childbearing. Furthermore, the avoidance of future care costs might appear to justify directiveness in a very broad range of antenatal diagnoses – not limited to severe abnormalities such as a HLHS.
Conclusions
Where antenatal diagnosis is available, many parents choose to terminate pregnancies after the diagnosis of serious abnormalities, especially if associated with a chromosomal abnormality [13]. However, some parents decide to continue their pregnancies after medical counseling. Doctors may be tempted to be directive, and to advise their patients that they should terminate. In this report, we have reviewed reasons that might motivate such directiveness – on the basis of harm to the fetus, to the mother, or to society. These yield potential exceptions to the norm of neutrality and non-directiveness in antenatal counseling (Table 1), although they would apply rarely, and it is questionable if they include the most severe forms of congenital heart disease. Where these conditions apply, it could be ethical to provide directive advice, although it would also be important to ensure that mothers are neither coerced nor pressured to terminate their pregnancy. There are cogent arguments to remain non-directive in most circumstances following prenatal diagnosis.
1. | Harm to the fetus. Conditions causing severe and treatment-refractory pain in the fetus and/or newborn and that are highly likely to lead to early death despite treatment (e.g., severe epidermolysis bullosa). |
2. | Harm to the mother. Conditions where continuing pregnancy poses a substantial risk to the mother’s life or health (e.g., severe maternal pulmonary hypertension). |
3. | Costs. Conditions where provision of life-sustaining treatment after birth is not cost-effective, and/or is unable to be provided. Without this treatment, the newborn is likely to die. |
Addendum
Ms. A continued with her pregnancy and was confined at a tertiary center and delivered normally at term. The diagnosis of a hypoplastic left heart was confirmed, the infant was commenced on prostaglandin E1 and transferred to the surgical center. On arrival at 4 h of age, the infant was pale and acidotic with a high lactate level. Further investigation revealed a bowel perforation from an infarct or as a result of necrotizing enterocolitis. Treatment was withdrawn, and the infant died soon afterward.
References
[1] Anderson G. Nondirectiveness in prenatal genetics: parents read between the lines. Nurs Ethics. 1999;6:126–36.10.1177/096973309900600205Search in Google Scholar PubMed
[2] Australasian Society for Ultrasound in Medicine. The 18–20 week obstetrical scan, http://www.asum.org.au.Search in Google Scholar
[3] Bernhardt BA. Empirical evidence that genetic counselling is directive: where do we go from here? Am J Hum Genet. 1997;60:17–20.Search in Google Scholar
[4] Bonnet D, Coltri A, Butera G, Fermont L, Le Bidois J, Kachaner J, et al. Detection of transposition of the great arteries in fetuses reduces neonatal morbidity and mortality. Circulation. 1999;99:916–8.10.1161/01.CIR.99.7.916Search in Google Scholar
[5] Caplan AL. Neutrality is not morality: the ethics of genetic counseling. In: Bartels DM, LeRoy BS, Caplan AL, editors. Prescribing our future: ethical challenges in genetic counseling. Hawthorne, NY: Aldine De Gruyter; 1993. p. 149–65.10.4324/9781351328609-16Search in Google Scholar
[6] Chrisant MR, Naftel DC, Drummon-Webb J, Chinnock R, Canter CE, et al. Fate of infants with hypoplastic left heart syndrome listed for cardiac transplantation: a multicentre study. J Heart Lung Transplant. 2005;24:576–82.10.1016/j.healun.2004.01.019Search in Google Scholar PubMed
[7] Cummins R. The subjective well-being of people caring for a family member with a severe disability at home: a review. J Intellect Dev Dis. 2001;26:83–100.10.1080/13668250020032787Search in Google Scholar
[8] Curran AL, Sharples PM, White C, Knapp M. Time costs of caring for children with severe disabilities compared with caring for children without disabilities. Dev Med Child Neurol. 2001;43:529–33.10.1017/S0012162201000962Search in Google Scholar PubMed
[9] Elwyn G, Gray J, Clarke A. Shared decision making and non-directiveness in genetic counselling. J Med Genet. 2000;37:135–8.10.1136/jmg.37.2.135Search in Google Scholar PubMed PubMed Central
[10] Kon AA. Healthcare providers must offer palliative treatment to parents of neonates with hypoplastic left heart syndrome. Arch Pediatr Adolesc Med. 2008;162:844–8.10.1001/archpediatrics.2008.3Search in Google Scholar PubMed
[11] Kotani Y, Kasahara S, Fujii Y, Yoshizumi K, Oshima Y, Otsuki S, et al. Clinical outcome of the Fontan operation in patients with impaired ventricular function. Eur J Cardiothorac Surg. 2009;36:683–7.10.1016/j.ejcts.2009.04.042Search in Google Scholar PubMed
[12] Mahle WT, Clancy RR, Moss EM, Gerdes M, Jobes DR, Wenovsky G. Neurodevelopmental outcome and lifestyle assessment in school-aged and adolescent children with hypoplastic left heart syndrome. Pediatrics. 2000;105:1082–9.10.1542/peds.105.5.1082Search in Google Scholar PubMed
[13] Malhotra A, Menahem S, Gillam L. Ethical issues in fetal management: a cardiac perspective. Int J Pediatr. 2010;2010:857460.10.1155/2010/857460Search in Google Scholar
[14] Malhotra A, Menahem S, Shekleton P, Gillam L. Medical and ethical considerations in twin pregnancies discordant for serious cardiac disease. J Perinat. 2009;29:662–7.10.1038/jp.2009.88Search in Google Scholar
[15] Mao X, Wertz DC. China’s genetic services providers’ attitudes towards several ethical issues: a cross-cultural survey. Clin Genet. 1997;52:100–9.10.1111/j.1399-0004.1997.tb02526.xSearch in Google Scholar
[16] Menahem S, Gillam L. Fetal diagnosis – obligations of the clinician: case studies in the prenatal diagnosis of a major heart abnormality. Fetal Diagn Ther. 2007;3:233–7.10.1159/000098725Search in Google Scholar
[17] Menahem S, Grimwade J. Pregnancy termination following prenatal diagnosis of serious heart disease in the fetus. Early Hum Dev. 2003;73:71–8.10.1016/S0378-3782(03)00078-1Search in Google Scholar
[18] Menahem S, Grimwade J. Counselling strategies in the prenatal diagnosis of major heart abnormalities. Heart Lung Circulat. 2004;13:261–5.10.1016/j.hlc.2004.06.009Search in Google Scholar
[19] Menahem S, Grimwade J. Prenatal counseling – helping couples make decisions following the diagnosis of severe heart disease. Early Hum Dev. 2005;81:601–7.10.1016/j.earlhumdev.2005.02.001Search in Google Scholar
[20] Meyer-Wittkopf M, Schonfeld B, Cooper S, Sholler G. Correlation between fetal cardiac diagnosis by obstetric and pediatric cardiologist sonographers and comparison with postnatal findings. Ultrasound Obstet Gynecol. 2001;17:392–7.10.1046/j.1469-0705.2001.00381.xSearch in Google Scholar
[21] Michie S, Bron F, Bobrow M, Marteau TM. Nondirectiveness in genetic counseling: an empirical study. Am J Hum Genet. 1997;60:40–7.10.1097/00006254-199706000-00010Search in Google Scholar
[22] Norwood WI Jr. Hypoplastic left heart syndrome. Ann Thorac Surg. 1991;52:688–95.10.1016/0003-4975(91)90978-YSearch in Google Scholar
[23] Paterson KA. Early medical abortion: legal and medical developments in Australia. Med J Aust. 2010;193:26–9.10.5694/j.1326-5377.2010.tb03736.xSearch in Google Scholar
[24] Pike NA, Evangelista LS, Doering LV, Koniak-Griffin D, Lewis AB, Child JS. Health-related quality of life: a closer look at related research in patients who have undergone the Fontan operation over the last decade. Heart Lung. 2007;36:3–15.10.1016/j.hrtlng.2006.06.002Search in Google Scholar
[25] Raina P, O’Donnell M, Rosenbaum P, Brehaut J, Walter SD, Russell D, et al. The health and well-being of caregivers of children with cerebral palsy. Pediatrics. 2005;115:626–36.10.1542/peds.2004-1689Search in Google Scholar
[26] Rao PS, Striepe V, Merrill WH. Hypoplastic left heart syndrome. In: Kambam J, editor. Cardiac anesthesia for infants and children. St. Louis, MO: Mosby-Year Book, 1994:296–309.Search in Google Scholar
[27] Reichman NE, Corman H, Noonan K. Effects of child health on parents’ relationship status. Demography. 2004;41: 569–84.10.1353/dem.2004.0026Search in Google Scholar
[28] Resta RG. Eugenics and nondirectiveness in genetic counseling. J Genet Couns. 1997;6:255–8.10.1023/A:1025624505382Search in Google Scholar
[29] Rogers BT, Msall ME, Buck GM, Lyon NR, Norris MK, Roland JM, et al. Neurodevelopmental outcome of infants with hypoplastic left heart syndrome. J Pediatr. 1995;126:496–8.10.1016/S0022-3476(95)70478-7Search in Google Scholar
[30] Sano S, Huang SL, Kasahare S, Yoshizumi K, Kotani Y, Ishino K. Risk factors for mortality for the Norwood procedure using right ventricle to pulmonary artery shunt. Ann Thorac Surg. 2009;87:178–85.10.1016/j.athoracsur.2008.08.027Search in Google Scholar
[31] Shinebourne E. Termination, consent and innovation: ethical and legal aspects of paediatric cardiology. Cardiol Young. 1998;8:428–36.10.1017/S104795110000706XSearch in Google Scholar
[32] Stumpflen I, Stumpflen A, Wimmer M, Bernaschek G. Effect of detailed echocardiography as part of the routine prenatal ultrasonographic screening on detection of congenital heart disease. Lancet. 1996;348:854–7.10.1016/S0140-6736(96)04069-XSearch in Google Scholar
[33] Tibballs J, Kawahira T, Carter BG, Donath S, Brizard C, Wilkinson J. Outcomes of surgical treatment of infants with hypoplastic left heart syndrome: an institutional experience 1983–2004. J Paediatr Child Health. 2007;43:746–51.10.1111/j.1440-1754.2007.01164.xSearch in Google Scholar PubMed
[34] Tworetzky W, McElhinney DB, Reddy VM, Brook MM, Hanley FL, Silverman NH. Improved surgical outcome after fetal diagnosis of hypoplastic left heart syndrome. Circulation. 2001;103: 1269–73.10.1161/01.CIR.103.9.1269Search in Google Scholar
[35] Weiner Z, Lorber A, Shalev E. Diagnosis of congenital cardiac defects between 11 and 14 weeks’ gestation in high-risk patients. J Ultrasound Med. 2002;21:23–9.10.7863/jum.2002.21.1.23Search in Google Scholar
[36] Welch KK, Brown SA. The role of genetic counseling in the management of prenatally detected congenital heart defects. Semin Perinat. 2000;24:373–9.10.1053/sper.2000.16547Search in Google Scholar
[37] Wernovsky G. Current insights regarding neurological and developmental abnormalities in children and young adults with complex congenital heart disease. Cardiol Young. 2006;16:92–104.10.1017/S1047951105002398Search in Google Scholar
[38] Wilkinson D. Antenatal diagnosis of trisomy 18, harm and parental choice. J Med Ethics. 2010;36:644–5.10.1136/jme.2010.040212Search in Google Scholar
[39] Wilkinson D. Should we replace disabled newborn infants? J Moral Philos. 2011;8:390–414.10.1163/174552411X591348Search in Google Scholar
[40] Williams C, Alderson P, Farsides B. Is nondirectiveness possible within the context of antenatal screening and testing? Soc Sci Med. 2002;54:339–47.10.1016/S0277-9536(01)00032-6Search in Google Scholar
[41] Williams DL, Gelijns AC, Moskowitz AJ, Weinberg AD, Ng JH, Crawford E, et al. Hypoplastic left heart syndrome: valuing the survival. J Thorac Cardiovasc Surg. 2000;119:720–31.10.1016/S0022-5223(00)70007-9Search in Google Scholar
[42] WMA Statement on Genetics and Medicine 2009. http://www.wma.net/en/30publications/10policies/g11/.Search in Google Scholar
[43] Yagel S, Achiron R, Ron M, Revel A, Antehy E. Transvaginal ultrasonography at early pregnancy cannot be used alone for targeted organ ultrasonographic examination in a high-risk population. Am J Obstet Gynecol. 1995;172:971–5.10.1016/0002-9378(95)90029-2Search in Google Scholar
[44] Yates JM, Lumley J, Bell RJ. The prevalence and timing of obstetric ultrasound in Victoria 1991–1992: a population-based study. Aust NZ J Obstet Gynaecol. 1995;35:375–9.10.1111/j.1479-828X.1995.tb02145.xSearch in Google Scholar PubMed
-
The authors stated that there are no conflicts of interest regarding the publication of this article.
©2012 by Walter de Gruyter Berlin Boston