A C TA Obstetricia et Gynecologica
AOGS M A I N R E SE A RC H A R TI C LE
Fetal ultrasound examination and assessment of genetic soft markers in Sweden: are ethical principles respected? AFSANEH HAYAT ROSHANAI1,*, CHARLOTTA INGVOLDSTAD1,2,* & PETER LINDGREN2 1
Department of Public Health and Caring Sciences, Uppsala University, Uppsala, and 2Department of Clinical Science, Intervention and Technology, Division of Obstetrics and Gynecology, Karolinska University Hospital, Karolinska Institute, Stockholm, Sweden
Key words Ethical principles, fetal ultrasound examination, genetic ultrasound markers, soft markers, second trimester, antenatal care, diagnosis
Abstract
Please cite this article as: Hayat Roshanai A, Ingvoldstad C, Lindgren P. Fetal ultrasound examination and assessment of genetic soft markers in Sweden: are ethical principles respected? Acta Obstet Gynecol Scand 2015; 94: 141–147.
Objective. To explore procedures for providing information, assessment and documentation about ultrasound soft markers in Sweden. Design. Descriptive, quantitative, cross-sectional survey. Sample. Eighty-two percent of all obstetric ultrasound clinics in Sweden (covering >90% of routine fetal ultrasound examinations). Methods. Postal questionnaire survey between December 2010 and January 2011. Main outcome measures. Items about provision of information, risk estimation, and follow-up strategies in relation to observed ultrasound soft markers. Results. More than 96% of all fetal routine ultrasound examinations were performed at 15–21 gestational weeks, primarily by midwives. Half of the clinics replying wanted prospective parents to be provided with information, but 38 (78%) of the clinics did not routinely inform about assessment of soft markers before the examination. Follow up and decisions on whether to give information when soft markers were found were based on the number and type of the observed markers, whether other structural deviations existed, and on the woman’s age and anxiety level. Only at eight clinics (17%) were parents informed about all soft marker findings. At 13 clinics (28%) observed markers were documented/recorded, even though the women were not informed. Conclusions. Information regarding the assessment and importance of observed soft markers seems to be inconsistent and insufficient. Provision of information and documentation of findings appear to be handled differently at obstetric ultrasound clinics. This suggests that Swedish ethical principles relating to healthcare and ultrasound examinations are incompletely followed and national guidelines appear to be necessary.
Received: 11 May 2014 Accepted: 2 December 2014
Abbreviations:
Correspondence Charlotta Ingvoldstad, Center for Fetal Medicine, Department of Obstetrics and Gynecology, Karolinska University Hospital, 14186, Stockholm, Sweden. E-mails: [email protected], charlotta. [email protected] *These authors contributed equally to the manuscript. Conflicts of interest The authors have stated explicitly that there are no conflicts of interest in connection with this article.
CUB, combined ultrasound and biochemical screening.
DOI: 10.1111/aogs.12554
Introduction Fetal ultrasound screening examinations are widely used in antenatal care all over the world (1–3). With improved technology ultrasound examinations have revealed more fetal details, and it is now possible to detect even minor structural anomalies (4). Some of these anomalies, called genetic ultrasound markers or soft markers, are small, nonspecific, and often transient structural changes that
Key Message The low but well-known association between fetal chromosomal abnormalities and certain genetic ultrasound markers challenges aspects of care and counseling when they are found. Caregivers in Sweden handle this very differently, which is not consistent with ethical principles regarding care on equal and adequate terms for the entire population.
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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are not pathological by themselves, but imply an increased risk for chromosomal abnormalities. Soft markers, when seen in isolation in an otherwise low-risk pregnancy, may be of negligible significance. Nevertheless, they appear to be more commonly found in fetuses with congenital anomalies, particularly in the case of trisomies 21 (Down syndrome), 13, and 18 (5–8). The risk for chromosomal abnormalities increases with the number of markers that are detected (9). In Sweden, all pregnant women are offered one routine ultrasound scan in the second trimester. The first-trimester screening with the combined ultrasound and biochemical (CUB) test is offered to approximately half of all pregnant women. This is because of different routines in the 21 counties of Sweden. The variations include screening offers for all women, screening dependent on age, and no screening at all (10,11). According to the autonomy principle regulated by the Swedish Health and Medical Services Act (1982:763), women should be provided with accurate information through nondirective counseling so they can give their voluntary and well-informed consent for prenatal diagnosis (12). The Genetic Integrity Act (SFS 2006:351) states that all women should be offered adequate information regarding prenatal screening. Providing appropriate information is of utmost importance because the results from the examination might lead to difficult decisions about additional diagnostic testing, or sometimes decisions about termination of the pregnancy. The ultrasound examination that is routinely offered should be of the same quality across the country to meet the ethical principles of beneficence and justice (4). There are no national recommendations in Sweden regarding the assessment of ultrasound soft markers or concerning the reporting of observed fetal genetic soft markers (13). The clinical procedures for dealing with the information obtained differ widely, both nationally and internationally (10). Hence, it is essential to ensure that the screening services are provided in an ethical and equitable way throughout the country and that prospective parents have access to information in a timely and appropriate manner. Our aim was to explore the manner in which soft markers are assessed and discussed in Sweden, and so provide a basis for national guidelines organized by the Swedish Society of Obstetrics and Gynecology.
Material and methods The study was a descriptive, cross-sectional survey using a quantitative approach, conducted between December 2010 and January 2011. A total of 60 obstetric ultrasound clinics, based in university hospitals, county hospitals and
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private practices, were approached. Some of the private clinics consisted of several units, so they were aggregated into one clinic because they used the same routines. Out of the 60 clinics that were approached, 49 (82%) consented to participate and filled out a questionnaire. The included clinics contribute to more than 90% of all routine mid-trimester fetal ultrasound scans in Sweden. The study questionnaire, together with the information letters, informed consent sheet, and prepaid envelopes, were mailed to the clinics. The respondents were either the midwives or the medical doctors. One reminder was sent to the nonresponders within a period of 2 months, by post, e-mail, or sometimes through personal contact by telephone. The study-specific questionnaire included 21 items with both predefined multiple choice alternatives and openended questions. The questions assessed the gestational age at which the examination was usually performed, assessment of the ultrasound markers, information provision, risk estimation, the documentation process of observed genetic markers, as well as the handling of potential findings on genetic markers when the women had undergone a CUB test and invasive prenatal testing earlier in the pregnancy. The questionnaire was pilot tested on 10 knowledgeable individuals in the field. According to the recommendation of the Board of Research Ethics in Uppsala University, this study did not need formal ethical approval. It was not possible to identify individuals from the information provided.
Data analysis All analyses were conducted using the SPSS statistical software version 21 (IBM Corp, Armonk, NY, USA). Descriptive statistics were computed and presented in running text and tables. When comparing groups of responders (midwives and doctors) independent t-test was used. A p-value of 1000 ultrasound examinations per year. Almost all of the examinations (96%) were performed at 15–21 weeks of gestation (Table 1), and primarily by the midwives. At one-third of the clinics (n = 16) the CUB test was offered to all women, at 31% (n = 15) it was offered only to women above the age of 35 years, and at one-third the CUB test was not offered at all (Table 1). The majority of the participating clinics (78%, n = 38) reported that they did not provide any information regarding the soft markers or their significance before the
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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Table 1. Performance of ultrasound examination. Variable
n
Practice type County hospital 33 Private clinic 11 University hospital 5 Performed ultrasound examinations per year/clinic 1–500 5 501–1000 8 1001–2000 17 >2000 15 Gestational week when ultrasound examination is performed 12–14 weeks 2 15–21 weeks 44 Other 3 Ultrasound examination is conducted by Midwives 31 Physician and midwives 16 Do you offer combined ultrasound and biochemical screening Yes to all women 16 Yes to all women above 35 years old 15 No 16
%
68 22 10 11 17 37 33 4 90 6 64 34 33 31 33
ultrasound examination. Twelve percent (n = 6) did inform prospective parents about assessment of soft markers before the ultrasound examination. One-third of the respondents (36%, n = 17) stated that they did not inform prospective parents about the observed soft markers if the mother was below the age of 35 years or when an observed marker was an isolated finding. At 34% of the clinics the mothers were informed regardless of their age, and a few clinics (17%, n = 8) highlighted that they provided women with information about all the findings. The physicians mostly provided information on the findings in association with the ultrasound examination (Table 2). Almost half of the staff wanted to inform prospective parents about the assessment of soft markers before the ultrasound examination and one-third would choose to discuss the importance of the markers. The majority also believed that prospective parents wanted to be informed before the screening (Table 3). Almost half of the clinics (48%, n = 22) stated that prospective parents were informed about elevated risk when soft markers were observed, but no risk estimate was provided. Only 6% (n = 3) both informed parents about an increased risk level and provided a risk estimate (Table 4). Further follow up was variably based on the number (63%) and type of observed markers (47%), followed by the level of new risk (31%), and the women’s age (26%). In addition, offering supplementary invasive prenatal diagnosis was frequently based on whether other structural deviations existed (61%) and/or when more than
one marker was observed (45%), followed by the level of the estimated risk, women’s age >35 years, and the anxiety level. For women who had undergone a CUB test earlier in the pregnancy, a new level of risk was usually estimated in a contingent strategy based on the soft markers’ known likelihood-ratios (Table 3). If invasive prenatal diagnosis was performed earlier in the pregnancy, 66% of the clinics offered a morphological examination by a fetal medicine specialist when certain markers were found, i.e. ventriculomegaly, echogenic bowel, choroid plexus cysts, and short femur length. Some clinics (n = 16) did not provide any information about the observed markers to women who had undergone invasive prenatal diagnosis earlier in pregnancy, and a few (n = 7) stated that they provided information if the findings did not have any clinical significance (Table 4). At 28% of the clinics (n = 13), the observed soft markers were recorded even though the women were not informed about them (Table 5). At 61% of the clinics (n = 28), the observed soft markers were recorded just in case the prospective mother would be informed about the sonographic findings. When documentation was generated, both pictures and text were used in 82% of the clinics. Image documentation was standard practice in 39% (n = 18) of the clinics (Table 5).
Discussion Information regarding soft markers was managed differently at different obstetric ultrasound clinics in Sweden. The majority of the clinics reported that they did not provide prospective parents with information regarding the assessment of genetic ultrasound markers and their importance before the examination. However, half of the staff wanted to inform prospective parents, and many of them believed that prospective parents wished to be informed about both the soft marker assessment and its importance before the fetal routine examination. When the soft markers were observed, the prospective parents were mostly informed of an elevated risk for fetal chromosomal abnormalities, but generally no risk estimation was provided. Only a few clinics informed women about every finding, regardless of the type, number of markers, and age of the pregnant woman. However, at most clinics, these variables were decisive for the decision to inform the women. Findings were documented even though the women were not informed. The screening for soft markers during a routine ultrasound examination may cause more harm than good for both the parents and the unborn child. For this reason, healthcare professionals should be cautious in using these
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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Table 2. Provision of information related to ultrasound examination. Variablea Information given regarding soft markers No information Information regarding assessment of ultrasound soft markers What soft markers are The significance of observed soft markers When women are usually informed about the significance of the findings? The same day at routine ultrasound examination At the appointment a few days after the examination By phone after ultrasound examination Other ways How is pre-information regarding assessment of soft markers provided? In writing Orally Individually In group Other way (e.g. via home page) Are there occasions when you choose not to inform prospective parents regarding observed soft markers? Isolated soft markers are observed under the age of 35 years Isolated soft markers are observed regardless of age If the women have undergone invasive diagnosis Information is provided regarding all findings If the women have undergone combined ultrasound and biochemical screening Yes, all soft markers are considered as normal findings regardless of age
nb
%
38 6 4 2
78 12 8 4
39 19 0 5
80 39 0 10
9 8 7 2 2
18 16 14 4 4
17 16 9 8 7 5
36 34 18 17 14 11
a
Multiple choice answers. Data not available for all participants.
b
Table 3. The staff opinions about pre-examination information. Yes Items
n
No %
n
%
p value
I would like to inform prospective parents about assessment of soft markers in ultrasound before the examination Midwives 24 54 20 46 0.597 Physicians 18 49 19 51 I would like to inform prospective parents about the importance of observed soft markers in ultrasound before the examination Midwives 18 41 26 59 0.191 Physicians 10 27 27 73 I believe that prospective parents wish to be informed about assessment of soft markers in ultrasound before the examination Midwives 28 64 16 36 0.382 Physicians 20 54 17 46 I believe that parents would like to be informed about the importance of any findings of soft markers in ultrasound before the examination Midwives 26 59 18 22 0.096 Physicians 15 40 22 60
markers as a screening method for identifying chromosomal abnormalities (14). In accordance with the principle of autonomy, one of the four ethical principles of Swedish legislation of health care, a medical examination such as an ultrasound screening should not be performed without the patient’s consent. However, a decision cannot be considered as being informed if the patient does not receive sufficient information on both
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the positive and negative consequences of their choice regarding prenatal diagnosis (12,15). At the same time, how to inform and advise prospective parents about the discovery of a genetic marker has become a common dilemma, given that the significance of the genetic ultrasound markers is still uncertain (7,16). According to the Genetic Integrity Act (SFS 2006:351), all findings from a prenatal examination that influence fetal health should be
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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Table 4. Risk estimation and follow up. Variable
n
Do you provide any risk estimation when soft markers are observed? State elevated risk, but not the level of increase 22 No 14 Yes, state increased risk (49) 1 Yes, state the level of the risk (1/250) 4 Yes, state both the increased risk and the estimation 3 Just risks above a certain level 2 According to which model is the risk estimation conducted?a No answer 31 Likelihood ratio according to Fetal Medicine Foundation 8 Likelihood ratio according to SBU report 2006 3 Separate estimation model 3 Other 4 Risk estimation for women who have undergone CUB test earlier in the pregnancy Estimation of risk level in association with observed genetic ultrasound markers No new risk is estimated, the CUB-risk would be applied 21 New risk estimation related to CUB-risk 11 New risk estimation related to the age 1 Other 6 What is the further follow-up based on?b The number of the observed markers 31 The type of the observed marker 23 The level of the new risk 15 Woman’s age 13 In which cases do you offer invasive prenatal diagnosis when soft markers are observed? If other structural deviations exist 30 If more than one marker is observed 22 If an increased risk is estimated 13 If the women is older than 35 years of age 12 If there is any indication of worry (all women) 12 Follow up of women who have undergone invasive prenatal diagnosis (chromosome analysis) earlier in the pregnancyb Morphological examination by physician if certain markers are observed 29 Do not inform about the findings 16 Provide information as if the finding does not have any significance 7
%
48 30 2 9 6 4 64 16 6 6 8
54 28 3 15 63 47 31 26 61 45 26 24 24 66 36 16
CUB, combined ultrasound and biochemical screening; SBU, Swedish Council on Health Technology. a Note that about 60% of participants did not provide any answer. b Multiple choice answers.
given to the woman. However, if the information is not related to this, it should only be revealed at the woman’s request. As the significance of the markers is not absolute, and as its relation to the health of the fetus is not completely known, it is not certain that it is covered by the Genetic Integrity Act (SFS 2006:351). The ethical dilemmas associated with assessment of ultrasound markers, which healthcare professionals can encounter, have also been discussed in previous studies (17,18). This study indicates that Swedish law and ethical rules are not being followed completely. First, the pre-examination information regarding the assessment and the importance of observed soft markers seems to be insufficient. Second, the quality of the antenatal care offered is unequal in this respect across the country. Third, the pro-
vision of information and the documentation of findings are handled differently at different obstetric ultrasound clinics. This is probably also the case in other countries. It is noteworthy that the majority of clinics did not offer any information, despite their staff wanting to do so. In line with previous study findings indicating that midwives and doctors do not want patients to worry and therefore avoid talking about risks (19), a feasible interpretation could be that healthcare personnel do not want to make patients anxious and expose them to unnecessary invasive tests (18). Midwives may also perceive the provision of information about fetal diagnosis as difficult, both from an ethical and a practical point of view (20). The results of another study (21) indicated that only a minority of midwives felt comfortable with providing advice regard-
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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Table 5. Documentation of the sonographic findings. Variable
References n
Do you keep records on observed soft markers? Only in case the women are informed about the markers 28 Even when women are not informed about the markers 13 No, we do not keep record on any markers 5 How is the documentation of observed soft markers conducted? As picture and text 37 As text (through medical record or reports) 4 As digital images 3 As paper images 1 Is routine photo documentation common at your work? Only when deviations are detected or in special cases 19 Yes, keep photo/clip from standard projections 18 Yes, tape record the entire examination 0 No, no photo documentation 10
%
61 28 11 82 9 7 2 40 39 0 21
ing available genetic tests, communicating risk estimates when soft markers were observed in a fetus, or providing support in dealing with the results of a genetic test. At the same time, prospective parents do not think that they receive enough information from the midwives during the ultrasound examination (22). One of the strengths of this study was that all ultrasound clinics in Sweden were contacted, providing a broad coverage on information regarding how soft markers are managed in Sweden. Of the few clinics that did not respond, most were small with a limited number of patients. A limitation of the study was that our questionnaire had not been used or evaluated in other studies because it was developed by our research group specifically for this study and for a predefined population and was distributed by the supervising staff of the clinic to the responders. It is therefore possible that the respondents might have had different responsibilities and experience at the clinics, compared with other personnel. National guidelines regarding the information provided to parents pre-examination as well as the information and documentation about actual findings could help healthcare professionals to handle this difficult information and ethical dilemma. That would allow consistent information to be presented to parents regardless of where one lives or from whom information is received, thereby improving the premises for informed choice. Such national guidelines and consensus would have been valuable when introducing first-trimester CUB (17) and will be of great importance when new methods, such as non-invasive prenatal testing, are introduced.
Funding No funding was obtained for this study.
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1. Ekelin M, Crang-Svalenius E. Midwives’ attitudes to and knowledge about a newly introduced foetal screening method. Scand J Caring Sci. 2004;18:287–93. 2. Garcia J, Bricker L, Henderson J, Martin MA, Mugford M, Nielson J, et al. Women’s views of pregnancy ultrasound: a systematic review. Birth. 2002;29:225–50. 3. Salomon LJ, Alfirevic Z, Berghella V, Bilardo C, Hernadez-Andrade E, Johnsen SL, et al. Practice guidelines for performance of the routine mid-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol. 2011;37:116– 26. 4. Cargill Y, Morin L, Bly S, Butt K, Denis N, Gagnon R, et al. Content of a complete routine second trimester obstetrical ultrasound examination and report. J Obstet Gynaecol Can. 2009;31:272–5, 6–80. 5. Smith-Bindman R, Hosmer W, Feldstein VA, Deeks JJ, Goldberg JD. Second-trimester ultrasound to detect fetuses with Down syndrome: a meta-analysis. JAMA. 2001;285:1044–55. 6. Nyberg DA, Souter VL, El-Bastawissi A, Young S, Luthhardt F, Luthy DA. Isolated sonographic markers for detection of fetal Down syndrome in the second trimester of pregnancy. J Ultrasound Med. 2001;20:1053– 63. 7. Agathokleous M, Chaveeva P, Poon LC, Kosinski P, Nicolaides KH. Meta-analysis of second-trimester markers for trisomy 21. Ultrasound Obstet Gynecol. 2013;41:247– 61. 8. Bethune M. Literature review and suggested protocol for managing ultrasound soft markers for Down syndrome: thickened nuchal fold, echogenic bowel, shortened femur, shortened humerus, pyelectasis and absent or hypoplastic nasal bone. Australas Radiol. 2007;51:218– 25. 9. Methods of Early Prenantal Diagnosis. Statens Beredning f€ or Medicinsk Utv€ardering (SBU) [Swedish Coucil on Health Technology]. Assessment. 2006. Available online at: http://www.sbu.se/en/Published/Yellow/Methods-ofEarly-Prenatal-Diagnosis/ (accessed 10 February 2014). 10. Ahman A, Runestam K, Sarkadi A. Did I really want to know this? Pregnant women’s reaction to detection of a soft marker during ultrasound screening. Patient Educ Couns. 2010;81:87–93. 11. SOC. Fosterskador och kromosomavvikelser. Stockholm: Sveriges Officiella Statistik, 2012. 12. Ferm Widlund K, Gunnarsson C, Nordin K, Hansson MG. Pregnant women are satisfied with the information they receive about prenatal diagnosis, but are their decisions well informed? Acta Obstet Gynecol Scand. 2009;88:1128– 32. 13. Larsson AK, Crang-Svalenius E, Dykes AK. Information for better or for worse: interviews with parents when their foetus was found to have choroid plexus cysts at a routine
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14.
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second trimester ultrasound. J Psychosom Obstet Gynaecol. 2009;30:48–57. Getz L, Kirkengen AL. Ultrasound screening in pregnancy: advancing technology, soft markers for fetal chromosomal aberrations, and unacknowledged ethical dilemmas. Soc Sci Med. 2003;56:2045–57. Green JM, Hewison J, Bekker HL, Bryant LD, Cuckle HS. Psychosocial aspects of genetic screening of pregnant women and newborns: a systematic review. Health Technol Assess. 2004;8:iii, ix–x, 1–109. Watson MS, Hall S, Langford K, Marteau TM. Psychological impact of the detection of soft markers on routine ultrasound scanning: a pilot study investigating the modifying role of information. Prenat Diagn. 2002;22:569– 75. € Ingvoldstad C, Georgsson Ohman S, Lindgren P. Implementation of combined ultrasound and biochemistry for risk evaluation of chromosomal abnormalities during the first trimester in Sweden. Acta Obstet Gynecol Scand. 2014;93:868–73. Ahman A, Axelsson O, Maras G, Rubertsson C, Sarkadi A, Lindgren P. Ultrasonographic fetal soft markers in a
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low-risk population: prevalence, association with trisomies and invasive tests. Acta Obstet Gynecol Scand. 2014;93:367–73. Asplin N, Wessel H, Marions L, Georgsson Ohman S. Pregnant women’s experiences, needs, and preferences regarding information about malformations detected by ultrasound scan. Sex Reprod Healthc. 2012;3:73–8. Ekelin M, Crang-Svalenius E, Dykes AK. A qualitative study of mothers’ and fathers’ experiences of routine ultrasound examination in Sweden. Midwifery. 2004;20:335–44. Benjamin CM, Anionwu EN, Kristoffersson U, ten Kate LP, Plass AM, Nippert I, et al. Educational priorities and current involvement in genetic practice: a survey of midwives in the Netherlands, UK and Sweden. Midwifery. 2009;25:483–99. Ahman A, Lindgren P, Sarkadi A. Facts first, then reaction – expectant fathers’ experiences of an ultrasound screening identifying soft markers. Midwifery. 2012;28:e667–75.
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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AOGS M A I N R E SE A RC H A R TI C LE
Fetal ultrasound examination and assessment of genetic soft markers in Sweden: are ethical principles respected? AFSANEH HAYAT ROSHANAI1,*, CHARLOTTA INGVOLDSTAD1,2,* & PETER LINDGREN2 1
Department of Public Health and Caring Sciences, Uppsala University, Uppsala, and 2Department of Clinical Science, Intervention and Technology, Division of Obstetrics and Gynecology, Karolinska University Hospital, Karolinska Institute, Stockholm, Sweden
Key words Ethical principles, fetal ultrasound examination, genetic ultrasound markers, soft markers, second trimester, antenatal care, diagnosis
Abstract
Please cite this article as: Hayat Roshanai A, Ingvoldstad C, Lindgren P. Fetal ultrasound examination and assessment of genetic soft markers in Sweden: are ethical principles respected? Acta Obstet Gynecol Scand 2015; 94: 141–147.
Objective. To explore procedures for providing information, assessment and documentation about ultrasound soft markers in Sweden. Design. Descriptive, quantitative, cross-sectional survey. Sample. Eighty-two percent of all obstetric ultrasound clinics in Sweden (covering >90% of routine fetal ultrasound examinations). Methods. Postal questionnaire survey between December 2010 and January 2011. Main outcome measures. Items about provision of information, risk estimation, and follow-up strategies in relation to observed ultrasound soft markers. Results. More than 96% of all fetal routine ultrasound examinations were performed at 15–21 gestational weeks, primarily by midwives. Half of the clinics replying wanted prospective parents to be provided with information, but 38 (78%) of the clinics did not routinely inform about assessment of soft markers before the examination. Follow up and decisions on whether to give information when soft markers were found were based on the number and type of the observed markers, whether other structural deviations existed, and on the woman’s age and anxiety level. Only at eight clinics (17%) were parents informed about all soft marker findings. At 13 clinics (28%) observed markers were documented/recorded, even though the women were not informed. Conclusions. Information regarding the assessment and importance of observed soft markers seems to be inconsistent and insufficient. Provision of information and documentation of findings appear to be handled differently at obstetric ultrasound clinics. This suggests that Swedish ethical principles relating to healthcare and ultrasound examinations are incompletely followed and national guidelines appear to be necessary.
Received: 11 May 2014 Accepted: 2 December 2014
Abbreviations:
Correspondence Charlotta Ingvoldstad, Center for Fetal Medicine, Department of Obstetrics and Gynecology, Karolinska University Hospital, 14186, Stockholm, Sweden. E-mails: [email protected], charlotta. [email protected] *These authors contributed equally to the manuscript. Conflicts of interest The authors have stated explicitly that there are no conflicts of interest in connection with this article.
CUB, combined ultrasound and biochemical screening.
DOI: 10.1111/aogs.12554
Introduction Fetal ultrasound screening examinations are widely used in antenatal care all over the world (1–3). With improved technology ultrasound examinations have revealed more fetal details, and it is now possible to detect even minor structural anomalies (4). Some of these anomalies, called genetic ultrasound markers or soft markers, are small, nonspecific, and often transient structural changes that
Key Message The low but well-known association between fetal chromosomal abnormalities and certain genetic ultrasound markers challenges aspects of care and counseling when they are found. Caregivers in Sweden handle this very differently, which is not consistent with ethical principles regarding care on equal and adequate terms for the entire population.
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
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are not pathological by themselves, but imply an increased risk for chromosomal abnormalities. Soft markers, when seen in isolation in an otherwise low-risk pregnancy, may be of negligible significance. Nevertheless, they appear to be more commonly found in fetuses with congenital anomalies, particularly in the case of trisomies 21 (Down syndrome), 13, and 18 (5–8). The risk for chromosomal abnormalities increases with the number of markers that are detected (9). In Sweden, all pregnant women are offered one routine ultrasound scan in the second trimester. The first-trimester screening with the combined ultrasound and biochemical (CUB) test is offered to approximately half of all pregnant women. This is because of different routines in the 21 counties of Sweden. The variations include screening offers for all women, screening dependent on age, and no screening at all (10,11). According to the autonomy principle regulated by the Swedish Health and Medical Services Act (1982:763), women should be provided with accurate information through nondirective counseling so they can give their voluntary and well-informed consent for prenatal diagnosis (12). The Genetic Integrity Act (SFS 2006:351) states that all women should be offered adequate information regarding prenatal screening. Providing appropriate information is of utmost importance because the results from the examination might lead to difficult decisions about additional diagnostic testing, or sometimes decisions about termination of the pregnancy. The ultrasound examination that is routinely offered should be of the same quality across the country to meet the ethical principles of beneficence and justice (4). There are no national recommendations in Sweden regarding the assessment of ultrasound soft markers or concerning the reporting of observed fetal genetic soft markers (13). The clinical procedures for dealing with the information obtained differ widely, both nationally and internationally (10). Hence, it is essential to ensure that the screening services are provided in an ethical and equitable way throughout the country and that prospective parents have access to information in a timely and appropriate manner. Our aim was to explore the manner in which soft markers are assessed and discussed in Sweden, and so provide a basis for national guidelines organized by the Swedish Society of Obstetrics and Gynecology.
Material and methods The study was a descriptive, cross-sectional survey using a quantitative approach, conducted between December 2010 and January 2011. A total of 60 obstetric ultrasound clinics, based in university hospitals, county hospitals and
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private practices, were approached. Some of the private clinics consisted of several units, so they were aggregated into one clinic because they used the same routines. Out of the 60 clinics that were approached, 49 (82%) consented to participate and filled out a questionnaire. The included clinics contribute to more than 90% of all routine mid-trimester fetal ultrasound scans in Sweden. The study questionnaire, together with the information letters, informed consent sheet, and prepaid envelopes, were mailed to the clinics. The respondents were either the midwives or the medical doctors. One reminder was sent to the nonresponders within a period of 2 months, by post, e-mail, or sometimes through personal contact by telephone. The study-specific questionnaire included 21 items with both predefined multiple choice alternatives and openended questions. The questions assessed the gestational age at which the examination was usually performed, assessment of the ultrasound markers, information provision, risk estimation, the documentation process of observed genetic markers, as well as the handling of potential findings on genetic markers when the women had undergone a CUB test and invasive prenatal testing earlier in the pregnancy. The questionnaire was pilot tested on 10 knowledgeable individuals in the field. According to the recommendation of the Board of Research Ethics in Uppsala University, this study did not need formal ethical approval. It was not possible to identify individuals from the information provided.
Data analysis All analyses were conducted using the SPSS statistical software version 21 (IBM Corp, Armonk, NY, USA). Descriptive statistics were computed and presented in running text and tables. When comparing groups of responders (midwives and doctors) independent t-test was used. A p-value of 1000 ultrasound examinations per year. Almost all of the examinations (96%) were performed at 15–21 weeks of gestation (Table 1), and primarily by the midwives. At one-third of the clinics (n = 16) the CUB test was offered to all women, at 31% (n = 15) it was offered only to women above the age of 35 years, and at one-third the CUB test was not offered at all (Table 1). The majority of the participating clinics (78%, n = 38) reported that they did not provide any information regarding the soft markers or their significance before the
ª 2014 Nordic Federation of Societies of Obstetrics and Gynecology, Acta Obstetricia et Gynecologica Scandinavica 94 (2015) 141–147
A. Hayat Roshanai et al.
Information regarding soft markers
Table 1. Performance of ultrasound examination. Variable
n
Practice type County hospital 33 Private clinic 11 University hospital 5 Performed ultrasound examinations per year/clinic 1–500 5 501–1000 8 1001–2000 17 >2000 15 Gestational week when ultrasound examination is performed 12–14 weeks 2 15–21 weeks 44 Other 3 Ultrasound examination is conducted by Midwives 31 Physician and midwives 16 Do you offer combined ultrasound and biochemical screening Yes to all women 16 Yes to all women above 35 years old 15 No 16
%
68 22 10 11 17 37 33 4 90 6 64 34 33 31 33
ultrasound examination. Twelve percent (n = 6) did inform prospective parents about assessment of soft markers before the ultrasound examination. One-third of the respondents (36%, n = 17) stated that they did not inform prospective parents about the observed soft markers if the mother was below the age of 35 years or when an observed marker was an isolated finding. At 34% of the clinics the mothers were informed regardless of their age, and a few clinics (17%, n = 8) highlighted that they provided women with information about all the findings. The physicians mostly provided information on the findings in association with the ultrasound examination (Table 2). Almost half of the staff wanted to inform prospective parents about the assessment of soft markers before the ultrasound examination and one-third would choose to discuss the importance of the markers. The majority also believed that prospective parents wanted to be informed before the screening (Table 3). Almost half of the clinics (48%, n = 22) stated that prospective parents were informed about elevated risk when soft markers were observed, but no risk estimate was provided. Only 6% (n = 3) both informed parents about an increased risk level and provided a risk estimate (Table 4). Further follow up was variably based on the number (63%) and type of observed markers (47%), followed by the level of new risk (31%), and the women’s age (26%). In addition, offering supplementary invasive prenatal diagnosis was frequently based on whether other structural deviations existed (61%) and/or when more than
one marker was observed (45%), followed by the level of the estimated risk, women’s age >35 years, and the anxiety level. For women who had undergone a CUB test earlier in the pregnancy, a new level of risk was usually estimated in a contingent strategy based on the soft markers’ known likelihood-ratios (Table 3). If invasive prenatal diagnosis was performed earlier in the pregnancy, 66% of the clinics offered a morphological examination by a fetal medicine specialist when certain markers were found, i.e. ventriculomegaly, echogenic bowel, choroid plexus cysts, and short femur length. Some clinics (n = 16) did not provide any information about the observed markers to women who had undergone invasive prenatal diagnosis earlier in pregnancy, and a few (n = 7) stated that they provided information if the findings did not have any clinical significance (Table 4). At 28% of the clinics (n = 13), the observed soft markers were recorded even though the women were not informed about them (Table 5). At 61% of the clinics (n = 28), the observed soft markers were recorded just in case the prospective mother would be informed about the sonographic findings. When documentation was generated, both pictures and text were used in 82% of the clinics. Image documentation was standard practice in 39% (n = 18) of the clinics (Table 5).
Discussion Information regarding soft markers was managed differently at different obstetric ultrasound clinics in Sweden. The majority of the clinics reported that they did not provide prospective parents with information regarding the assessment of genetic ultrasound markers and their importance before the examination. However, half of the staff wanted to inform prospective parents, and many of them believed that prospective parents wished to be informed about both the soft marker assessment and its importance before the fetal routine examination. When the soft markers were observed, the prospective parents were mostly informed of an elevated risk for fetal chromosomal abnormalities, but generally no risk estimation was provided. Only a few clinics informed women about every finding, regardless of the type, number of markers, and age of the pregnant woman. However, at most clinics, these variables were decisive for the decision to inform the women. Findings were documented even though the women were not informed. The screening for soft markers during a routine ultrasound examination may cause more harm than good for both the parents and the unborn child. For this reason, healthcare professionals should be cautious in using these
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Table 2. Provision of information related to ultrasound examination. Variablea Information given regarding soft markers No information Information regarding assessment of ultrasound soft markers What soft markers are The significance of observed soft markers When women are usually informed about the significance of the findings? The same day at routine ultrasound examination At the appointment a few days after the examination By phone after ultrasound examination Other ways How is pre-information regarding assessment of soft markers provided? In writing Orally Individually In group Other way (e.g. via home page) Are there occasions when you choose not to inform prospective parents regarding observed soft markers? Isolated soft markers are observed under the age of 35 years Isolated soft markers are observed regardless of age If the women have undergone invasive diagnosis Information is provided regarding all findings If the women have undergone combined ultrasound and biochemical screening Yes, all soft markers are considered as normal findings regardless of age
nb
%
38 6 4 2
78 12 8 4
39 19 0 5
80 39 0 10
9 8 7 2 2
18 16 14 4 4
17 16 9 8 7 5
36 34 18 17 14 11
a
Multiple choice answers. Data not available for all participants.
b
Table 3. The staff opinions about pre-examination information. Yes Items
n
No %
n
%
p value
I would like to inform prospective parents about assessment of soft markers in ultrasound before the examination Midwives 24 54 20 46 0.597 Physicians 18 49 19 51 I would like to inform prospective parents about the importance of observed soft markers in ultrasound before the examination Midwives 18 41 26 59 0.191 Physicians 10 27 27 73 I believe that prospective parents wish to be informed about assessment of soft markers in ultrasound before the examination Midwives 28 64 16 36 0.382 Physicians 20 54 17 46 I believe that parents would like to be informed about the importance of any findings of soft markers in ultrasound before the examination Midwives 26 59 18 22 0.096 Physicians 15 40 22 60
markers as a screening method for identifying chromosomal abnormalities (14). In accordance with the principle of autonomy, one of the four ethical principles of Swedish legislation of health care, a medical examination such as an ultrasound screening should not be performed without the patient’s consent. However, a decision cannot be considered as being informed if the patient does not receive sufficient information on both
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the positive and negative consequences of their choice regarding prenatal diagnosis (12,15). At the same time, how to inform and advise prospective parents about the discovery of a genetic marker has become a common dilemma, given that the significance of the genetic ultrasound markers is still uncertain (7,16). According to the Genetic Integrity Act (SFS 2006:351), all findings from a prenatal examination that influence fetal health should be
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Table 4. Risk estimation and follow up. Variable
n
Do you provide any risk estimation when soft markers are observed? State elevated risk, but not the level of increase 22 No 14 Yes, state increased risk (49) 1 Yes, state the level of the risk (1/250) 4 Yes, state both the increased risk and the estimation 3 Just risks above a certain level 2 According to which model is the risk estimation conducted?a No answer 31 Likelihood ratio according to Fetal Medicine Foundation 8 Likelihood ratio according to SBU report 2006 3 Separate estimation model 3 Other 4 Risk estimation for women who have undergone CUB test earlier in the pregnancy Estimation of risk level in association with observed genetic ultrasound markers No new risk is estimated, the CUB-risk would be applied 21 New risk estimation related to CUB-risk 11 New risk estimation related to the age 1 Other 6 What is the further follow-up based on?b The number of the observed markers 31 The type of the observed marker 23 The level of the new risk 15 Woman’s age 13 In which cases do you offer invasive prenatal diagnosis when soft markers are observed? If other structural deviations exist 30 If more than one marker is observed 22 If an increased risk is estimated 13 If the women is older than 35 years of age 12 If there is any indication of worry (all women) 12 Follow up of women who have undergone invasive prenatal diagnosis (chromosome analysis) earlier in the pregnancyb Morphological examination by physician if certain markers are observed 29 Do not inform about the findings 16 Provide information as if the finding does not have any significance 7
%
48 30 2 9 6 4 64 16 6 6 8
54 28 3 15 63 47 31 26 61 45 26 24 24 66 36 16
CUB, combined ultrasound and biochemical screening; SBU, Swedish Council on Health Technology. a Note that about 60% of participants did not provide any answer. b Multiple choice answers.
given to the woman. However, if the information is not related to this, it should only be revealed at the woman’s request. As the significance of the markers is not absolute, and as its relation to the health of the fetus is not completely known, it is not certain that it is covered by the Genetic Integrity Act (SFS 2006:351). The ethical dilemmas associated with assessment of ultrasound markers, which healthcare professionals can encounter, have also been discussed in previous studies (17,18). This study indicates that Swedish law and ethical rules are not being followed completely. First, the pre-examination information regarding the assessment and the importance of observed soft markers seems to be insufficient. Second, the quality of the antenatal care offered is unequal in this respect across the country. Third, the pro-
vision of information and the documentation of findings are handled differently at different obstetric ultrasound clinics. This is probably also the case in other countries. It is noteworthy that the majority of clinics did not offer any information, despite their staff wanting to do so. In line with previous study findings indicating that midwives and doctors do not want patients to worry and therefore avoid talking about risks (19), a feasible interpretation could be that healthcare personnel do not want to make patients anxious and expose them to unnecessary invasive tests (18). Midwives may also perceive the provision of information about fetal diagnosis as difficult, both from an ethical and a practical point of view (20). The results of another study (21) indicated that only a minority of midwives felt comfortable with providing advice regard-
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Table 5. Documentation of the sonographic findings. Variable
References n
Do you keep records on observed soft markers? Only in case the women are informed about the markers 28 Even when women are not informed about the markers 13 No, we do not keep record on any markers 5 How is the documentation of observed soft markers conducted? As picture and text 37 As text (through medical record or reports) 4 As digital images 3 As paper images 1 Is routine photo documentation common at your work? Only when deviations are detected or in special cases 19 Yes, keep photo/clip from standard projections 18 Yes, tape record the entire examination 0 No, no photo documentation 10
%
61 28 11 82 9 7 2 40 39 0 21
ing available genetic tests, communicating risk estimates when soft markers were observed in a fetus, or providing support in dealing with the results of a genetic test. At the same time, prospective parents do not think that they receive enough information from the midwives during the ultrasound examination (22). One of the strengths of this study was that all ultrasound clinics in Sweden were contacted, providing a broad coverage on information regarding how soft markers are managed in Sweden. Of the few clinics that did not respond, most were small with a limited number of patients. A limitation of the study was that our questionnaire had not been used or evaluated in other studies because it was developed by our research group specifically for this study and for a predefined population and was distributed by the supervising staff of the clinic to the responders. It is therefore possible that the respondents might have had different responsibilities and experience at the clinics, compared with other personnel. National guidelines regarding the information provided to parents pre-examination as well as the information and documentation about actual findings could help healthcare professionals to handle this difficult information and ethical dilemma. That would allow consistent information to be presented to parents regardless of where one lives or from whom information is received, thereby improving the premises for informed choice. Such national guidelines and consensus would have been valuable when introducing first-trimester CUB (17) and will be of great importance when new methods, such as non-invasive prenatal testing, are introduced.
Funding No funding was obtained for this study.
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