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3 Two-Dimensional and Three-Dimensional Doppler in Reproductive Medicine
35
and showed that subendometrial VI, FI and VFI
were signifi cantly lower in pregnant cycles than
nonpregnant ones. Logistic regression analysis
found that the subendometrial FI was the strongest predictive factor for the pregnancy outcome
among other 3D Doppler fl ow indices.
Kupesic et al. [ 23 ] performed 3D ultrasound
examination on the day of blastocyst transfer
and found that subendometrial FI was signifi cantly higher in pregnant cycles. Subendometrial
VI and VFI were similar between pregnant and
nonpregnant patients. Wu et al. [ 28 ] measured
subendo metrial blood fl ow on the day of hCG
and demonstrated that subendometrial VFI
was signifi cantly higher in the pregnant group.
Subendometrial VI and FI were also similar between pregnant and nonpregnant cycles.
Subendometrial VFI was superior to subendometrial VI, subendometrial FI and endometrial volume in predicting the successful outcome in the
receiver-operating characteristics (ROC) curve
analysis.
On the day of oocyte retrieval, Dorn et al. [ 29 ]
compared the subendometrial blood fl ow before
and after an intravenous administration of
Levovist, which is a contrast agent and consists
of 99.9 % of D-galactose. All subendometrial 3D
Doppler fl ow indices after the administration of
the contrast agent were signifi cantly higher than
those without the contrast agent. However, all
subendometrial 3D Doppler fl ow indices with
and without the contrast agent were comparable
between pregnant and nonpregnant cycles. The
results of this study suggested that the use of 3D
power Doppler ultrasound under a contrast agent
during IVF treatment provided no additional
advantage over the conventional 3D power
Doppler ultrasound examination.
Järvelä et al. [ 30 ] determined endometrial and
subendometrial VI after gonadotrophin stimulation but before hCG administration and again the
day of oocyte retrieval. There were no differences between the pregnant and nonpregnant
groups in endometrial and subendometrial VI on
either day examined. I have published the largest
study involving 451 transfer cycles [ 31 ]. Patients
in the pregnant group had signifi cantly lower
uterine RI, endometrial VI and VFI than those in
the nonpregnant group. Endometrial thickness,
endometrial volume, endometrial pattern, uterine
PI, endometrial FI and subendometrial VI, FI and
VFI were similar between the nonpregnant and
pregnant groups. The number of embryos
replaced and endometrial VI were the only two
predictive factors for pregnancy in a logistic multiple regression analysis. ROC curve analysis
revealed that the area under the curve was around
0.5 for all ultrasound parameters for endometrial
receptivity. Implantation and pregnancy rates
were comparable for patients with and without
endometrial and subendometrial blood fl ow [ 31 ].
The age of women, their smoking habits, their
types of infertility and parity and causes of subfertility had no effect on all endometrial and subendometrial 3D Doppler fl ow indices [ 35 ]. Endometrial
blood fl ow was negatively affected by serum oestradiol concentration on the day of hCG. Indeed,
endometrial and subendometrial 3D Doppler fl ow
indices in the stimulated cycles were signifi cantly
lower than those in the natural cycles of the same
patients undergoing IVF treatment [ 36 ].
Uterine PI, uterine RI, endometrial and subendometrial 3D Doppler fl ow indices were comparable between the nonpregnant and pregnant
groups’ frozen-thawed embryo transfer cycles
using natural or clomiphene-induced cycles [ 32 ].
On the other hand, endometrial and subendometrial blood fl ow was signifi cantly higher in pregnant patients with live birth following IVF and
frozen-thawed embryo transfer treatment [ 37 ].
Mercè et al. [ 33 ] found that endometrial 3D
power Doppler fl ow indices were statistically signifi cantly higher in the pregnant group. The area
under ROC curve was statistically signifi cant for
endometrial VI, FI and VFI when no grade 1
embryos or only one was transferred, but not when
two or three grade 1 embryos were transferred.
Changes in Endometrial and Subendometrial Blood Flow
Ultrasound examination was performed on the
day of hCG [ 28 , 33 ], oocyte retrieval [ 29 – 31 ]
and blastocyst transfer [ 23 ]. There is no
consensus when the ultrasound examination for
36
E.H.Y. Ng
assessing endometrial receptivity in IVF treatment should be done. The day of the ultrasound
examination in these studies was chosen for
logistic reasons.
Endometrial blood fl ow changes throughout
the menstrual cycle [ 38 ]. Raine-Fenning et al.
[ 38 ] showed that endometrial and subendome-
trial blood fl ow by 3D ultrasound increased during the proliferative phase, peaking around
3 days prior to ovulation before decreasing to a
nadir 5 days post-ovulation. Hypoxia in the
endometrium may play a benefi cial role for
implantation as the expression of vascular endothelial growth factor is upregulated by hypoxia
[ 39 ] and relatively low oxygen tension was pres-
ent around the blastocyst during the time of
implantation [ 40 ].
Endometrial and subendometrial blood fl ow
was measured on the days of hCG and ET [ 34 ].
Patients in nonpregnant and pregnant groups had
comparable 3D Doppler fl ow indices of endometrial and subendometrial regions measured on
either day. Percentage changes in endometrial
and subendometrial 3D Doppler fl ow indices
between these 2 days were also similar. Again,
none of the ultrasound parameters was predictive
of pregnancy in a multiple logistic regression
analysis and the ROC curve analysis.
Prediction of Ovarian Response to Gonadotrophin
Development of multiple follicles in response to
ovarian stimulation is the key factor leading to a
successful outcome of IVF treatment. Poor ovarian response is associated with lower pregnancy
rates, while exaggerated ovarian response leads
to an increased risk of ovarian hyperstimulation
syndrome. Prediction of ovarian responses prior
to gonadotrophin stimulation is useful in counselling patients and helpful in tailoring the dosage of gonadotrophin to individual patients.
A number of ultrasound parameters have been
examined to predict the ovarian response to
gonadotrophins, including ovarian volume, antral
follicle count [ 41 ] and ovarian stromal blood fl ow
[ 15 , 42 – 45 ].
Folliculogenesis in the human ovary is a
complex process regulated by a variety of endocrine and paracrine signals [ 46 ]. It has been sug-
gested that the availability of an adequate vascular
supply to provide endocrine and paracrine signals may play a key role in the regulation of follicle growth [ 47 ]. It is postulated that increased
ovarian stromal blood fl ow may lead to a greater
delivery of gonadotrophins to the granulosa cells
of the developing follicles.
Ovarian Stromal Blood Flow by 2D Doppler
Ovarian stromal blood fl ow can be assessed by
colour Doppler and power Doppler ultrasound.
Power Doppler is better suited to the study of the
ovarian stromal blood fl ow as it is more sensitive
to lower velocities and essentially angle independent [ 11 , 48 ]. Flow velocity waveforms were
obtained from stromal blood vessels away from
the ovarian capsule, if present. The ‘gate’ of the
Doppler was positioned when the vessel with
good colour signals was identifi ed on the screen.
PI, RI and peak systolic blood fl ow velocity
(PSV) of stromal vessels was calculated electronically when three similar, consecutive waveforms
of good quality were obtained.
Zaidi et al. [ 42 ] showed that mean ovarian
stromal PSV prior to pituitary downregulation
was signifi cantly correlated with the number of
follicles, after controlling for patients’ age.
Patients with >6 follicles at retrieval had signifi cantly higher velocity than those <6 follicles
(10.2 ± 5.8 cm/s vs. 5.2 ± 4.2 cm/s). Similarly,
Engmann et al. [ 43 ] demonstrated that ovarian
stromal PSV after pituitary downregulation was
the most important independent predictor of the
number of oocytes obtained in patients with normal basal FSH concentration, when compared
with age of women, basal FSH concentration, E2
concentration or FSH:LH ratio. Bassil et al. [ 49 ]
reported that women with RI of ovarian blood
fl ow >0.56 had a signifi cantly longer stimulation
and a signifi cantly lower mean number of oocytes
retrieved. Both BMI and AFC were not included
in these three studies.
3 Two-Dimensional and Three-Dimensional Doppler in Reproductive Medicine
37
Popovic-Todorovic et al. [ 15 ] evaluated
ovarian stromal blood by 2D power Doppler
ultrasound and a semi-quantitative score was
allocated to each ovary according to the number
and area of the power Doppler signals. Total
Doppler score was the sum of scores for each
ovary: score 1 for poor fl ow, score 2 for moderate
fl ow and score 3 for good fl ow. The number of
oocytes was predicted by AFC, total Doppler
score, serum testosterone concentration and
smoking status.
In a prospective study, 136 women aged
<40 years with basal FSH concentration <10 IU/L
received a standard regimen of ovarian stimulation in their fi rst IVF cycle [ 50 ]. The ovarian stro-
mal blood fl ow measured by 2D power Doppler
was compared to age of women, body mass
index, basal FSH concentration and AFC in the
prediction of the ovarian response. Basal FSH
concentration achieved the best predictive value
in relation to the number of oocytes obtained, followed by AFC and BMI. AFC was the only predictive factor of serum oestradiol concentration
on the day of hCG, while BMI was predictive of
the gonadotrophin dosage. Ovarian stromal blood
fl ow indices measured by power Doppler ultrasound had no predictive value for the ovarian
response.
Ovarian Stromal Blood Flow by 3D Doppler
Therefore, ovarian stromal blood fl ow
measured after pituitary downregulation by both
2D and 3D power Doppler was not predictive of
the ovarian response in terms of the number of
oocytes obtained, the duration and dose of FSH
used and maximum serum E2 concentrations.
These results were in line with those of previous
studies assessing ovarian stromal blood fl ow in
fertile Chinese women [ 52 , 53 ]. There was no
effect of age on mean PSV of ovarian stromal
blood vessels determined by 2D colour Doppler
ultrasound. Using 3D Doppler ultrasound, ovarian stromal vascularity was signifi cantly lower in
fertile Chinese women aged ≥41 years, and the
rate of decline of total ovarian vascularity index
was only 0.18 % per year [ 53 ]. These data
strongly suggest that reduction in ovarian stromal
blood fl ow with increasing age is a relatively late
phenomenon, and ovarian stromal blood fl ow is
unlikely an early marker for ovarian response.
Conclusion
Angiogenesis plays a critical role in various
female reproductive processes such as fol-
liculogenesis, formation of a corpus luteum,
growth of endometrium and implantation.
Assessment of blood fl ow by Doppler ultra-
sound may add a physiological dimension to
the anatomical USS parameters, but for the
time being, 2D and 3D Doppler study of the
endometrium and the ovary has no defi nite
benefi t in routine patient care in IVF treatment.
I further evaluated the role of ovarian stromal
blood fl ow by 3D power Doppler. Age of women,
BMI, basal FSH concentration, AFC and ovarian
stromal vascularity indices measured by 3D
power Doppler were compared in 111 women
aged <40 years old with basal FSH concentration
<10 IU/L in their fi rst IVF cycle [ 51 ]. The results
indicated that AFC achieved the best predictive
value in relation to the number of oocytes
obtained, followed by age of women and BMI.
Basal FSH concentration was the only predictive
factor for the duration and dosage of gonadotrophin used. Mean ovarian 3D power Doppler fl ow
indices were not predictive of pregnancy in a
multiple logistic regression analysis.
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Legal Aspects of Ultrasound Imaging in Reproductive Medicine
James M. Shwayder
4
Legal Aspects of Ultrasound Imaging in Reproductive Medicine
Medical liability concerns all providers and has
great impact on the health system. Recognizing
the prime areas of risk and proactively addressing
these issues can reduce the frequency and severity of litigation. However, liability now extends
to billing fraud, which can be even more fi nancially devastating.
The elements of malpractice include the following: (1) the duty to care for a patient; (2) a
breach of that duty, i.e., a breach of the standard
of care; (3) that breach is the proximate cause of
an adverse outcome or complication; and (4)
damages result that are compensable. If any one
of these elements is not met, then the action fails
or in other words defensible. Litigation in ultrasound imaging focuses on two areas: (1) the
proper performance of the study with acquisition
of images suitable to render a diagnosis and (2)
errors surrounding study interpretation and
reporting.
J. M. Shwayder , MD, JD
Department of Obstetrics and Gynecology ,
University of Mississippi , 2500 North State Street,
Room L305 (for FedEx or UPS) , Jackson ,
MS 39216 , USA
e-mail: jshwayder@umc.edu
Performance of the Ultrasound Study
Litigation in this area tends to focus on the
following:
1. Inadequate training of the person performing
the ultrasound study
2. Inadequate and thus negligent performance of
the study, with inadequate or incomplete images
3. Inadequate supervision of the sonographer
4. Lost or misplaced images
5. Inadequate equipment maintenance
Personnel Performing Ultrasound Examinations
There are specifi c issues that are unique to
ultrasound. Ultrasound performance is often
delegated to other personnel. The American
Institute of Ultrasound in Medicine (AIUM)
accreditation guidelines require that all persons
who perform ultrasounds, other than physicians, are either RDMS (Registered Diagnostic
Medical Sonographer) certifi ed or eligible [
However, many reproductive medicine practices
use nurses, nurse practitioners, or other personnel who do not meet these criteria to perform
ultrasound. In 2009, the American Institute
of Ultrasound in Medicine (AIUM) and the
American Society of Reproductive Medicine
1 ].
L.A. Stadtmauer, I. Tur-Kaspa (eds.), Ultrasound Imaging in Reproductive Medicine,
DOI 10.1007/978-1-4614-9182-8_4, © Springer Science+Business Media New York 2014
41
42
J.M. Shwayder
(ASRM) issued a consensus statement regarding
focused ultrasounds in reproductive medicine
[ 2 ]. Ultrasounds for follicular monitoring are
intended to provide specifi c diagnostic information comprising the number and size of developing follicles, as well as uterine evaluation
including endometrial thickness and morphology.
These are considered limited ultrasounds, rather
than complete diagnostic sonographic studies.
The consensus is that such limited examinations
are within the scope of practice of a nurse with
specifi c training and with appropriate physician
supervision in an infertility practice. However, it
states that a comprehensive ultrasound examination should have been performed within the prior
4–6 months to exclude signifi cant gynecologic
pathology.
A caution is that the position of AIUM and
ASRM on nurses performing ultrasound examinations pertains to the limited studies appropriate
for monitoring ovulation induction. If the practice performs comprehensive diagnostic studies,
according to AIUM guidelines, these should be
performed by physicians or appropriately trained
and qualifi ed personnel. If not, the physician is at
increased legal risk in the event of misdiagnosis.
However, the training of the nonphysician
personnel who perform the diagnostic procedure
and equipment maintenance are the responsibility of the physician [ 6 ]. Thus, any errors resulting
from inadequately performed ultrasound studies
fall within legal concept of respondeat superior.
This concept holds the employer, or physician,
liable for the wrong of an employee if it was
committed within the scope of employment [ 7 ].
The exception to this supervision level is in the
performance of sonohysterography that requires
“personal supervision.” Personal supervision
requires the physician’s presence in the room
during the performance of the procedure. In most
instances this requirement is met when the physician inserts the catheter and instills fl uid while
the ultrasound is performed. Similar requirements exist for sonosalpingography. If the physician is not available for immediate consultation,
then guidelines should be established that address
immediate communication with the supervising
physician. In addition, callback mechanisms
should be established when further evaluation of
the patient is required.
Image Acquisition and Retention
Adequacy of the Ultrasound Study
Images obtained should conform with the guidelines set forth by AIUM [ 3 – 5 ]. Incomplete stud-
ies expose the physician to increased risk as the
lack of images supporting the reported diagnosis
reduces defensibility. Also, the lack of a documented complete study can expose the physician
to a claim of insurance fraud specifi cally billing
for a higher level of service than supported by
documentation.
Ultrasound Supervision
The Centers for Medicare and Medicaid Services
(CMS) states, with one exception, that “general
supervision” of personnel performing ultrasounds is required. “General supervision” dictates that the physician’s presence is not required
during the performance of the procedure.
Images obtained should conform with the guidelines set forth by AIUM [ 3 – 5 ]. Ideally, images
should be retained in a digital format to maximize retention of image quality for a more
extended time. At a minimum, thermal print
images of critical fi ndings should remain in the
medical record. The images, as well as the report,
should be retained for the statute of limitations as
required in the applicable jurisdiction.
Equipment Maintenance
AIUM accreditation specifi es that preventive
maintenance and resolution testing should be
done on an annual basis. This maintenance is
critical to assure optimum performance and is
recommended regardless of accreditation status.
Ultrasound performance with outmoded technology or with machines that are not properly maintained exposes the physician to additional risk.
4 Legal Aspects of Ultrasound Imaging in Reproductive Medicine
43
Study Interpretation and Reporting
Ultrasound litigation surrounding ultrasound
remains most frequent with obstetrical ultrasound. However, gynecologic ultrasound is now
the second most common cause of ultrasoundrelated litigation [ 8 ]. The most common causes
of liability actions comprise the following: (1)
perception errors, (2) interpretation errors, (3)
failing to suggest the next appropriate procedure,
and (4) failure to communicate signifi cant abnormal fi ndings [ 9 ].
Perception errors occur when an abnormality
is seen in retrospect but it was missed when interpreting the initial study [ 10 ]. An example would
be an adnexal mass with a gestational sac, consistent with an ectopic pregnancy, which was not
identifi ed on the initial study but identifi ed on
subsequent review. Although the error rate in
radiology is approximated at 30 % [ 10 ], this rate
is not accepted when errors occur. The critical
question is: “Was it below the standard of care for
the physician not to have seen the abnormality?”
[ 11 ] These cases are diffi cult to defend with
almost 80 % of cases decided against the physician if the case goes to jury verdict [ 11 ]. Thus,
most of these suits are settled. The best defense is
(1) a complete examination performed in a systematic fashion, evaluating all appropriate structures; (2) appropriate and adequate image
documentation; (3) appropriate and reasonable
interpretation of the fi ndings; and (4) ongoing
continuing education for the interpreting
physician.
Interpretation errors occur when the abnor-
mality is perceived but is incorrectly described
[ 9 ]. One example that is becoming a more fre-
quent source of litigation is the misdiagnosis of
an “ectopic pregnancy.” In this instance an early
intrauterine pregnancy, with no visualized gestational sac, and a corpus luteum is diagnosed as an
ectopic pregnancy, with subsequent administration of methotrexate. A more common error is
when a normal variant is called abnormal, such as
a corpus luteum diagnosed as a malignancy. The
converse is when a malignant lesion is called
benign, such as a complex ovarian mass diagnosed as a benign lesion. These errors often occur
due to lack of knowledge or faulty judgment of
the interpreting physician. The best defense is
available when the interpretation includes an
appropriate differential diagnosis, particularly if
it includes the correct diagnosis. As these cases
are subject to interpretation, they tend to be more
defensible, with 75 % won if the case goes to jury
verdict [ 11 ].
Failing to suggest the next appropriate proce-
dure places the interpreting physician at risk of
litigation and liability. The prudent physician or
radiologist should suggest the next appropriate
study or procedure based upon the fi ndings and
clinical information. The recommended study
should add meaningful information to clarify or
confi rm the diagnosis [ 12 ]. This is particularly
apropos when performing and interpreting ultrasound studies referred from outside physicians.
An example is when a study is consistent with a
pregnancy of unknown location. The appropriate
recommendation would be serial hCG levels and
a repeat ultrasound as clinically indicated.
Failure to communicate signifi cant abnormal
fi ndings on an ultrasound again places the interpreting physician at risk for liability. Two examples are the diagnosis of an ectopic pregnancy or
an ovarian malignancy without prompt notifi cation of the referring physician. These fi ndings
place the patient at signifi cant risk and merely
providing a written report is not adequate.
Practices should have established protocols or
guidelines for notifying referring physicians of
sonographic results, particularly for those cases
with critical fi ndings. It is preferred that all studies have a fi nal reading and report issued within
24 h of the original procedure. Following these
protocols and guidelines provide the best defense
for the physician [ 9 ].
New Horizons in Ultrasound Liability
First-Trimester Ultrasound
Identifying the early embryo and cardiac activity
is an emotional event for patients. One should
avoid the temptation to demonstrate the fetal
heart rate with Doppler sonography as this
exposes the early embryo to higher than ideal
44
J.M. Shwayder
energy. All ultrasound studies should be
performed with the ALARA (as low as reasonably achievable) principle as the standard. This
minimizes fetal exposure and the potential risk to
the developing fetus.
Some physicians defer referral to an obstetrical or maternal-fetal medicine specialist until the
early second trimester. This habit should be carefully scrutinized in light of advances in antenatal
diagnosis. ACOG recommends antenatal screening for all patients prior to 20 weeks of gestation
[ 13 ]. First-trimester screening with nuchal trans-
lucency, integrated and sequential testing in the
fi rst and second trimesters, and maternal blood
screening for fetal cell-free DNA are all options
for earlier detection of chromosomal abnormalities. However, counseling and appropriate referral are crucial to the effective use of these
diagnostic modalities. In addition, there is
increasing evidence that screening for anatomic
abnormalities may be feasible in the fi rst trimester. With this background, if one is not prepared
to provide the necessary counseling and screening, it may be prudent to refer patients once cardiac activity is demonstrated, such that appropriate
counseling and screening may be performed.
Healthcare Fraud
Increasing liability exists related to inappropriate
billing for ultrasound-related procedures.
Insurance fraud is assuming a greater role in liability in a physician’s practice. In reproductive
medicine, one must be cautious to avoid liability
exposure for fraud. For example, infertility services may not be covered by a patient’s insurance
plan. In such cases, patients may request a change
in the diagnostic codes to gain insurance coverage. Pursuing such action, when not clinically
appropriate, exposes one to the claim of insurance fraud, with devastating consequences, ranging from monetary penalties (up to $11,000 per
instance); exclusion from governmental payers,
such as Medicare, Medicaid, and Tri-Care;
closing of one’s offi ce; and even prison sentences. One must remind patients of these potential consequences and resist such actions.
Intent to commit fraud is not necessary to
face litigation and liability. However, compliance
programs can mitigate damages and penalties
when in place and functioning. Guidance for
even individual and small group practices has
been provided by the Offi ce of the Inspector
General [ 14 ]. This includes the following
recommendations:
1 . Conduct internal monitoring and auditing.
Audits should be conducted at least every
6 months with a representative set of patient
charts.
2 . Implement compliance and practice stan-
dards . Practice standards should be adopted
and adhered to.
3 . Designate a compliance offi cer or contact .
It is recommended that the compliance offi cer
should not be the same person responsible for
coding and bill submission. An “independent”
person is best suited to detect billing and
coding irregularities.
4 . Conduct appropriate training and education .
The physicians and their staffs should receive
ongoing education, with appropriate updates,
to remain up-to-date on proper coding and
billing practices.
5 . Respond appropriately to detected offenses
and develop corrective action . If inappropriate payments are detected, the practice
should return these promptly. Further, education and actions to correct any detected
irregularities are to be instituted upon
discovery.
6 . Develop open lines of communication . The
physician should maintain an environment
that encourages compliance, open communication, and transparency.
7 . Enforce disciplinary standards through well-
publicized guidelines . Discipline for intentional coding or billing irregularities should
be established, published, and enforced.
Conclusion
This chapter has addressed several areas of
potential liability related to ultrasound imag-
ing in reproductive medicine. Discussed are
strategies and practices that minimize liability
exposure and risk. Unfortunately, the potential
4 Legal Aspects of Ultrasound Imaging in Reproductive Medicine
45
for a liability action exists even if all of the
recommendations are followed. However, a
case is more defensible when these best
practices are followed.
References
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July 2012.
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6 July 2012.
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of sonohysterography.
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