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TRIBUTE

This book, previously entitled simply Sonography in ous awards and honors, among them are the Larry Mack
Obstetrics and Gynecology, is now entitled Fleischer’s Award for Best Research Paper by the Society of Radiologists
Sonography in Obstetrics and Gynecology, in honor of the in Ultrasound in 1998, the William Fry Award for Outstanding
lead author, Arthur C. Fleischer, MD, whose brilliance, Contributions to Ultrasound by the American Institute
intellect, and experience have spanned eight editions. of Ultrasound in Medicine in 1999, the Frank H. Boehm
Arthur C. Fleischer was born in Miami, Florida in Award for Contribution to Continuing Medical Education
1952. His parents were Lucille and Eugene. Lucille was by Vanderbilt University School of Medicine in 2005, and the
a lifelong learner and educator, graduating from Hunter Distinguished Alumnus Award from the Medical College of
College in 1942 (when she was 17), obtaining a Master’s Georgia in 2007. In 2011, Dr. Fleischer was honored with the
in Education from the University of Miami in 1951, and Cornelius Vanderbilt Chair in Radiology.
graduating first in her class at the University of Miami Art and Lynn have three children, Braden, Jared, and
School of Law in 1958. Eugene attended the University of Amy, and one grandson, Jakob. When asked about her
Miami after military service, became a general contractor father, Amy had the following words:
in Miami, and was instrumental in starting a new Reform
Jewish congregation, Temple Beth Am in Kendall, Florida.
Art Fleischer’s grandparents were Hungarian immigrants The essence of Dr. Fleischer (our dad, or “Daddio,” as we
who came to New York City from Budapest in 1921. As know him) is exemplified by an unconditional love of learn­
a child, Art was fortunate to excel at equestrian competi- ing. Whether our family discussions took place at the dinner
tions and was state champion from 11 to 18 years of age. At table or at his favorite lunch spot (let’s be honest, most of
Emory University, he completed his thesis on ultrasound our chats involved food), he always exuded an enthusiasm
enhancement of treatments and received his BS degree, for learning.
magna cum laude, in biology in 1973. He met Lynn in 1974 In fact, the most valuable gift our dad gave us (besides
through the introduction from a mutual medical school life itself!) is his infectious curiosity. His passion for new
friend, and they were married in 1975. technology is not only evidenced by the every-growing stack
In 1976, he received the MD degree from the Medical of medical and academic publications he has authored
College of Georgia at Augusta, and in 1980, he complet- (during his 40-year career) but also by the abundant sea of
ed the Radiology Residency/Fellowship at Vanderbilt gadgets in his office! His thirst for innovative tools and tech­
University Medical Center inNashville, Tennessee. nology is unquenchable, even when our mom threatens to
Dr. Fleischer began his medical career in 1974 as the purge his “toys” in order to make a path through the house.
Acting Director of Diagnostic Ultrasound at the Medical
College of Georgia. He came to Vanderbilt University School In amongst these toys, a plethora of textbooks, articles, pho­
of Medicine in 1976 and has held the following positions: tos, and old x-ray films make our home a monument to his
Acting Director of Diagnostic Ultrasound; Clinical Fellow in staggering medical career. To us, such tangible evidence—of
Ultrasound; Assistant Professor (Radiology and Obstetrics which this book is now a vital part—will always serve to
and Gynecology); and Associate Professor (Radiology and represent his most deeply held belief in the value of asking
Obstetrics and Gynecology). Additionally, Dr. Fleischer was good questions while seeking new understanding about the
Visiting Professor in Radiology (Diagnostic Ultrasound) world.
at Thomas Jefferson University Hospital. Presently, he is Amy Fleischer, MS, OTR/L, on behalf of Art’s
Professor of Radiology and Radiological Sciences (1987); three children
Professor of Obstetrics and Gynecology (Secondary) (1987);
Medical Director of the Sonography Training Program Luis Gonçalves, MD, has the following observations:
(1981); and Medical Director of Ultrasound.
Dr. Fleischer has been active in several specialty There are moments in life when one wonders about how the
societies, including the American Institute of Ultrasound Universe conspires to align with perfection those people who
in Medicine (Board of Governors, Fellow), the American eventually become a permanent part of our path on Earth.
College of Radiology (Fellow), the Society of Radiologists in I would like to take this moment to acknowledge the oppor­
Ultrasound (Fellow), and the Society for the Advancement tunity of having Arthur Fleischer cross my path 24 years
of Women’s Imaging (Cofounder and President). ago at Vanderbilt University. Art has certainly inspired me
Professor Fleischer has authored more than 200 then and will continue to inspire those of us who have been
research papers regarding clinical aspects of diagnostic fortunate enough to have crossed his path and know first-
ultrasound and 23 textbooks involving the use of diagnostic hand the enormity of the human being who teaches and
sonography in obstetrics/gynecology. He has received numer- leads with a light heart.

Fleischer_FM_i-xxiv.indd 21 08/09/17 5:18 pm


Tribute xxii

Eugene C. Toy, MD, on behalf of the tens of thousands of knowledge, and so much zeal, and so much compassion
physicians, sonographers, residents and students who have can be in one person!” Dr. Fleischer has been one the cor­
been touched by Dr. Art Fleischer, has these words: nerstones in advancing imaging in women’s health over the
past 40 years, particularly in the areas of gynecologic ultra­
Art Fleischer has been a tremendous inspiration to everyone
sound. Not only has he propelled this embryologic science
around him. He has an amazing sense of humor, a consci­
into a maturing and exciting field in science and informa­
entiousness that goes far beyond the normal “call of duty,”
tion, he has also put his own personal heart and soul into
and a dedication to women’s health through imaging and
gynecologic sonography. I feel so fortunate to be able to call
the prevention and diagnosis of disease. Art is an amazing
Art Fleischer my friend, mentor, and inspiration. For the
educator, and I have sat in his conferences amazed at how
tens of thousands who use imaging to help treat women, and
much he is able to teach—from the anatomical structures,
the millions of women who are dependent on this modal­
to the imaging, to the disease. More than all of this, Art has
ity for their care, we pause a moment to give tribute to a
a tremendous love for people and cares so deeply about all
man who worked tirelessly in his significant contributions
of those who are fortunate enough to cross paths with him.
to the science and art of gynecologic sonography. For this
One physician who was in a medical school radiology rota­
reason, we have entitled this book, Fleischer’s Sonography
tion with Art summed it up: “I don’t know how so much
in Obstetrics and Gynecology.

Fleischer_FM_i-xxiv.indd 22 08/09/17 5:18 pm


PART 1

GENERAL OBSTETRIC
SONOGRAPHY

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2 Part 1 GENERAL OBSTETRIC SONOGRAPHY

Chapter 1

ULTRASOUND BIOEFFECTS AND SAFETY:


WHAT THE PRACTITIONER SHOULD KNOW

Jacques S. Abramowicz ● Eyal Sheiner

Key Terms1 7. Output Display Standard (ODS): actual name—


Standard for Real-Time Display of Thermal and
1. Acoustic streaming: movement of tissue or fluid, Mechanical Acoustic Indices on Diagnostic Ultra-
resulting from the passage of alternating positive sound Equipment. Introduced to make end users
and negative pressures of the ultrasound wave. Can aware, in real time, of the potential effects of ultra-
also result from movements of bubbles, as a result of sound in tissues. See also mechanical index and
changes in pressure. thermal index.
2. ALARA principle: stands for As Low As Reasonably 8. Radiation force: force resulting from absorption of
Achievable, a way to obtain the best, clinically rel- some of the energy of the acoustic wave by tissue
evant image while keeping ultrasound intensity and and transformation into heat.
exposure as low as possible. 9. Scanned mode: refers to the ultrasound beam
3. Cavitation: bubble activity, secondary to ultrasound moving through the field, with energy distributed
insonation. The positive aspect of the ultrasound over a large volume, such as in B-mode and color-
pressure wave causes compression of the bubble flow Doppler.
while the negative part, also called rarefactional, 10. Thermal index (TI): expresses the potential for
causes production of the bubbles or expansion of temperature increase in tissues traversed by the
existing ones. Cavitation can be stable or inertial. ultrasound wave. It is given by the ratio of the power
emitted by the transducer to the ultrasonic power
• Stable cavitation: bubble activity where bubble required to raise tissue temperature by 1°C for the
does not collapse (see inertial cavitation) but is specific exposure conditions. This is a relative indi-
moving back and forth in the tissue or fluid, thus cation and does not necessarily correspond to the
potentially causing the surrounding medium to actual temperature increase. One of three thermal
flow (ie, stream, hence the term streaming). indices is displayed, based on whether soft tissue
• Inertial (previously known as transient) cavita- (TIS, mostly first and early second trimesters), bone
tion: bubbles that are compressed and expanded (TIB, late second and third trimesters), or adult cra-
but with each compressing (positive) component, nium (TIC) is being scanned.
causing the volume to diminish ever more, until 11. Unscanned mode: the ultrasound beam is station-
collapse occurs. This collapse can generate tre- ary with power concentrated along a single line,
mendously elevated temperature and pressure such as in M-mode and spectral Doppler.
for an extremely short time and over an extremely
short space (called an adiabatic reaction). This can
result in production of several more bubbles, local
cell damage, and/or generation of free radicals. INTRODUCTION
4. Derating: action of multiplying a value measured in “Is this safe for my baby?” Ultrasound practitioners hear
water with standard methods by a correction factor this question almost every day in clinical practice. The
to account for the attenuation of the ultrasound field answer generally given is: “Of course. Ultrasound is not
by the tissue traversed by the beam (usually 0.3 dB/ x-rays, it is not invasive; it has been used for close to sixty
cm/MHz). years and is perfectly safe.” While this answer may, in fact,
5. Dwell time: the time during which the ultrasound contain some correct facts (ultrasound is not x-rays), the
beam impinges on a specific organ, body part, or concept of perfect safety is not scientifically valid, and
entire organism. furthermore, the level of knowledge regarding poten-
6. Mechanical index (MI): expresses the potential for tial effects of ultrasound in tissues is, by and large, very
nonthermal (also known as mechanical) effects in low among end-users of this technology. Ultrasound in
tissues traversed by the ultrasound wave. Depends obstetrics is convenient, painless, and results are available
on the pressure and the frequency ( = P/ f ). immediately. The belief exists that is does not pose any risk

Fleischer_CH01_p001-p024.indd 2 08/09/17 10:50 am


Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 3

to the pregnant patient or her fetus. Ultrasound, however, 6


is a form of energy and, as such, has effects in biological Resolution
tissues (bioeffects). The physical mechanisms responsible Penetration
for these effects are nonthermal (mechanical) or thermal. 5
The nonthermal mechanisms can further be separated
into acoustic cavitation (inertial and noninertial) and
noncavitational mechanisms, ie, acoustic radiation force
(time-averaged force exerted by the ultrasound beam), 4
acoustic radiation torque (producing in the insonated tis-
sue a tendency to rotate or spin), and acoustic streaming
(circulatory flow). It is the role of science to show whether 3
any of these bioeffects may be harmful. The question has
been debated since the introduction of ultrasound in clini-
cal obstetrics, particularly as it relates to the fetal nervous 2
system2,3 and continues to be discussed currently.4-9(1)
This chapter presents basic notions of acoustics and
physics as they relate to ultrasound, examines some
literature on bioeffects and the safety of ultrasound, 1
reviews statements of various ultrasound organizations,
and affords a practical approach to limit the potential risks
to the fetus of exposure to diagnostic ultrasound (DUS). 0
Figure 1-1. Resolution (solid line) and penetration (dotted line) as a
BASIC PHYSICS OF ULTRASOUND function of increasing frequency, represented by the x-axis. Units on the
y-axis are not actual but representative of increasing values. The green
A detailed description of ultrasound physics can be found arrow represents the goal of improving penetration at high frequencies.
in various publications.10-12 However, certain properties of
ultrasound are very important when trying to understand (better resolution), the lower the penetration of the beam
safety and bioeffects. Equally important are tissue charac- through a given tissue (Figure 1-1).
teristics, such as attenuation coefficient. A basic knowl- Diagnostic ultrasound is pulsed, ie, pulses of acoustic
edge of instrument controls (“knobology”) is essential not energy separated by “silent” gaps. The number of pulses
only for appropriate clinical usage, but it is imperative to occurring in 1 second is the pulse repetition frequency
avoid potential harm. (PRF) and is controlled by the instrument in B-mode. In
Doppler mode, it can be altered by the end user. Another
important parameter is the duty factor: this is the fraction
The Ultrasound Wave
of time that the pulsed ultrasound is on. With an increase
Sound is a mechanical vibratory form of energy. It propa- in PRF, the duty factor increases. The pulse amplitude
gates through a medium by means of the motions of reflects pressure and is the maximum variation from the
the particles in the medium, under the influence of the baseline, expressed in MPa’s. Since the ultrasound wave is
alternating positive and negative components of the wave. sinusoidal, there are periods of positive and negative pres-
Megapascal (MPa) is the unit for pressure. Ultrasound sure. When the ultrasound wave exerts pressure on the
instrumentation can generate peak pressures of 5 MPa resisting insonated tissue, work is produced. The ability of
and above. This is in comparison to the atmospheric pres- the wave to do work is its energy (in joules). The rate at
sure, which is 0.1 MPa. Several other characteristics define which the energy is transformed from one form to another
the ultrasound beam. The ultrasonic wave progresses in is the power (in watts or milliwatts). Intensity represents
the insonated tissue at a velocity that is related to the the rate at which energy passes through area unit. Average
sound characteristics as well as the tissue properties. For intensity of a beam is expressed by the beam power (in
practical purposes, the average speed of sound propaga- milliwatts, mW), divided by the cross-sectional area of the
tion in biological tissues is estimated at 1540 ms/sec. beam (in cm2) and is, therefore, expressed in mW/cm2. As
Frequency is the number of cycles per second, measured stated earlier, DUS is performed with a pulsed wave. The
in hertz (Hz). The limits of human hearing spans from intensity is proportional to the square of the instantaneous
approximately 20 to 20,000 Hz. Diagnostic ultrasound is, ultrasound wave pressure. There are pulses of energy
generally, 2 to 10 million Hz (megahertz, MHz). Wave- intermingled with periods where no energy is emitted.
length is the distance between 2 corresponding points Depending on the time and location of the measurement,
on a particular wave. It is inversely proportional to the several parameters can be described in relation to time
frequency. Equipment resolution (the shortest distance or space: temporal peak intensity (the greatest intensity),
between 2 objects or parts of an object to be represented average intensity over time, ie, including “silent” time
by 2 separate echoes) depends on the wavelength: axial between pulses (temporal-average intensity), maximal
resolution ranges between 2 and 4 wavelengths. Hence, intensity at a particular location (spatial-peak intensity),
the shorter the wavelength (ie, the higher the frequency), as well as average-spatial intensity. By combining time
the better the resolution (the distance between 2 points and space, 6 intensities can be described: spatial average–
is smaller). The trade-off is that the higher the frequency temporal average (ISATA), spatial average–pulse average

Fleischer_CH01_p001-p024.indd 3 08/09/17 10:50 am


4 Part 1 GENERAL OBSTETRIC SONOGRAPHY

transesophageal or, in obstetrics and gynecology, transvaginal


 VALUES OF ISPTA BY MODALITY scanning. Another possibility is increasing the power of the
Table 1-1 AND YEAR OF DEFINITION instrument, resulting in improved resolution, as depicted by
the green arrow in Figure 1-1. This is seemingly simple, but
Modality/ 1976 1986 1992
instrument outputs are regulated in the United States (see
Application Values Values Values
The Output Display Standard section). Another important
Fetal imaging 46 94 720 parameter is acoustic impedance, which can be described
as the opposition to transmission or progression of the ultra-
Cardiac 430 430 720 sound wave. It is proportional to the velocity of sound in the
tissue (estimated at 1540 ms/sec) and to the tissue density.
Peripheral vessel 720 720 720

Ophthalmic 17 17 17
Instrument Outputs
Note: All are derated values in mW/cm .
2
Although some publications of various instrument outputs
Data from Nyborg WL. Biological effects of ultrasound: development of safety
guidelines. Part II: general review. Ultrasound Med Biol. 2001;27:301-333; are available,20-22 these are generally quickly outdated, since
Abramowicz JS. Prenatal exposure to ultrasound waves: is there a risk? Ultra- manufacturers introduce new commercial machines to the
sound Obstet Gynecol. 2007;29:363-367; Gressens P, Huppi PS. Are prenatal market (or modify existing ones) at a rate too fast for imme-
ultrasounds safe for the developing brain? Pediatr Res. 2007;61:265-266.
diate objective evaluation. From a clinical standpoint, there is
no easy way to verify the actual output of the instrument in
(ISAPA), spatial average–temporal peak (ISATP), spatial peak– use. In addition to the variety of instruments, each attached
temporal average (ISPTA), spatial peak–pulse average (ISPPA), transducer will generate a specific output, further compli-
and spatial peak–temporal peak (ISPTP). The most practical, cated by the different modes that may be applied.23 When
and commonly referred to, is the ISPTA. comparing modes, the ISPTA increases from B-mode (34 mW/
The maximal permitted value varies by clinical applica- cm2, average) to M-mode to color Doppler to spectral Dop-
tion. This had been determined in 1976 by the US Food and pler (1180 mW/cm2). Average values of the temporal aver-
Drug Administration (FDA),13 but was modified in 1986.14 aged intensity are 1 W/cm2 in Doppler mode but can reach 10
The most recent definition dates from 1992.15 These values W/cm2.23 Therefore, caution should be exercised when apply-
are shown in Table 1-1. One can observe from the table that, ing Doppler mode, particularly in the first trimester. Color
for fetal imaging, the ISPTA has been allowed to increase by a Doppler, while having higher intensities than B-mode, is still
factor of almost 16-fold from 1976 and almost 8-fold from much lower than spectral Doppler. This is mainly due to the
1986 to 1992, yet, all epidemiological information available mode of operation—sequences of pulses, scanned through
regarding fetal effects predates 1992. A remarkable fact is the region of interest (ROI or “box”). Most measurements are
that intensity for ophthalmic examination has not changed obtained from manufacturers’ manuals, having been derived
from the original 17 mW/cm2, a value approximately 42.5 in laboratory conditions. Real-life conditions may be differ-
times lower than the present allowed value for fetal scanning. ent.24 Furthermore, machine controls can alter the output. If
This will be addressed in more detail further in the chapter. one keeps in mind that, for instance, the degree of tempera-
ture elevation is proportional to the product of the amplitude
Tissue Characteristics of the sound wave by the pulse length and the PRF, it becomes
immediately evident why any change (augmentation) in these
When the ultrasound wave travels through a medium, its properties can add to the risk of elevating the temperature, a
intensity diminishes with distance.16 In completely homo- potential mechanism for bioeffects (see Thermal Effects). The
geneous, idealized materials, the signal amplitude would be 3 important parameters under end-user control are the scan-
reduced only because the wave is spreading. Biologic tissues, ning (or operating) mode, including transducer choice; the
however, are different and induce further weakening by system setup and output control; and the dwell time.
absorption and scattering (an effect called attenuation) and
by reflection. Many models have been described to help cal- 1. Scanning mode: as mentioned previously, B-mode
culate attenuation, particularly in obstetrical scanning,17 but carries the lowest risk, and spectral Doppler carries the
the most commonly used model uses an average attenuation highest (with M-mode and color Doppler in between).
of 0.3 dB/cm/MHz.18 It is important to note that the attenu- High pulse repetition frequencies are used in pulsed
ation increases logarithmically with frequency and distance Doppler techniques, generating greater temporal aver-
traveled. Technically, many measurements of acoustic power age intensities and powers than B- or M-mode, and
are performed in water, which has almost no attenuation. hence greater heating potential. An additional risk is
To apply these calculations to tissues, values are multiplied that since, in spectral Doppler, the beam needs to be
by this factor, an action called derating.19 Absorption is the held in relatively constant position over the vessel of
sound energy being converted to other forms of energy, and interest, there may be a further increase in temporal
scattering is the sound being reflected in directions other average intensity. Naturally, transducer choice is of
than its original direction of propagation. Since attenua- great consequence since it will determine frequency,
tion is proportional to the square of sound frequency, it penetration, resolution, and field of view.
becomes evident why higher frequency transducers have less 2. System setup: starting or default output power and,
penetration (but better resolution; see Figure 1-1). One needs, particularly, mode (B-mode, Doppler, etc) control
therefore, to be closer to the organ of interest, such as through changes. A subtler element is fine tuning performed

Fleischer_CH01_p001-p024.indd 4 08/09/17 10:50 am


Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 5

by the examiner to optimize the image and influence


output but with no visible effect (except if one follows
thermal index [TI] and/or mechanical index [MI] dis-
plays). Controls that regularize output include focal
depth (usually with greatest power at deeper focus but
occasionally, on some machines, with highest power
in the near field); increasing frame rate; and limit-
ing the field of view, for instance, by high-resolution
magnification or certain zooms (Figure 1-2).
3. In Doppler mode, changing sample volume and/or
velocity range (all done to optimize received signals)
changes output. Video Clip 1 demonstrates change in
output (as observable by change in TI) when changing
the focal distance. A very important control in every
mode is receiver gain. It often has similar effects to
the above controls on the recorded image but none
on the output of the outgoing beam, and is therefore
completely safe to manipulate (Figure 1-3). In other A
words, the receiver gain should be maximized before
output is increased. In addition, over the years, output
of instruments has increased.22, 25

C
Figure 1-3. A: Image obtained with 100% power (blue arrow). Note
MI = 1.2 and TI + 0.1 (yellow arrow). B: Power has been reduced to 85%
B (blue arrow). Note MI = 0.7 and TI + 0.0 (yellow arrow). This image is less
diagnostic. C: Receiver gain has been increased. Power is unchanged from
Figure 1-2. Acoustic output changes (as reflected by changes in TI).
B (nor are MI and TI) but image is as diagnostic as A.
A: Nonzoomed image. Please note TI = 0.2. B: Zoomed image. Please
note TI = 1.0 (arrow).

Fleischer_CH01_p001-p024.indd 5 08/09/17 10:50 am


6 Part 1 GENERAL OBSTETRIC SONOGRAPHY

4. Dwell time: is directly under the control of the exam- The organ at greatest risk is the central nervous
iner. Interestingly, dwell time is not taken into account system (CNS) due to a lack of compensatory growth of
in the calculation of the safety indices (thermal index, damaged neuroblasts. In experimental animals the most
TI and mechanical index, MI,) nor, in general, until common defects are of the neural tube, microphthalmia,
now, reported in clinical or experimental studies. cataract, and microencephaly, with associated functional
However, one needs to remember that it takes only and behavioral problems.32 Defects of craniofacial develop-
one pulse to induce cavitation, and about a minute ment including clefts,36 the axial and appendicular skeleton,37
to raise temperature to its peak. Directly related with the body wall, teeth, and heart38 are also commonly found.
dwell time is examiner experience: knowledge of Hyperthermia in utero (due to maternal influenza) has
anatomy, bioeffects, instrument controls, and scanning been described as a risk factor for congenital anomalies39,40
techniques. It can be safely assumed that the more and subsequent childhood psychological/behavioral distur-
experienced the examiner, the less scanning time will bances41 and, more particularly, schizophrenia.42 Nearly all
be needed to obtain the needed diagnostic images. these defects have been found in human epidemiological
studies following maternal fever or hyperthermia during
A standardized method of providing the end user pregnancy. It should be emphasized that these investigations
a parameter related to acoustic output and expressing have not involved ultrasound-induced hyperthermia effects.
potential for bioeffects is clearly needed; hence, the gener- Yet, there are data on the effects of hyperthermia and mea-
ation of the Output Display Standard, based on the 2 most surements of in vivo temperature induced by pulsed ultra-
likely interactions of ultrasound with tissues: thermal sound, but not in human beings.43-46 These data have been
and nonthermal or mechanical.26 widely reviewed.32,35,47-49 There is, however, a serious lack of
data that examine the effects of ultrasound while rigorously
THERMAL EFFECTS excluding other confounding factors. Two widely accepted
facts are that ultrasound has the potential to elevate the
Normal core human body temperature is generally accepted temperature of the tissues being scanned,50-53 and elevated
to be 37°C (98.6°F) with a diurnal variation of ±0.5°C to 1.0°C, maternal temperature, whether from illness or exposure to
although 36.8°C ± 0.4°C (95% confidence interval) may be heat, can produce teratologic effects.31,32,35,54-56 The major
closer to the actual mean for large populations.27 During question is, therefore, whether DUS can induce a harmful
the entire gestation, temperature of the human embryo/ rise in temperature in the fetus.57-59 Some believe that this
fetus is higher than maternal core body temperature28 and temperature rise is, in fact, a major mechanism for ultrasound
gradually rises until the final trimester (near term). The fetal bioeffects.30,35 Temperature elevation in the insonated tissue
temperature generally exceeds that of the mother by 0.5°C.29 can be calculated and estimated fairly accurately if the field is
Thermally induced teratogenesis (production of congenital sufficiently well characterized.60,61 For prolonged exposures,
malformations in an embryo or fetus) has been demon- temperature elevations of up to 5°C have been obtained.57
strated in many animal studies, as well as several controlled Temperature change in insonated tissues depends on the
human studies.30 While elevated maternal temperature in balance between heat production and heat loss. A particular
early gestation has been associated with an increased inci- tissue property that strongly influences the amount of heat
dence of congenital anomalies,31 the majority of these studies transported is local perfusion, which very clearly diminishes
do not involve ultrasound-induced temperature elevation. the risk, if present. Similar experimental conditions caused
Edwards and others have demonstrated that hyperther- a 30% to 40% lower maximal temperature increase in live
mia is teratogenic for numerous animal species, including versus dead sheep fetuses exposed in the near field,45 while
humans,32 and suggested a 1.5°C temperature elevation in guinea pig fetuses exposed at the focus the difference was
above the normal value as a universal threshold.33 Some approximately 10%.46 These findings were estimated to be
scientists believe that there are, indeed, temperature thresh- secondary to vascular perfusion in live animals. A significant
olds for hyperthermia-induced birth defects, hence the As cooling effect of vascular perfusion was observed only when
Low As Reasonably Achievable (ALARA) principle. There the guinea pig fetuses reached the stage of late gestation near
is, however, some evidence that any positive tempera- term, when the cerebral vessels were well developed. In the
ture differential for any period of time has some effect. In midterm, there was no significant difference when guinea
other words, that there may be no thermal threshold for pig fetal brains were exposed, alive (perfused) or postmortem
hyperthermia-induced birth defects.34 From careful thermal (nonperfused), in the focal region of the ultrasound beam.46
dose determinations, derived from published literature in In early pregnancy, under 6 weeks gestation, there
this area, it may be that hyperthermia-induced birth defects appears to be minimal maternal-fetal circulation, that is,
are produced in accordance with an Arrhenius relation for minimal fetal perfusion, which may potentially reduce heat
chemical rate effects, and thus have no threshold.35 Any tem- dispersion.62 The lack of perfusion is one reason why the
perature increment for any period of time has some effect. spatial peak-temporal average intensity (ISPTA) for ophthal-
Likewise, the higher the temperature differential or the lon- mic applications has been kept very low, in fact much lower
ger the temperature increment, the greater the likelihood of than peripheral, vascular, cardiovascular, and even obstetric
producing an effect. Gestational age is a vital factor: milder scanning, despite the general increase in acoustic power
exposure during the preimplantation period can have similar that was allowed after 1992 (see Table 1-1). There are some
consequences to more severe exposures during embryonic similarities in physical characteristics between the early,
and fetal development and can result in prenatal death and first-trimester embryo and the eye. Neither is perfused; they
abortion or a wide range of structural and functional defects. can be of similar size; and protein is present (in an increasing

Fleischer_CH01_p001-p024.indd 6 08/09/17 10:50 am


Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 7

elevation is proportional to the product of the wave ampli-


tude, length of the pulse, and PRF. Hence, manipulating any
of these via instrument controls will alter the in situ condi-
tions. It is clear that temperature increases of 1°C are easily
reached in routine scanning.67 Elevation of up to 1.5°C were
obtained in the first trimester and up to 4°C in the second
and third trimesters, particularly with the use of pulsed Dop-
pler.68 There is a large body of literature on heat shock pro-
teins (HSPs), the production of which is triggered by a core
temperature increase and the function of which is to protect
against hazardous effects of elevated temperature as well as
to induce some thermotolerance, ie, the ability to withstand
higher elevations than in the past, with no harmful results.69
While their production is activated by whole-body tempera-
ture elevation, and may be speculated in ultrasound-induced
thermal effects, it has not been shown to actually occur dur-
ing experimental (or clinical) insonation.
Figure 1-4. First trimester (11 weeks) measurement of the crown-
rump length: the entire fetus is within the ultrasound beam (“whole body
scanning”). MECHANICAL EFFECTS
proportion in the fetus). As mentioned previously, one must Ultrasound bioeffects also occur through mechanical mech-
then wonder why, from the time intensities were checked anisms.70,71 These are interactions between the ultrasound
and recommended in clinical practice, ISPTA was from the wave and the tissue that do not cause a significant degree
beginning and has continued to be maintained at 17 mW/ of temperature increase (less than 1°C above physiologic
cm2, while for fetal imaging it was allowed to reach 720 temperature). These include acoustic cavitation as well as
mW/cm2, up from 46 mW/cm2. At about weeks 4 to 5, the radiation torque and force, and acoustic streaming second-
gestational sac is about the size of the eye (2.5 cm in diam- ary to propagation of the ultrasound waves. While included
eter), and by week 8 it is around 8 cm in diameter. This may in this category, some effects are, in fact, the result of the
allow whole-body fetal scanning (and possibly temperature mechanical interaction but are actually physical (shock
increase), a concept that is generally ignored in the literature wave) or chemical (release of free radicals) effects. Table 1-29
dealing with thermal effects of ultrasound (Figure 1-4). summarizes nonthermal effects described in the literature
The issue of transducer heating, which may be par- in laboratory or animal experiments—and not in humans—
ticularly relevant in the first trimester, specifically if per- which may be pertinent to fetal ultrasound.
forming endovaginal scanning, is also often ignored.63,64 Investigations with laboratory animals clearly indicate
There are additional concerns in early gestation because that nonthermal interactions of ultrasound fields with tis-
of minimal or lack of perfusion. Only at about weeks sues can produce biological effects in vivo.71 It is interesting
10 to 11 does the embryonic circulation actually linkup
with the maternal circulation.65 There may thus be some  MAJOR NONTHERMAL EFFECTS
underestimation of the actual DUS-induced temperature OF ULTRASOUND OBSERVED
in early gestation, mainly because of the absence of perfu- IN THE LABORATORY AND
sion. The perfusion issue is in addition to modifications Table 1-2
IN ANIMALS AND WITH THE
of tissue temperature due to ambient maternal and fetal POTENTIAL TO AFFECT THE
temperatures. Furthermore, motions (even very small) FETUS
of the examiner’s hand as well as the patient’s breathing
and body movements (in the case of obstetric ultrasound, Free-radical generation
both the mother and the fetus) tend to spread through Increase in cell membrane permeability
the region being heated. However, for spectral (pulsed) Erythrocyte agglutination
Growth restriction (transient decrease)
Doppler studies, it is necessary to have the transducer as
DNA single-strand break
steady as possible. This is because, in general, blood ves- Increased sister chromatid exchange
sels are small in comparison to the general organ or body Increased mutation frequency
size being scanned with B-mode imaging, and hand move- Capillary petechiae
ments while performing Doppler studies will have more Vasoconstriction
undesired effects on the resulting image. As described Lung microvascular hemorrhage
earlier, the intensity (ISPTA) and acoustic power associated Intestine microvascular hemorrhage
with Doppler ultrasound are the highest of all the general- Neuronal migration delay
use categories. Ziskin66 reported that among 15,973 Dop- Auditory tract stimulation
pler ultrasound examinations, the average duration was 27 Tactile radiation pressure perception effect
Cardiac, premature contractions
minutes (and the longest 4 hours!).
There is a mathematical/physical relation between tem- Modified with permission from Stratmeyer ME, Greenleaf JF, Dalecki D, et al.
perature elevation and several beam characteristics. The Fetal ultrasound: mechanical effects. J Ultrasound Med. 2008 Apr;27(4):597-605.

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8 Part 1 GENERAL OBSTETRIC SONOGRAPHY

to note that chemical effects of ultrasound were described scientific evidence of potential effect, particularly in the first
more than 80 years ago!72 Cavitation seems to be the major trimester.93
factor in mechanical effects73 as it has been demonstrated to
occur in living tissues under ultrasound insonation.74,75 Two
types of cavitation can be described—stable and inertial THE OUTPUT DISPLAY STANDARD
(previously defined as transient)—both of which need the In 1992, the FDA yielded to pressure from ultrasound
presence of gas bubbles to occur. Stable cavitation indi- clinical users as well as manufacturers to increase the power
cates vibrations or small backward and forward move- output of instruments. The rationale for this request was
ments with possible resulting microstreaming. Inertial that higher outputs would generate better images, and thus
cavitation indicates expansion and reduction in volume, improve diagnostic accuracy. To allow clinical users of
secondary to alternating positive and negative pressures ultrasound to use their instruments at higher powers than
generated by the ultrasound wave. Expansion in growth is originally intended and to reflect the two major potential
less with each cycle until collapse occurs with production biological consequences of ultrasound (mechanical and
of very high pressure (hundreds of atmospheres) and very thermal, see above), the American Institute of Ultrasound
elevated temperature (thousands of degrees), but on such a in Medicine (AIUM), the National Electrical Manufacturers’
small area (less than 100 nm) and for such a brief time (few Association (NEMA), and the FDA (with representatives
tens of nanoseconds) that it will not be felt and is very hard from the Canadian Health Protection Branch, the National
to measure (adiabatic reaction—occurring without the gain Council on Radiation Protection and Measurements,94 and
or loss of heat) but can produce microstreaming—a phe- 14 other medical organizations30) developed a standard
nomenon that has been described also with no clear involve- related to the potential for ultrasound bioeffects. The full
ment of bubbles,76-78 or even release of free radicals.79,80 name was the Standard for Real-Time Display of Thermal
Acoustic streaming is easily demonstrated by watch-
and Mechanical Indices on Diagnostic Ultrasound Equip-
ing ultrasound-induced movements of solid-matter-
ment, generally known as the Output Display Standard
containing fluids in insonated cavities (see Video 1).
or ODS.15 The importance of this document and what it
Radiation torque refers to the induction, in objects describes is that it represents historically the first attempt
found in the acoustic field, of rotation or of the tendency at providing the end user with quantitative safety-related
to rotate. Biological effects of ultrasound in animals such as information. One important result is that the end users are
local intestinal,81 renal,82 and pulmonary83 hemorrhages have able to see how manipulation of the instrument controls
been attributed to mechanical effects, although cavitation during an examination causes alterations in the output and,
could not always be implicated. Furthermore, since gas bub- thus, on the exposure. As a consequence, for fetal imaging
bles do not seem to be present in fetal lungs or bowels (where the output, as expressed by the ISPTA, went from a previous
effects have been described in neonates or adult animals), the value of 92 to 720 mW/cm2 (see Table 1-1).
risk from mechanical effect secondary to cavitation appears To allow the output to reach such levels, the manufac-
to be minimal.84 There are several other effects that do not turers were requested to display, on screen and in real-time,
appear to involve cavitation such as tactile sensation of the two types of indices with the intent of making the user aware
ultrasound wave, auditory response, cell aggregation, and cell of the potential for bioeffects, as described earlier. These
membrane alteration. Hemolysis has also been reported.85 It indices are the thermal index (TI), to provide some indica-
seems, however, that the presence of some cavitation nuclei tion of potential temperature increase, and the mechanical
is necessary for hemolysis to occur. At present, there is no index (MI), to provide indication of potential for nonther-
clear clinical indication for the use of ultrasound contrast mal (ie, mechanical) effects15,30,95 (Figure 1-5). The TI is the
agents (a source of cavitation nuclei, when injected into the ratio of total acoustic power to the acoustic power estimated
body before ultrasound examination) in fetal ultrasound, and
to date, no studies have specifically investigated the interac-
tion of ultrasound and microbubble contrast agents in fetal
tissues in vivo. Nevertheless, it should be noted that in the
presence of such contrast agents, fetal red blood cells are
more susceptible to lysis from ultrasound exposure in vitro.86
Additionally, fetal stimulation caused by pulsed ultra-
sound insonation has been described, with no appar-
ent relation to cavitation.87 This effect may be secondary
to radiation forces associated with ultrasound exposures.
These forces were suspected at the earliest stages of ultra-
sound research88 and are known to possibly stimulate audi-
tory,89 sensory,90 and cardiac tissues.91 No harmful effects
of DUS, secondary to nonthermal mechanisms, have been
reported in human fetuses. A very intriguing nonthermal
effect of ultrasound is acceleration of bone fractures heal-
ing in animals and humans.92 Because of these known
effects of ultrasound in living tissues and the fact that pres-
sures involved with Doppler propagation are much higher
than B-mode, caution is further recommended, based on Figure 1-5. Onscreen TI (= 0.3, red arrow) and MI (= 1, yellow arrow).

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Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 9

to be required to increase tissue temperature by a maximum Furthermore, several assumptions were made, which
of 1°C. It is an estimate of the maximal temperature rise at prompts some questions on the clinical value of these
a given exposure. There are 3 variants: for soft tissue (TIS), indices. Maybe the most significant (from a clinical aspect)
to be used mostly in early pregnancy when ossification is is the choice of the homogeneous attenuation path model
low; for bones (TIB), to be used when the ultrasound beam (defined as the H3 model), with an attenuation coefficient
impinges on bone at or near the beam focus, such as late of 0.3 dB/cm/MHz, as detailed previously in Tissue Char-
second and third trimesters of pregnancy; and for transcra- acteristics. The reason to employ models of that nature is
nial studies (TIC) when the transducer is essentially against the impossibility, for obvious reasons, to perform certain
bone, mostly for examinations in adult patients, but also measurements in pregnant women. This coefficient may
in neonatal scanning, which is an area that is, generally, be an overestimation of the attenuation in many clinical
ignored. These indices were required to be displayed if equal scenarios, a situation that would underestimate the actual
to or over 0.4. It needs to be made very clear that TI does exposure. In National Council on Radiation Protection
not represent an actual or an assumed temperature increase. and Measurements (NCRP) report number 140,30 there is
It bears some correlation with temperature rise in degrees an entire chapter (Chapter 9) indicating conditions where
Celsius but in no way allows an estimate or a guess as to both indices may be inaccurate, eg, long fluid path (full
what that temperature change actually is in the tissue.95 bladder, amniotic fluid, ascites, or hydrocephalus) or path
The MI represents the potential for nonthermal damage in through increased amounts of soft tissue such as obese
tissues but is not based on actual in-situ measurements. It is patients. Because of these uncertainties, the accuracy of
a theoretical formulation of the ratio of the pressure to the the TI and MI may be within a factor of 2 or even 6.107 For
square root of the ultrasound frequency (hence, the higher example, an on-screen TI of 1 may correspond to an actual
the frequency, the lesser risk of mechanical effect). value of 0.5°C or 2°C if the error factor is 2, but possibly
Both the TI and MI can and should be followed as an 0.33°C or 6°C, if the error factor is 6 (as previously stated,
indication of change in output during the clinical examina- these are not actual temperature indications). A further
tion with higher values indicating the potential for higher disturbing and confusing element is that outputs reported
thermal and nonthermal effects than lower values. A clear by manufacturers are not necessarily equivalent to those
mandate in the ODS original document was education calculated in the laboratory.108
of the end user as a major part in the implementation of
the indices. Attempts have been made to educate the end Risk Assessment
users,96 but, unfortunately, this aspect of the ODS does not
seem to have succeeded as end users’ knowledge of bioef- Risk means the chance or the possibility of loss or bad
fects, safety, and output indices is found lacking.97,98 consequence. It refers to the possibility, with a certain
In a questionnaire that was distributed to ultra- degree of probability, of damage to health, environment,
sound end users (82% were obstetricians) attending review and objects, in combination with the nature and magni-
courses and hospital grand rounds, only 17.7% gave the tude of the damage.109 These are the 3 important charac-
correct answer of the definition of the TI, and only 3.8% teristics of risk: probability of occurrence, and nature and
described MI properly. Almost 80% of end users did not magnitude of harm. It has been, specifically, applied to the
know where to find the acoustic indices when various use of medical instruments.110 A complicating factor that
responses included the machine documentation, a text- makes definition and classification difficult is that the con-
book, a complicated calculation or in real time on the cept of risk means various things to different people. Age,
ultrasound monitor (the correct answer).97 Similar results background, education, morals, religion, and many other
were recorded in surveys abroad, performed in Europe, traits will direct this evaluation and not only the absolute
Asia, or the Middle East98,99,100,101 indicating that clini- possible result of the activity, putting the participant at
cal end users worldwide show poor knowledge regarding risk. For instance, in bungee jumping, rupture of the elas-
safety issues of ultrasound during pregnancy.102,103 More tic cord and subsequent death may be, indisputably, the
recently, knowledge of residents in obstetrics and gyne- worst possible outcome, but different people evaluate this
cology was also found to be grossly lacking 104 and, fur- and make decisions that are not necessarily based on this
thermore, similar results were obtained when surveying absolute result. Furthermore, the reason to take a possible
sonographers, with no difference in years of experience.105 risk has to be taken in consideration.
Compliance with the ALARA (as low as reasonably Two approaches are possible in risk evaluation: how
achievable) principle by practitioners seeking credential- much harm is acceptable to obtain the desired results
ing for nuchal translucency (NT) measurement between (risk-benefit ratio) or how much harm can be avoided by
11 and 14 weeks’ gestation was evaluated. Only 5% of the withholding the action or modifying it (the precautionary
providers used the correct TI type (TIb) at lower than 0.5 principle). The risk-benefit principle is what is almost
for all submitted images, 6% at lower than 0.7, and 12% at universally used in medicine to justify a medical diag-
1.0 or lower. A TI (TIb or TIs) higher than 1.0 was used nostic procedure (such as ultrasound) or a therapeutic
by 19.5% of the providers. Proficiency in NT measurement intervention. If the benefit to be obtained from the proce-
and educational background (physician or sonographer) dure in terms of diagnosis (ultrasound) or intervention (a
did not influence compliance with ALARA. The authors newly discovered and not yet commercialized cancer or
concluded that clinicians seeking credentialing in NT do AIDS drug, for instance) is deemed to be sufficient, then,
not demonstrate compliance with the recommended use even if this diagnostic or interventional procedure car-
of the TIb in monitoring acoustic output.106 ries some risks (recognized or presumed to be possible),

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10 Part 1 GENERAL OBSTETRIC SONOGRAPHY

the benefit overrides these risks, assuming the subject 1. There must be scientific uncertainty about nature of
understands those risks and is willing to take them. The harm, probability, magnitude, and causality (fulfilled
precautionary principle (PP) is a diametrically opposed by DUS).
ethical, political, and economic approach stating that if 2. Mere speculation is not enough to invoke the PP.
a certain action may cause severe damage to the public, Scientific analysis must have triggered the process
in the absence of a scientific consensus that harm would (also fulfilled by DUS).
not ensue, the burden of proof falls on those who would 3. Per definition, the PP deals with procedures with
advocate taking that action.111 This principle is much probability of unclear outcome, in that it is differ-
less familiar to the medical field, although “first do no ent from prevention or from risk-benefit assessment
harm” is its direct application, but it may be extremely where some clear knowledge or precise suspicion
relevant when considering safety and risks of a proce- exists, and where decision may be made to go ahead
dure, such as prenatal ultrasound. The concept origi- despite this risk by, for instance, taking additional
nated in the 19th century when John Snow, a London, measures to attempt and limit the danger. Clearly,
UK, physician, determined that cholera was due to the the ALARA principle is the exact application of this
extensive, common use of an unclean water supply and element121,122 (fulfilled by DUS).
recommended closing of this source of water, although it 4. In general, the PP applies to unacceptable (“serious,”
was the sole one in a large vicinity.112 This may have been “irreversible,” “global”) high levels of risk to large
the first epidemiological analysis of a disease. Although populations, present or future, local or distant123
the beginning of the PP was medical, it became a social (may not be the case for DUS).
idea in Germany in the 1930s as Vorsorge, “forecaring.” 5. One needs to intervene (not observe or procrasti-
This later became the Vorsorgeprinzip, the forecaring or nate) before damage has been demonstrated (eg, “do
precautionary principle, in West German environmental not perform DUS”).
law in the 1970s.113 The idea was adopted by decision and 6. The intervention must be proportional to the pos-
policy makers but, remarkably, much more extensively sible risk: indicating DUS may be acceptable but not
in Europe than in the United States. Some key concepts nonclinical use of DUS. A level of “zero risk” is prob-
in the original formulation were environmental harm to ably never attainable.
a population and responsibility: “When an activity raises
threats of harm to human health or the environment, Those who support the PP make the following very
precautionary measures should be taken even if some strong argument for precaution: serious damage may be
cause and effect relationships are not fully established caused if one uses a risk-based approach. A well-known
scientifically. In this context the proponent of an activity, example is what constitutes toxic levels of lead in paint.
rather than the public, should bear the burden of proof” As early as 1897, it was known that lead may be toxic, but
(the Wingspread Statement on the Precautionary Prin- at first the upper limit of safety for children was assumed
ciple114). From environmental research it spread to toxi- to be 60 μg/dL of blood, and this had terrible results. The
cology and was first applied only recently in the United “safe” level was reduced over the years to 40, then 20, then
States to a clinical medical field.115 However, several med- 10, which it is today, although some scientists feel that
ical mishaps clearly belong to the history of the develop- even 2 μ/dL may pose some risk.124 The basic conclusion of
ment of the PP—from the diethylstilbestrol debacle116 risk analysis with the PP is that measures against a possible
to the thalidomide tragedy.117 While referring mostly to risk should be taken (such as exposure avoidance) even if
environmental issues, such as global warming, the PP can the available evidence is weak (or maybe absent) regard-
certainly be extended to other medical activities (such ing the existence of that risk as a scientifically established
as diagnostic ultrasound) and be applied to individuals fact.125 In many European countries this “stop first then
(such as fetuses). The simple enunciation of the prin- study” approach (a clear application of the PP) has been
ciple, particularly in reference to diagnostic ultrasound adopted (particularly for chemicals). The exact opposite
in general, and entertainment ultrasound in particular, is is often true in the United States where something, once
that even if a particular action or procedure has not been introduced, has to be proven harmful by science before
proven to be harmful, it is better to avoid it so as not to being removed or forbidden. A major goal of the PP is to
take the risk until safety is established through clear, sci- help delineate (preferably quantitatively) the possibility
entific evidence, popularly expressed as “better safe than that some exposure is hazardous, even in cases where this
sorry.”118 This is also the basis of the Hippocratic Oath, is not established beyond reasonable doubt.126 The classi-
which includes the recommendation to first do no harm. cal statistical approach to hypothesis testing is unhelpful
A major difference with the risk-benefit principle is that because lack of significance can be due to either uninfor-
proponents of the PP believe that public action is neces- mative data or genuine lack of effect (type II error).127
sary if there is any evidence of likely or substantial harm, There are many critics of the PP because of the risk
however limited but plausible, and the burden of proof of exaggeration in caution and slowing down of scientific
is shifted from showing the presence of risk to demon- progress.128,129 A major issue is that the PP relies very heav-
strating its absence.119 As such, epidemiologic research ily on a single conjecture: prevention is better than cure.
on chronic diseases and the use of surrogates for human There is no scientific evidence for this. Furthermore, it
studies (eg, animal research or tissue cultures) have been may be true that, often, it is better to be “safe than sorry”
shown to be uncertain.120 There are several variations of and the primum non nocere (first do no harm) principle is
the PP, but all have some common key elements: a direct application of this, but preventative measures can

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Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 11

be long lasting and possibly incapacitating, whereas cures liver,156 resulting from ultrasound exposure of a few sec-
can be targeted and effective.128 What is more, no moral onds at 1 and 3 MHz, respectively. Other observed effects
opinion is formed of people when treating them, but if the include limb paralysis as a result of spinal cord injury in the
main focus is upon precaution, then it can be deemed mor- rat,157,158 as well as lesions in the liver, kidney, and testicles
ally wrong not to take preventative measures. The whole of rabbits.159 While some effects are likely due to mechani-
precaution approach is imbued with what may appear to cal influences, very high temperature elevations (much
many as an excessively moralistic tone and a “I am the higher than anything reachable with diagnostic ultra-
expert and therefore know what is best for you” attitude.130 sound) have also been observed and may be more directly
Furthermore, the probability of a problem occurring that involved with the tissue damage. Effects in muscles have
one tries to avoid has to be high (which does not apply, as been obtained, but with outputs much higher than those
far as we know, to ultrasound) and preventative measures usually generated in clinical studies,160 and so have intes-
have to be effective. Hence this approach may be adopted tinal81 and lung161 hemorrhages, also at acoustic pressures
with some restrictions and this is, in fact, exactly what well above those generated by ultrasound fields. These are
ALARA recommends.122 Most scientists and professional helpful in understanding the mechanisms involved with
organizations have recommended such a practice in clini- possible bioeffects of DUS. It should also be noted that
cal obstetrical ultrasound.131-133 some similar effects have also been demonstrated with
acoustic fields much closer to clinically pertinent ones, in
particular lung and intestinal hemorrhage.81 Several major
HISTORICAL RESEARCH clinical end points for bioeffects that could have direct
The first descriptions of ultrasound as an imaging mode relevance to human studies include fetal growth and birth
date from the 19th century.134 The French engineer Paul weight, effects on brain and CNS function, and change in
Langevin designed an ultrasound machine using Pierre hematological function, and these will be considered in
Curie’s principle of the piezoelectric effect. During World more detail. Decreased birth weight after prenatal expo-
War I, he attempted to use this instrument to detect sub- sure to ultrasound has been reported in the monkey162,163
marines through echo location (hence the later coined and the mouse,164,165 but not convincingly in the rat.166
term SONAR: Sound Navigation And Ranging). He also Therefore, clear species differences seem to exist,167 mak-
demonstrated that the waves produced by his machine ing it difficult to generalize, and even more difficult to
could kill small animals in an insonated water bath, and extrapolate, to humans.
could cause pain to his assistants when they were required Tarantal and Hendrickx162 evaluated 30 pregnancies
to plunge their hands in the water bath in the path of the in monkeys, half of which were exposed to ultrasound.
beam. Other bioeffects observed included the searing of The scanned fetuses had lower birth weights and were
skin when touching a resonant quartz bar, and explosive shorter than the control group. No significant differences
atomization (!) of fluid drops from the end of the rod. Since were noted between the groups with regard to the rate of
that time, the question of effects and safety has been on abortions, major malformations, or stillbirths. Moreover,
the minds of researchers88 and has given rise to literature all showed catch-up growth when examined at 3 months
too extensive to review in detail.2,3,6,49,131,135-147 Initially, cell of age.162 It should be noted that in-situ intensities were
suspensions and cell and tissue cultures were employed, higher than what is considered routine in clinical obstet-
and many reports described clear effects of the ultrasound rical imaging in humans. Hande and Devi168 evaluated
waves on these, mostly secondary to cavitational and the effect of prenatal exposure to diagnostic ultrasound
other nonthermal mechanisms, such as cell aggregation,148 on the development of mice. Swiss albino mice were
membrane damage,149 and cell lysis.150 Plants were another exposed to diagnostic ultrasound for 10 minutes on day
extensively studied organism for effects of ultrasound,151 3.5 (preimplantation period), 6.5 (early organogenesis
particularly the Elodea leaf, since internal gas channels period), or 11.5 (late organogenesis period) of gestation.
are present.152 Insects have been exposed to ultrasound Sham-exposed controls were maintained for comparison.
with significant effects, such as death of eggs and larvae as Fetuses were dissected out on the 18th day of gestation,
well as abnormal development, presumably secondary to and changes in total mortality, body weight, body length,
the presence of gas-filled channels.153 Additionally, altera- head length, brain weight, sex ratio, and microphthalmia
tions at the chromosomal and even DNA levels have been were recorded. Exposure on day 3.5 of gestation resulted
described.154 These effects have been reviewed extensively in a small increase in the resorption rate and a significant
elsewhere,5,30 and while they are of major scientific and reduction in fetal body weight. Low fetal weight and an
historical importance, they are not of major relevance to increase in the incidence of intrauterine growth-restriction
clinical exposure of human fetuses. were produced by exposure on day 6.5 postcoitus.168
Others have also demonstrated restricted growth
in newborns after in utero exposure to DUS.169 Subtler
Animal Research
findings have also been described. Pregnant Swiss albino
Effects of ultrasound were demonstrated in animals more mice were exposed to diagnostic ultrasound (3.5 MHz, 65
than 80 years ago.88 Since then, multiple studies have mW, ISPTP = 1 W/cm2, ISATA = 240 W/cm2) for 10, 20, or
been performed with ultrasound on a wide variety of 30 minutes on day 14.5 (fetal period) of gestation.170 Sham-
species. Studies of gross effects on the brain and liver of exposed controls were studied for comparison. There were
cats were first performed with well-defined lesions and significant alterations in behavior in the exposed groups as
demyelination in the brain155 and tissue damage in the revealed by decreased locomotor and exploratory activity,

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12 Part 1 GENERAL OBSTETRIC SONOGRAPHY

and an increase in the number of trials needed for learn- further research in larger and slower-developing brains of
ing. No changes were observed in physiological reflexes nonhuman primates and continued scrutiny of unneces-
and postnatal survival. The authors concluded that ultra- sarily long prenatal ultrasound exposure is warranted. It
sound exposure during the early fetal period can impair is unclear whether a relatively small misplacement in a
brain function in the adult mouse.170 Likewise, Hande relatively small number of cells that retain their origin cell
et al171 found that anxiolytic activity and latency in learn- class is of any clinical significance. It is also important to
ing were more noticeable in ultrasound-treated animals. note that there are several major differences between the
The authors exposed pregnant Swiss mice to diagnostic experimental setup of Ang et al172 and the clinical use of
levels of ultrasound (3.5 MHz, maximum acoustic out- ultrasound in humans.6 The most noticeable difference
put: ISPTP = 1 W/cm2 and ISATA = 240 mW/cm2, acoustic was the length of exposure of up to 7 hours in the setup of
power = 65 mW) for 10 minutes on postcoital day 11.5 Ang et al. No real mechanistic explanation was given for
or 14.5. At 3 and 6 months postpartum, offspring were the findings, and furthermore, there was no real dose effect
subjected to behavioral tests. The effect was more pro- with high effects at the penultimate high dose, but less so
nounced in the 14.5 days postcoital group than in the at the highest dose. Moreover, scans were performed over
11.5 days group. They concluded that exposure to diag- a small period of several days. The experimental setup was
nostic ultrasound during late organogenesis period or such that embryos received whole-brain exposure to the
early fetal period in mice may cause changes in postna- beam, which is rare in humans, although quite possible in
tal behavior.171 Temperature elevations were induced by the earliest stages of gestation. In addition, brains of mice
ultrasound in guinea pig fetal brains.46 In fact, mean tem- are much smaller than those in humans, and develop over
perature increases of 4.9°C close to parietal bone and 1.2°C days. This should not completely deter from the study,
in the midbrain were recorded after 2-minute exposures, but encourages caution. It should be noted that some have
albeit at exposure conditions higher than what is usually described a complete lack of effects of prenatal ultrasound
employed in clinical examinations.46 This greatest temper- exposure on postnatal development and growth173 or
ature rise recorded close to the skull correlated with both behavior.174 The influence of prenatal ultrasound exposure
gestational age and progression in bone development.43 on the blood–brain barrier (BBB) integrity as measured by
The skull bone becomes progressively thicker and denser the permeation of Evans blue (EB) through the BBB during
between 30 and 60 days’ gestational age (normal gesta- the postnatal development of 139 rats was evaluated by
tion for guinea pigs is 66 to 68 days). After only 2 minutes Yang et al.175 Diagnostic levels of ultrasound (2.89 MHz,
of insonation with an ISPTA of 2.9 W/cm2 (about 4 times mechanical index = 1.1, acoustic output power = 70.5 mW)
higher than currently permitted by the FDA for diagnostic for 1 and 2 hours per day, for 9 consecutive days were used
use), mean maximum temperature increases varied from on Sprague-Dawley rats. Offspring were assessed postna-
1.2°C at 30 days to 5.2°C at 60 days. It is important to note tally on days 10, 17, 24, and 38. A statistically significant
that most of the heating (80% of the mean maximum tem- amount of EB extravasation into the cerebrum and cer-
perature increase) occurred within 40 seconds. The rate of ebellum could be detected on postnatal day 10 (but not
heating is relevant to the safety of clinical examinations in later), following exposure to diagnostic levels of ultrasound
which the dwell time may be an important factor. Because during embryonic development. The authors concluded
maximal ultrasound-induced temperature increase occurs there is a need for further investigation of the effects of
in the fetal brain near bone, worst-case heating will occur ultrasound exposure during the potentially vulnerable
later in pregnancy, when the ultrasound beam impinges on period of intense BBB development in the human fetus.
bone, and less will occur earlier in pregnancy, when bone is This study did not provide clear evidence that there is
less mineralized. However, milder insults early in gestation cause for concern for clinical prenatal diagnostic imaging
may be as significant (or more) than more severe ones in in humans. The study had several methodological flaws,
later stages. and specifically, the acoustic exposure was intense and
Neurons of the cerebral neocortex in mammals, includ- untranslatable to clinical practice.176
ing humans, are generated during fetal life in the brain pro- In another study177 chick brains were exposed, in ovo,
liferative zones and then migrate to their final destinations on day 19 of a 21-day incubation period to B-mode (5 or
by following an inside-to-outside sequence. Ang et al172 10 minutes), or to pulsed Doppler (1, 2, 3, 4, or 5 minutes)
evaluated the effect of ultrasound waves on neuronal ultrasound. After hatching, learning and memory function
positioning within the embryonic cerebral cortex in mice. were assessed at day 2 post hatch. B-mode exposure did
Neurons generated at embryonic day 16 and destined not affect memory function. However, significant memory
for the superficial cortical layers were chemically labeled impairment occurred following 4 and 5 minutes of pulsed
in over 335 animals. A small, but statistically significant, Doppler exposure. Short-, intermediate-, and long-term
number of neurons failed to acquire their proper position memory was equally impaired, suggesting an inability
and remained scattered within inappropriate cortical lay- to learn. Chicks were also unable to learn with a second
ers and/or in the subjacent white matter when exposed to training session. In this study, exposure to pulsed Doppler
ultrasound for a total of 30 minutes or longer during the ultrasound adversely affected cognitive function in chicks.
period of their migration. The magnitude of dispersion of Although some methodological issues exist and extrapo-
labeled neurons was variable but systematically increased lation to humans is unwarranted, these findings justify
with duration of exposure to ultrasound (although not further investigations.
linearly, with some extended exposure yielding less effect The hematological system is the second major system
than lower ones). These investigators concluded that to be investigated for ultrasound effects. The following have

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Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 13

been assessed: hemolysis, coagulation factors and platelets, In a later study, the authors concluded that the relation-
and leukocyte production and function.178 Increased hemo- ship of ultrasound exposure and reduced birth weight may
lysis has been demonstrated for ultrasound in (human) be due to shared common risk factors, which lead to both
fetal cells as compared to adult cells, but only in the pres- exposure and a reduction in birth weight.190 Another ret-
ence of ultrasound contrast agents, with human cells being rospective study, with Moore as a coauthor, reported a 2.0
less fragile than certain tested animals.86,179 Other altera- greater risk of low birth weight after 4 or more exposures to
tions have been described in the hemolytic system180 but diagnostic ultrasound.144 These results were not reproduced
appear to be of minimal, if any, clinical significance. in other retrospective studies.189 In a large study (originally
10,000 pregnancies exposed to ultrasound matched with
500 controls) with a 6-year follow-up, Lyons et al191 did not
Human Research and Epidemiology
find differences in birth weight (nor increased congenital
In 2005, the American Institute of Ultrasound in Medicine malformations, chromosomal abnormalities, infant neo-
(AIUM) published the following statement: “Based on the plasms, speech or hearing impairment, or developmental
epidemiological data available and on current knowledge problems).
of interactive mechanisms, there is insufficient justification Newnham et al192 performed a randomized control
to warrant a conclusion of a causal relationship between trial including more than 2800 parturients. Of these,
diagnostic ultrasound and recognized adverse effects in about half received 5 ultrasound imaging and Doppler
humans. Some studies have reported effects of exposure to flow studies at 18, 24, 28, 34, and 38 weeks’ gestation, and
diagnostic ultrasound during pregnancy, such as low birth half received a single ultrasound imaging at 18 weeks.
weight, delayed speech, dyslexia, and non–right-handed- They found an increased risk of IUGR when exposed
ness. Other studies have not demonstrated such effects. to frequent Doppler examinations, possibly via some
The epidemiological evidence is based on exposure condi- effects on bone growth. However, when children from
tions prior to 1992, the year in which acoustic limits of the previously mentioned study were examined at 1 year
ultrasound machines were substantially increased for fetal/ of age, there were no differences between the study and
obstetrical applications.”181 Applied to ultrasound, epide- control groups. In addition, after examining their original
miology is the study of effects on human populations as a subjects after 8 years, no evidence of long-term adverse
result of ultrasound scanning and, in the case of obstetri- impact in neurological outcome was noted by the same
cal ultrasound, this should include the pregnant patient as group.192 Similarly, no harmful effect of a single or 2 pre-
well as her infant. Laboratory animal experiments under natal scans on growth were found in several randomized
similar diagnostic exposure levels have shown some effects studies.193,194 In fact, in some studies, birth weight was
from ultrasound, under certain conditions. Effects have slightly higher in the scanned group, but not significantly
also been reported in humans, but a definitive statement so, except in one.195 In conclusion, decreased birth weight
regarding risk should, ideally, include direct analysis of has been extensively analyzed after DUS exposure in
the effects in human populations. Several epidemiologi- utero, and it does not appear that such exposure is associ-
cal studies have been published.4,49,182 For an extensive ated with reduced birth weight, although Doppler expo-
discussion, including elements of statistics, see Chapter sure may have some risks.147 In a few studies that appear
12 in NCRP report number 140,30 an extensive review by to favor such an effect, a major problem is that there is
Newnham,143 and AIUM document, Conclusions Regard- an important confounding factor: many studies include
ing Epidemiology for Obstetric Ultrasound.183,184. Relevant pregnancies at risk for IUGR due to existing maternal or
details will be summarized. fetal conditions.
Several biological end points have been analyzed in the A second major potential effect extensively evaluated
human fetus/neonate in an attempt to determine whether is delayed speech. In an attempt to determine if there is
prenatal exposure to diagnostic ultrasound had observ- an association between prenatal ultrasound exposure and
able effects: intrauterine growth restriction (IUGR) and delayed speech in children, Campbell et al185 studied 72
low birth weight, delayed speech, dyslexia, neurological children with delayed speech and found a higher rate of
and mental development or behavioral issues, and, more ultrasound exposure in utero than the 144 control sub-
recently, non–right-handedness. Occasional studies report jects. Some issues render these results less valid: there
an association between diagnostic ultrasound and some was neither a dose-response effect nor any relationship to
specific abnormalities such as lower birth weight,182 delayed time of exposure, and many of the records were more than
speech,185 dyslexia,186 and non–right-handedness.187,188 5 years old. Another study of over 1100 children exposed
With the exception of low birth weight (also demonstrated to ultrasound in utero and over 1000 controls found no
in monkeys,179) these findings have never been duplicated, significant differences in delayed speech, limited vocabu-
and the majority of studies have been negative for any asso- lary, or stuttering.196
ciation. Moore et al189 examined a large number of infants Dyslexia is another widely studied subject. In one study
(over 2000, half of them exposed to ultrasound) and found a over 4000 children, aged 7 to 12, exposed to ultrasound in
small but statistically significant lower mean birth weight of utero were used as a study group and compared to matched
exposed versus nonexposed infants. However, information controls to evaluate the appearance of adverse effects.186
was collected several years after exposure, no indications for Seventeen outcomes measures were examined, at birth
the examination are known, and no exposure information is (APGAR scores, gestational age, head circumference, birth
available. This lack of detail about the exposure parameters weight, length, congenital abnormalities, neonatal infection,
is, very often, the major problem in analyzing these reports. and congenital infection) or in early infancy (hearing, visual

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14 Part 1 GENERAL OBSTETRIC SONOGRAPHY

acuity and color vision, cognitive function, and behavior). populations scanned after 1992, when regulations were
No significant differences were found, except for a sig- altered and acoustic output of diagnostic instruments
nificantly greater proportion of dyslexia in those children were permitted to reach levels many times higher than
exposed to ultrasound. The authors, however, indicated previously allowed (from 94 to 720 mW/cm2 ISPTA for fetal
that this could be an incidental finding, given the design applications). There are no epidemiological studies related
of the study and the presence of several confounding fac- to the output display standard (thermal and mechanical
tors that could have contributed to the possible dyslexia indices) and clinical outcomes. The safety of new technolo-
finding. On the other hand, it should be noted that expo- gies such as harmonic imaging and three-dimensional (3D)
sure conditions were probably much lower than modern ultrasound, as well as that of probe self-heating, needs to
ultrasound systems, given that the fetal examinations were be investigated.
performed from 1968 to 1972. Subsequently, a long-term
follow-up study was performed on over 2100 children.193,197 Clinical Exposimetry
End points included evaluation for dyslexia along with
additional hypotheses, including an examination of non– There is, unfortunately, no way to perform actual sono-
right-handedness said to be associated with dyslexia. These graphic exposure measurements in the human fetus. Pres-
studies198-200 included the specific examination of more than sure, intensity, and power are not measured in situ, but
600 children with various tests for dyslexia such as spelling are estimated from laboratory obtained measurements.
and reading. No statistically significant differences were Several tissue models have been developed to help with
found between ultrasound-exposed children and controls this estimation, depending mostly on approximate attenu-
for reading, spelling, arithmetic, or overall performance as ation coefficients for various tissues or beam paths.30,50 A
reported by teachers. Specific dyslexia tests showed similar large range of variation is expected secondary to individual
rates of occurrence among scanned children and controls patient characteristics, such as weight and thickness of tis-
in reading, spelling, and intelligence scores, and no discrep- sues.206 Because of these possible variations, the reasonable
ancy between intelligence and reading or spelling. Since the worst-case scenario is usually considered. There are scarce
original finding of dyslexia was not confirmed in subsequent data on instruments’ acoustic output (nor patient acous-
randomized controlled trials, it is considered unlikely that tic exposure) for routine clinical ultrasound examina-
routine ultrasound screening exams can cause dyslexia. tions. Acoustic output was recorded in several prospective
However, these studies did raise the issue of laterality (in observational studies investigating first-trimester ultra-
terms of handedness). sound,207,208 Doppler studies,209 and 3D/four-dimensional
The topic of non–right-handedness as a result of pre- (4D) studies.210 Basically, first-trimester ultrasound was
natal exposure has caused much ink to be used in extensive associated with very low TI values (with a mean of 0.2 ±
discussions and reports. The first report of a possible link 0.1).207 The TI was significantly higher in the pulsed wave
between prenatal exposure to ultrasound and subsequent Doppler (mean 1.5 ± 0.5, range 0.9-2.8) and color flow
non–right-handedness in insonated children was published imaging studies (mean 0.8 ± 0.1, range 0.6-1.2) as com-
in 1993 by Salvesen et al,198 but according to the authors, pared to B-mode ultrasound (mean 0.3 ± 0.1, range 0.1-0.7;
“only barely significant at the 5% level.” In a later analysis of P < .01).209 In the same study, TI was above 1.5 in 43% of
the data, they described that the association was restricted to the Doppler studies.209 Mean TI during the 3D (0.27 ± 0.1)
males.193 A second group of researchers (with Salvesen, the and 4D examinations (0.24 ± 0.1) was comparable to the TI
main author of the first study, included but with a new popu- during the B-mode scanning (0.28 ± 0.1; P = .343).210 There
lation, in Sweden as opposed to Norway) published similar is ever-increasing use of 3D/4D ultrasound in clinical
findings of a statistically significant association between
ultrasound exposure in utero and non–right-handedness in
males.187 Salvesen then published a meta-analysis of these 2
studies and of previously unreported results.188 No difference
was found in general, but a small increase in non–right-
handedness was present when analyzing boys separately.
No valid mechanistic explanation is given in the studies to
explain the findings. In conclusion, although there may be a
small increase in the incidence of non–right-handedness in
male infants, there is not enough evidence to infer a direct
effect on brain structure or function or even that non–right-
handedness is an adverse effect. An intriguing recent study
showed that fetuses self-touched their faces more often with
the left hand than the right, as observed by ultrasound, in
correlation to stress levels of the mother.189 Furthermore, lat-
erality is, mostly, genetically determined.190 Other end points
that have been considered but not found to be associated
with ultrasound exposure include congenital malformations,
hearing problems and malignancies.204,205
There has been no published epidemiological study Figure 1-6. TI and MI during M-mode examination. Please note
that found negative effects of obstetrics ultrasound in TI = 0.8 (arrow).

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Chapter 1 Ultrasound Bioeffects and Safety: What the Practitioner Should Know 15

Figure 1-7. TI and MI during color Doppler exam. Please note TI = 0.6 Figure 1-8. TI and MI during spectral Doppler examination. Please
(arrow). note TI = 2.4 (arrow).

medicine, thus knowledge about bioeffects and safety is from Bioeffects and Safety Committees of various profes-
mandatory.211 Figures 1-6 through 1-9 are examples of sional organizations (American Institute of Ultrasound
actual screen shots during clinical exams, for M-mode, in Medicine-AIUM, European Federation of Ultrasound
color Doppler, spectral Doppler, and 3D acquisition, in Medicine and Biology-EFSUMB, International Society
respectively. Figure 1-10 demonstrates that extremely for Ultrasound in Obstetrics and Gynecology-ISUOG,
elevated TIs are easily reachable with spectral Doppler, and World Federation for Ultrasound in Medicine and
although in manufacturer’s fetal setting. Biology-WFUMB), several manufacturers have changed
Adequate diagnostic information may be obtained their default settings, specifically for pulsed Doppler in
with low output levels (as documented by values of the fetal mode, from very high (as it was originally, presumably
TI). This is seen in Figure 1-11 and Video 1. This has in an attempt to obtain better images) to very low, with
been reported in the literature, specifically for Doppler, the end user capable or raising the output, if desired. Since
the mode with the highest output, both in early and later acoustic output is high in Doppler, special precaution is
pregnancy.212,213 It should be noted that, under pressure recommended, particularly in early gestation.214

Figure 1-9. TI and MI during multiplanar acquisition in 3D scanning. Please note TI = 0.4 (arrow).

Fleischer_CH01_p001-p024.indd 15 08/09/17 10:50 am


16 Part 1 GENERAL OBSTETRIC SONOGRAPHY

Because of the possible errors inherent in the calcula-


tion of the TI and MI, various attempts have been made to
find a better quantification of the potential risk.215 These
have not been adopted by the clinical community.
The other side of the equation is, “What are we looking
for?” Ultrasound is neither radiation nor thalidomide, and
it is certain that ultrasound does not kill fetuses, does not
cause limb amputations, and does not cause gross structural
anomalies.216 But are we looking where we should, and have
we studied enough cases in a scientific fashion, looking at
subtle changes? The answer is clearly, “No.” We have been
looking for macroscopic, gross findings and have not found
any, but is it possible that harmful effects of ultrasound
have been missed because the wrong time frame refer-
ence was used? Two possible factors are described for such
errors.217 If one uses a term human pregnancy (280 days
[40 weeks]) to life expectancy of 70 years (25,550 days) ratio,
Figure 1-10. Second-trimester spectral Doppler. Please note TI = 3.3 then 7 in utero days are comparable to about 631 ex-utero
(arrow). This is with the instrument on “fetal” setting. days. Therefore, it is conceivable that a much shorter time
interval (1 day) should be used to group fetuses to evaluate

A B

C D
Figure 1-11. Color and spectral Doppler of umbilical artery. A: Color Doppler with high output power (as reflected by TI = 0.7). B: Lower output
power (TI = 0.1). C: Spectral Doppler with high output power (as reflected by TI = 2.4). D: Lower output power (TI = 0.6). Image is equally diagnostic.

Fleischer_CH01_p001-p024.indd 16 08/09/17 10:51 am


Another random document with
no related content on Scribd:
be in the Scheldt, struggling in his gun-boat against a gale which, in
spite of all his endeavors and seamanship, drove him ashore, under
the guns of the Belgians. A crowd of Belgian volunteers leaped
aboard, ordered him to haul down his colors and surrender. Von
Speyk hurried below to the magazine, fell upon his knees in prayer,
flung a lighted cigar into an open barrel of powder, and blew his ship
to atoms, with nearly all who were on board. If he, by this sacrifice,
prevented a Dutch vessel from falling into the enemy’s power, he
also deprived Holland of many good seamen. The latter country,
however, only thought of the unselfish act of heroism, in one who
had been gratuitously educated in the orphan house at Amsterdam,
and who acquitted his debt to his country, by laying down his life
when such sacrifice was worth making. His king and countrymen
proved that they could appreciate the noble act. The statue of Von
Speyk was placed by the side of that of De Ruyter, and the
government decreed that as long as a Dutch navy existed there
should be one vessel bearing the name of Von Speyk.
To return to the knights of earlier days, I will observe that indifferent
as many of them were to meeting death, they, and indeed other men
of note, were very far from being so as to the manner in which they
should be disposed of after death. In their stone or marble coffins,
they lay in graves so shallow that the cover of the coffin formed part
of the pavement of the church. Whittingham, the Puritan Dean of
Durham, took up many of their coffins and converted them into horse
or swine troughs. This is the dean who is said to have turned the
finely-wrought holy-water vessels into salting-tubs for his own use.
Modern knights have had other cares about their graves than that
alluded to above. Sir William Browne, for instance, one of George
II.’s knights, and a medical man of some repute, who died in 1770,
ordered by his will that when his coffin was lowered into the grave,
there should be placed upon it, “in its leathern case or coffin, my
pocket Elzevir Horace, comes viæ vitæque dulcis et utilis, worn out
with and by me.” There was nothing more unreasonable in this than
in a warrior-knight being buried with all his weapons around him.
And, with respect to warrior-knights and what was done with them
after death, I know nothing more curious than what is told us by
Stavely on the authority of Streder. I will give it in the author’s own
words.
“Don John of Austria,” says Stavely, “governor of the Netherlands for
Philip II. of Spain, dying at his camp at Buge” (Bouges, a mile from
Namur), “was carried from thence to the great church at Havre,
where his funeral was solemnized and a monument to posterity
erected for him there by Alexander Farnese, the Prince of Parma.
Afterward his body was taken to pieces, and the bones, packed in
mails, were privately carried into Spain, where, being set together
with small wires, the body was rejointed again, which being filled or
stuffed with cotton, and richly habited, Don John was presented to
the King, entire, leaning upon his commander’s staff, and looking as
if he were alive and breathing. Afterward the corpse being carried to
the Church of St. Laurence, at the Escurial, was there buried near
his father, Charles V., with a fitting monument erected for him.”
Considering that there was, and is, a suspicion that Philip II. had
poisoned his kinsman, the interview must have been a startling one.
But Philip II. was not, perhaps, so afraid of dead men as the fourth
Spanish king of that name. Philip IV., by no means an unknightly
monarch, was born on a Good Friday, and as there is a Spanish
superstition that they who are born on that day see ghosts whenever
they pass the place where any one has been killed or buried, who
died a violent death, this king fell into a habit of carrying his head so
high, in order to avoid seeing those spirits, that his nose was
continually en l’air, and he appeared to see nobody.
Romance, and perhaps faithful history, are full of details of the
becoming deaths of ancient knights, upon the field. I question,
however, if even Sir Philip Sidney’s was more dignified than that of a
soldier of the 58th infantry, recorded in Nichols’s “Anecdotes of the
Eighteenth Century.” A straggling shot had struck him in the
stomach. As he was too dreadfully wounded to be removed, he
desired his comrades would pray by him, and the whole guard knelt
round him in prayer till he died. Bishop Hurd remarked, when this
was told him, that “it was true religion.” There was more of religion in
such sympathy than there was of taste in the condolence of Alnwick,
on the death of Hugh, Duke of Northumberland—a rather irascible
officer, and Knight of the Garter. “O,” cried the Alnwick poet—

“O rueful sight! Behold, how lost to sense


The millions stand, suspended by suspense!”

But all fruitlessly were the millions so suspended, for as the minstrel
remarked in his Threnodia—

“When Time shall yield to Death, Dukes must obey.”

“Dying in harness,” is a favorite phrase in chivalric annals to illustrate


the bravery of a knight falling in battle, “clothed in complete steel.”
So to die, however, was not always to die in a fray. Hume says of
Seward, Earl of Northumberland, that there are two circumstances
related of him, “which discover his high sense of honor and martial
disposition. When intelligence was brought to him of his son
Osborne’s death, he was inconsolable till he heard the wound was
received on his breast, and that he had behaved with great gallantry
in the action. When he found his own death approaching, he ordered
his servants to dress him in a complete suit of armor, and sitting
erect on the couch, with a spear in his hand, declared that in that
position, the only one worthy of a warrior, he would patiently await
the fatal moment.”

See how the chief of many a field


Prepares to give his latest breath;
And, like a well-trimmed warrior, yield
Becomingly t’impending death—
That one, stern conqueror of all,
Of chieftain in embattled tower,
Of lord within his ancient hall,
And maiden in her trellised bower.

To meet that surest of all foes,


From off his soft and pillowed bed,
With dignity old Seward rose,
And to a couch of state was led.
Fainting, yet firm of purpose there,
Stately as monarch on his throne,
Upright he sat, with kingly air,
To meet the coming foe, alone.

“Take from these limbs,” he weakly cried,


“This soft and womanish attire;
Let cloak and cap be laid aside—
Seward will die as died his sire:
Not clad in silken vest and shirt,
Like princes in a fairy tale;
With iron be these old limbs girt—
My vest of steel, my shirt of mail.

“Close let my sheaf of arrows stand;


My mighty battle-axe now bring;
My ashen spear place in my hand;
Around my neck my buckler sling.
Let my white locks once more be pressed
By the old cap of Milan steel;
Such soldier’s gear becomes them best—
They love their old defence to feel.

“’Tis well! Now buckle to my waist


My well-tried gleaming blade of Spain
My old blood leaps in joyful haste
To feel it on my thigh again.
And here this pendent loop upon,
Suspend my father’s dagger bright;
My spurs of gold, too, buckle on—
Or Seward dies not like a knight.”

’Twas done. No tear bedimmed his eyes—


His manly heart had ne’er known fear;
It answered not the deep-fetched sighs
Of friends and comrades standing near.
Death was upon him: that grim foe
Who smites the craven as the brave.
With patience Seward met the blow—
Prepared and willing for the grave.

The manner of the death, or rather of the dying of Seward, Earl of


Northumberland, was in part, unconsciously, imitated by the great
Mansfeldt. When the career of the latter was nearly at its close, his
fragile frame was already worn out by excess of action—his once
stout soul irritated by disappointment, and his former vigorous
constitution shattered by the ravages of a disease which had long
preyed on it in secret. The erst gallant knight lay helpless in the
miserable village of Zara, in Dalmatia. As he found his last moment
drawing near, he put on one of his richest uniforms, and girded his
favorite sword to his side. It was the one he most constantly carried
in battle. Thus accoutred, he summoned his chief officers to attend
him. He was held up by the two whom he most wished to distinguish,
because of their unwavering fidelity. Thus upheld, he exhorted all to
go on, unwearied, in the path of glory; and, living or dying, never to
bate a breath of inveterate hatred for Austria—whose government
has been accursed in all time, since there has been an Austria, for
its unmitigated infamy. “With the indifference of a man preparing for a
journey of no extraordinary importance,” thus speaks Naylor, when
describing the scene, “he continued tranquilly to converse with his
friends to the latest moment of his existence. His body was interred
with military pomp at Spalatio, in Dalmatia, at the expense of the
Venetians. Thus was the emperor delivered from an enemy who,
though often defeated, never ceased to be formidable; and whose
transcendent genius was so fertile in resources, that, without the
smallest funds to support the expenses of war, he maintained an
honorable contest during seven campaigns against the most
powerful monarchs in Europe.”

His hour at length is come:


The hero of a hundred fields,
Who never yielded, only yields
To Him who rules the tomb.

He whose loud trumpet’s blast,


Carried upon the trembling gale
The voice of death o’er hill and dale,
Is struck himself at last.

The same who, but of late,


Serenely saw destruction hurled,
And slaughter sweeping through the world,
Serenely meets his fate.
The spirit of the brave,
That led him o’er the embattled plain
’Gainst lines of foes, o’er countless slain,
Waits on him to the grave.

And with his latest breath


The warrior dons his proud array,
Prepared to meet, and to obey,
His last commander—Death!

The mournful tears and sighs


Fall not for him who, like the swan,
Wears his best plumes, sings sweetly on,
Sounds his last song—and dies!

With regard to the burial of knights, we may observe that, down to a


comparatively late period the knights and barons of England were
buried with much solemn splendor. At the obsequies of a baron,
there was an official present who wore the armor of the defunct,
mounted a horse in full trappings, and carried the banner, shield, and
helmet, of the deceased. So, in Henry the Eighth’s time, Lord William
Courtney was buried with the ceremonies observed at the funeral of
an earl, to which rank it had been the king’s intention to elevate him.
On this occasion Sir Edmund Carew, a gallant knight, rode into the
church in full armor, with the point of his battle-axe downward—a
token, like a reversed torch, of death.
The latest instance I have met with of a union of ancient and modern
customs at the burial of a knight, occurred at Treves, in 1781, at the
interment of the Teutonic knight, General Frederick Casimir. This
gallant soldier’s charger was led to the brink of the grave in which
the body had just been deposited; the throat of the steed was swiftly
cut by an official, and the carcass of the horse was flung down upon
the coffin of the knight. Such sacrifices were once common enough.
At the funerals in England of cavalry soldiers, or of mounted officers,
the horse is still processionally conducted to the brink of the grave,
but we are too wisely economical to leave him there, or to fling him
into it.
Where chivalry had great perils and temptations, we need not be
surprised to find that there were many scions of noble houses who
either declined to win spurs by encountering mortal danger, or who
soon grew weary of making the attempt. Let us, then, consider the
unambitious gentlemen who grew “tired of it.”
THE KNIGHTS WHO GREW “TIRED OF IT.”
“How blest are they that waste their weary hours
In solemn groves and solitary bower
Where neither eye nor ear
Can see or hear
The frantic mirth
And false delights of frolic earth;
Where they may sit and pant,
And breathe their pursy souls;
Where neither grief consumes, nor griping want
Afflicts, nor sullen care controls!
Away false joys! Ye murder where ye kiss;
There is no heaven to that, no life to this.”
Francis Quarles.

As marriage or the cloister was the alternative submitted to most


ladies in the days of old, so young men of noble families had small
choice but between the church and chivalry. Some, indeed,
commenced with arms, won knightly honors, cared nothing for them
when they had obtained the prize, and took up the clerical
profession, or entered monasteries. There are many distinguished
examples. There was first St. Mochua or Cluanus, who, after serving
in arms with great distinction, entered a monastery and took to
building churches and establishing cities. Of the former he built no
less than thirty; and he passed as many years in one church as he
had built of churches themselves. He was the founder of one
hundred and twenty cells. He is to be looked upon with respect. Old
warriors in our own days are often moved by the same impulse
which governed Mochua; and when we see retired admirals taking
the chair at meetings where Dr. Cumming is about to exhibit; or
infirm major-generals supporting, with unabated mental energy, their
so-called Puseyite pastors, we only look upon men who, acting
conscientiously, are worthy of respect, and are such Mochuas as
modern times and circumstances will admit of.
We have another example in Adelard, the cousin of Charlemagne.
He was a gay and gallant chevalier at his imperial cousin’s court,
and there was no stouter wielder of a sword in all the army; but
Alard, or Adelard, grew weary of camp and court alike. He fled from
some very pretty temptations in the one, as well as great perils in the
other. The young prince, he was only twenty, took the monastic habit
at Corbie, where he was employed as a gardener, and spoiled
cartloads of vegetables before he got his hand and his thoughts to
his new profession. He was occasionally busy too in the kitchen, but
not to the visible gratification of the monks. Charlemagne often
insisted on his appearing at court, where at last he held one or two
high offices; and, when he left, wrote a book for the guidance of
courtiers generally, by which the latter as little profited, say wicked
wits, as other nobility, for whom a nation has long prayed that grace,
wisdom, and understanding might be their portion. St. Adelard, for
the imperial knight was canonized, lived to be the chief authority in
the monastery where he had commenced as cook and gardener, and
St. Gerard composed an office in his honor, in gratitude for having
been cured of a violent headache through the saint’s interposition.
This seems to me one of the oddest ways of showing gratitude for a
small service that I ever heard of.
I believe that St. Cedd, Bishop of London, in very early days, was
also of a family whose profession was military. When or why he
entered the church I do not know; but he has some connection with
military matters in the fact that Tilbury Fort occupies part of the site
of a monastery which St. Cedd had founded, in which he resided,
and which was the pride of all the good people in the then pleasant
and prosperous city of Tillabury.
Touching St. Aldric, Bishop of Mans, there is no doubt whatever. He
was of a noble family, and commenced life at twelve years old, as
page to Louis le Debonnaire, at the court of Charlemagne. He was
speedily sick of the court, and as speedily sick of the camp. At the
age of twenty-one he withdrew to Metz, entered the clerical
profession, and became chaplain and confessor to the sovereign
whom he had once served as page. His military training made him a
very sharp disciplinarian during the quarter of a century that he was
bishop; and it is only to be regretted that he had not some influence
over the king whose conscience he directed, and of whom a legend
will be found in another part of this volume.
There was a second son of Eric, King of Denmark, known by the
name of St. Knudt or Canute. He was Duke of Schleswig, and was
much more of a monk than a duke. He was canonized accordingly
for his virtues. He had a rough way of joking. His knights were
nothing better than robbers and pirates, and he resolved to make
them forswear violence and live peaceably. They represented, in
vain, that they had a right to live as became knights, which Canute
did not dispute; he simply dissented from the construction of the right
as set down by the knights themselves. To prevent all mistakes on
the matter, he one day condemned seven of these gentlemen to be
hanged for acts of piracy. One of these exclaimed that, “fitting as the
sentence might be for his fellows, there must necessarily be
exemption for him.” He was like the German corporal in the “Etoile
du Nord,” who can very well understand that it is quite proper that a
man should be hanged, but could not comprehend that he himself
should be the man. The Schleswig knight claimed special exemption
on the ground that he was a kinsman of Canute. The latter allowed
that this entitled him to some distinction, and the saintly duke hung
his cousin six feet higher than any of his accomplices.
We come back more immediately to a knight who grew tired of his
vocation, in the person of Nathalan, a Scottish noble of the fifth
century. He sold arms, horses, and estate, divided the proceeds
among the poor, and devoted himself to preparations for ordination,
and the cultivation of vegetables. He bears a highly respectable
reputation on the roll of Bishops of Aberdeen.
We meet with a man more famous, in Peter of Sebaste, whose
pedigree showed more heroes than could be boasted by any of
Peter’s contemporaries. He is not an example, indeed, of a man
quitting the camp for the cloister; but he and two of his brothers
exhibit to us three individuals who might have achieved great worldly
profit, by adopting arms as a vocation, but who preferred the Church,
and became, all three, bishops.
We have a similar example in the Irish St. Felan. His high birth and
great wealth would have made him the flower of Irish chivalry, but he
selected another profession, and despising chivalry, entered the
Church. He went a Mundo ad Mundum, for it was from the hands of
Abbot Mundus that he received the monastic habit. Thus, as it was
wittily said, the world (Mundus) at once drove and drew him into the
Church. It is clear, however, that, like the old war-horse, he pricked
up his ears at the sound of battle, and took an interest in stricken
fields. To such conclusion we must come, if it be true, as is asserted
of him, that the battle of Bannockburn, in 1314, was won by Bruce
through the saint’s especial intercession. The Dukes of Normandy
owed equal obligations to St. Vaneng, who unbuckled the armor from
his aristocratic loins, to cover them with a frock; and built churches
for the Normans, where he offered up continual prayer for the
Norman dukes.
Then again, there was William Berringer, of the family of the Counts
of Nevers. No persuasion could induce the handsome William to
continue in the career he had embraced, the career of chivalry and
arms. His uncle, Peter the Hermit, may have had considerable
influence over him, and his change of profession was by no means
unprofitable, for the once horse-loving William became Archbishop of
Bourges: and he defended the rights of his Church against kings and
councils with as much boldness, zeal, and gallantry, as any knight
could have exhibited against the stoutest of assailants.
Among our English saints, the one who most nearly resembles him
is St. Egwin, who was of the royal blood of the Mercian kings, and
who, after a short trial of the profession of arms, retired to the
cloister, but was ultimately raised to the see of Worcester. The spirit
of the man may perhaps be seen through the legend which says that
on setting out on a penitential pilgrimage to Rome, he put iron
shackles on his legs, the key of which shackles he flung into the
Avon. This is very possible; but when we are told that on requiring
the key at a subsequent period, he found it inside a fish, we see that
the author of the legend has plagiarized from the original constructor
of the story of Polycrates and his ring.
St. Egwin was far less a benefactor to his fellow-men than St.
Benedict Biscop, a noble knight of the court of Oswi, the pious king
of the Northumbrians. When Benedict, or Bennet, as he is familiarly
called, retired from the profession of arms to follow that of the
Church, he continued quite as active, and twice as useful, as he had
been before. He was a great traveller, spent and gave liberally, and
brought over with him, from the continent, workers in stone to erect
that monastery at Weremouth which, in its ruins, commemorates his
name and deeds. He also brought from France the first glaziers who
ever exercised the art of glass-making in England. Altogether St.
Bennet is one of those who find means to effect good to others,
whatever may be the position they are in themselves.
Aelred of Ridal was a man of similar quality. He was a young North-
of-England noble, when he figured as the handsomest cavalier at the
court of that “sair saint to the Church,” the Scottish king, David. He
was remarkable for his good temper, and was as well-disciplined a
monk as he had been a military man; for when he once happened to
inadvertently break the rule of permanent silence, which prevailed in
the monastery at Ridal, into which he entered at the age of twenty-
five, he became so horror-stricken that he was eager to increase the
penalty put upon him in consequence. He had only dropped a single
word in the garden, to a monk who, like himself, had been a knight,
but who gave him in return so edifying a scowl, that in an instant
poor Aelred felt all the depth of his unutterable iniquity, and
accounted himself as criminal as if he had set fire to the neighboring
nunnery. He never afterward allowed himself the indulgence of
reading his favorite Cicero, but confined his reading to his own work
“On Spiritual Friendship,” and other books of a similar description.
The great St. Hilary was another of the men of noble family following
arms as a vocation, who gave up the profession for that of the
Church, and prospered remarkably in consequence. St. Felix of Nola
affords us an additional illustration of this fact. This noble young
soldier found no happiness in the business of slaughtering, and all
the sophistry in the world could not persuade him that it was
honorable. “It is a disgusting business,” said the Saint, “and as I can
not be Felix [happy] in performing it, I will see if I can not be Felix in
the Church;” and the punning saint found what he sought.
There is something more wonderful in the conversion of St. Maurus.
He was the son of a nobleman, had St. Benedict for a tutor, and was
destined to the career of arms. The tutor, however, having awoke
him one night, and sent him to pick a monk out of the river, whom
Benedict, in a dream, had seen fall in, Maurus, although no
swimmer, obeyed, walked upon the surface of the water, pulled out
the struggling monk, walked back with him, arm-in-arm, to the shore,
and immediately concluded that he was called to another vocation
than that of arms. As for St. John Calybyte, he would not be a
soldier, but ran away from home before his wealthy sire could
procure him a commission, and only returned to stand, disguised as
a mendicant, in front of his father’s house, where he received alms
till he died. A curious example of idiosyncrasy. St. Honoratus was
wiser. He was of a consular family; but, in declining the military
profession, he addressed himself with sincerity to be useful in the
Church; and the well-deserved result was that he became
Archbishop of Arles. St. Anthony, the patriarch of monks, made still
greater sacrifices, and chose rather to be a hermit than a
commander of legions. St. Sulpicius, the Debonnair, was both rich
and good-looking, but he cared less for helmet and feathers than for
cord and cowl, and the archbishopric of Bourges rewarded his self-
denial. There was more than one King Canute too, who, though not
surrendering royalty and generalship of armies, seemed really more
inclined, and indeed more fitted, to be studious monks than
chivalrous monarchs. Wulstan of Worcester was far more decided,
for finding himself, one night, most warmly admiring the young lady
who was his vis-à-vis in a dance, the gallant officer was so shocked
at the impropriety, that he made it an excuse for taking to the cowl
forthwith. He did not so ill by the exchange, for the cowl brought him
to the mitre at Worcester.
St. Sebastian was a far bolder man, seeing that although he hated a
military life, he, to the very utmost, did his duty in that state of life to
which it had pleased God to call him; and if half be true of what is
told of him, there never was knight of the actual days of chivalry who
performed such bold and perilous actions as St. Sebastian. What
was a cavalier, pricking against a dragon, to a Roman officer
preaching Christianity to his men, under Diocletian?
In later days we meet with St. Raymund of Pennafort, the wealthy
young lord, who, rather than serve for pay or plunder, went about
teaching philosophy for nothing. St. John, the Patriarch of
Alexandria, might have been known as a conqueror, but he preferred
being handed down, under the title of the Almoner. He was like that
St. Cadoc who chose rather to be abbot in, than prince of, Wales. St.
Poppo of Stavelo exhibited similar humility. He was rapidly rising in
the Flandrian army when he suddenly sunk into a cell, and became a
sort of Flemish John Wesley. He preached against all tournaments,
but only succeeded in abolishing the very exciting combats between
a knight and a bear, which were greatly patronized by Flemish
ladies, and at which parties staked great sums upon their favorite
animal.
St. Francis of Sales, on the other hand, that gentlemanly saint, was
saved from the knightly career which his noble birth seemed to
promise him, by a vow made by his mother, before he was born. She
was resolved that he should be a saint and not a soldier, and as all
things went as the lady desired, she placed her son in a position
direct for the Church, and the world certainly lost nothing by the
matron’s proceeding. I respect St. Francis of Sales all the more that
he had small human failings, and did not scatter damnation over
men whom he saw in a similar concatenation. Sulpicius Severus
was, in many respects, like him, save that he had some experience
of a soldier’s life. But he laid down the sword for the pen, and gave
us that admirable historical romance, in which he details so
graphically the life of another noble warrior, who quitted the
command of soldiers, to take up the teaching of men—St. Martin of
Tours.
There was a lady, St. Aldegonde, of the royal blood of France, in the
seventh century, who at least encouraged young knights to abandon
their fancied vocation, and assume that of monks or friars. She was,
most undeservedly, I dare say, assailed by scandalizing tongues
accordingly. Indeed, I never heard of lady more persecuted in this
way, except perhaps this particular lady’s namesake, who once
belonged to the gay troupe of the Varietés, and to whom the most
rattling of chansonniers alluded, in the line of a song, which put the
significant query of

Que fait Aldegonde avec le monde entier?

One of the most remarkable features in the characters of many of


these young nobles who were disinclined to take up arms, or who
laid them down for the religious vocation, is the dread they
entertained of matrimony. In illustration of this fact, I may notice the
case of St. Silvin of Auchy. There was not a gayer or braver knight at
the court of Childeric II., nor a more welcome wooer among the
ladies. In due time he proposed to a noble maiden, who was in a
flutter of happiness at the thought of carrying off such a bachelor
from a host of competitors. The wedding was brilliant, up to the
conclusion of the ceremony. That over, no persuasion could induce
the bridegroom to go to the breakfast. As he had been brought to the
altar, there he was resolved to remain. He denounced all weddings
as wicked vanities, and darting out of the church-door, left bride and
bridal party to take what course they would. There was no end of
conjectures as to the cause of the sudden fright which had seized
upon the young bridegroom. The latter set it down to inspiration, and
as he took to the cowl and led a most exemplary life, no one
presumed to doubt it, except the bride and her relations.
The case of St. Licinius is easier of explanation. He was the most
rollicking knight-bachelor at the court of Clotaire I. It must, however,
be said for him that he sowed his wild oats early, and fought none
the less stoutly for going to mass daily, and confessing once a
quarter. He was rich, and had a maiden neighbor who was richer.
The families of knight and maiden were united in thinking that the
estates of the two, encircled in one ring fence, would be one of the
most desirable of consummations. The maiden was nothing loath,
the knight alone was reluctant. He too, had his doubts about the
excellence of marriage, and it was only with very considerable
difficulty he was brought to woo the lady, who said “Yes” before the
plume in his bonnet had touched the ground when he made his bow
to her. The wedding-day was fixed, and as the old epitaph says,
“wedding-clothes provided.” On the eve of the eventful day, however,
Licinius, on paying a visit to the bride, found her suddenly attacked
with leprosy. The doctor protested that it would be nothing, but
Licinius declared that it was a warning which he dared not neglect.
He looked at the leprous lady, muttered the word “unpleasant,” and
at once betook himself, not to active military life, but to a religious
mission. In this occupation he is alleged to have performed such
miracles as to deserve canonization, if only the half of them were
true.
Now, a bride afflicted with leprosy may fairly be said to be an
unpleasant sight. Licinius may even be considered authorized to
hesitate in performing his promise, if not in altogether declaring off.
We can not say as much in extenuation of another knight who broke
his word to a lady, and was clapped into the Roman calendar of
deified men. This gentleman in question had a rather unchristian-
sounding name. He was called Abraham of Chiduna. At tilt and
tournament, and in tented field, there was no cavalier who sat more
perfectly in saddle, or handled his lance and wielded his battle-axe
with more terrible effect. He was of noble birth, of course; was
wealthy, somewhat addicted to light living, in his salad days, but a
man who lived soberly enough when those were over. He then
resolved to marry, and he had the “good taste,” if one may use a
term which, we are told, belongs to the literary milliner’s vocabulary,
to offer himself to, and ask the hand of a very pious maiden with a
highly satisfactory dower. The required conclusion was soon come
to, and one fine spring morning saw the two principals and their
respective friends in church. The knight, it is true, was the last to
arrive, and he had been, previously, as unwilling to get up and be
married, as Master Barnardine was to get up and be hanged. He
was finally brought to the altar, and after some little delay, such as
searching for the ring which he had misplaced, and only recovered
after much search, the nuptial knot was tied. When this had been
accomplished, surrounding friends approached to offer their
congratulations; but the icy Abraham coldly waved them back, and
announced his determination, then and there, to end his short-lived
married state. As he immediately rushed into the wood which was in
the vicinity of the church, there was a universal cry that he
contemplated suicide. The bride was conveyed home amid much
sympathy, and a general but an ineffectual search was made for the
“groom.” Yet, not altogether ineffectual, for at the end of seventeen
days he was discovered, offering up his orisons, in the midst of a
marsh. There he had been, he said, for a fortnight, and there he
declared he would remain, unless those who sought him consented
to the terms he should propose. These were, that he should be
allowed to retire to a cell which should be entirely walled up, save a
small square aperture for a window. The agreement was ratified, and
Abraham was shut up according to his desire; and by a long life of
seclusion, passed in preaching to all who approached the window,
and taking in all they brought through the same aperture, Abraham
has had “Beatus” attached to his name, and that name has been
recorded upon the roll of saints.
If there be any reader who objects to this story as unnatural, I would
remark to the same, that similar incidents may be met with in our
own time. In proof thereof I will briefly relate an anecdote which was
told me by the reverend father of a legal knight, who was himself the
officiating minister at the ceremony of which I am about to speak.
To the clergyman of a pretty village in Wales, due notice had been
given, and all preliminary legal observances having been fulfilled, he
awaited in his vestry, ready to marry an ex-sergeant and one of the
girls of the village. The canonical hours were fast gliding away, and
yet the priest was not summoned to the altar. By certain sounds he
could tell that several persons had assembled in the church, and he
had two or three times seen a pretty face peeping in at the vestry-
door, with a look upon it of pleasure to see that he was still there,
and of perplexity as if there was something to be told which only
waited to be asked for. At half-past eleven the face again peeped in,
whereupon the clergyman invited the owner of it to approach nearer.
The invitation was obeyed, and the clergyman inquired the reason
for the unusual delay, remarking at the same time, that if the parties
were not speedily prepared it would be too late to perform the
ceremony that day.
“Well sir,” said the nymph, “I was about asking your advice. I am the
bride’s sister; and there is a difficulty—”
“What is it?” asked the priest.
“Just this, sir,” said Jenny. “Sergeant Jones has promised to marry
sister Winnifred if father will put down five pounds. Father agrees;
but he says that if he puts down the money before the marriage, the
sergeant will walk off. And the sergeant will not come up to be
married till the money is put down. So, you see, sir, we are in a
terrible difficulty; and we want you to propose a method to get us out
of it.”
“There is nothing easier,” said the minister; “let your father put the
money into the hands of a trusty third person, who will promise to
place it in the sergeant’s possession as soon as he has married your
sister.”
Jenny Morgan saw the excellence of the device in a moment, rushed
back to the bridal parties, and they showed their appreciation of the
clergyman’s suggestion, by crowding to the altar as soon as the
preliminary proceeding recommended to them had been
accomplished. At length the clergyman came to the words, “Wilt thou
have this woman to thy wedded wife?”
“Jack,” said the ex-sergeant, looking round at the stake-holder, “have
you got the cash?”
“All right!” nodded Jack.
“Then I will,” said the sergeant; “and now, Jack, hand over the tin.”
The agreement was rigidly fulfilled; but had not the minister thought
of the means which solved the difficulty, Sergeant Jones would have
been nearly as ungallant to his lady as Abraham, Silvin, and Licinius,
had been to theirs.
But to return to Abraham. I have said this knight, on assuming his
monkly character, had caused himself to be walled up in his cell. I
have my suspicions, however, that it was a theatrical sort of wall, for
it is very certain that the saint could pass through it. Now, there
resided near him a lady recluse who was his “niece,” and whose
name was Mary. The two were as inseparable as the priest Lacombe
and Madame Guyon; and probably were as little deserving of
reproach. This Mary was the original of “Little Red Riding Hood.” She
used to convey boiled milk and butter, and other necessary matters
to her uncle Abraham. Now it happened that the ex-knight used also
to be visited by a monk whose name was Wolf, or who, at all events,
has been so called by hagiographers, on account of his being quite
as much of a beast as the quadruped so called. The monk was wont
to fall in with Mary as she was on her way to her uncle’s cell with
pleasant condiments under a napkin, in a wicker-basket. He must
have been a monk of the Count Ory fashion, and he was as
seductive as Ponchard, when singing “Gentille Annette” to the “Petit
Chaperon Rouge,” in Boieldieu’s Opera. The result was, that the
monk carried off Mary to a neighboring city—Edessa, if I remember
rightly—and if I am wrong, Mr. Mitchell Kemble will, perhaps, set me
right, in his bland and gentleman-like way. The town-life led by these
two was of the most disgraceful nature; and when the monk had
grown tired of it, he left Mary to lead a worse, without him. Mary
became the “Reine Pomare,” the “Mogadore,” the “Rose Pomponne”
of Edessa, and was the terror of all families where there were elder
sons and latch-keys. Her doings and her whereabouts at length
reached the ears of her uncle Abraham, and not a little astonished
were those who knew the recluse to see him one morning, attired in
a pourpoint of rich stuff, with a cloak like Almaviva’s, yellow buskins
with a fall of lace over the tops, a jaunty cap and feather on his head,
a rapier on his thigh, and a steed between his legs, which curveted
under his burden as though the fun of the thing had given it
lightness. At Mary’s supper, this cavalier was present on the night of
his arrival in Edessa. He scattered his gold like a Crœsus, and Mary
considered him worth all the more penniless knights put together.
When these had gone, as being less welcome, Abraham declared
his relationship, and acted on the right it gave him to rate a niece
who was not only an ungrateful minx, but who was as mendacious
as an ungrateful niece could well be. The old gentleman, however,
had truth on his side, and finally so overwhelmed Mary with its
terrible application, that she meekly followed him back to the desert,
and passed fifteen years in a walled-up cell close to that of her
uncle. The miracles the two performed are adduced as proofs of the
genuineness of the personages and their story; matters which I
would not dispute even if I had room for it.
The next knight whom I can call to mind as having been frightened
by marriage into monkery, is St. Vandrille, Count of the Palace to
King Dagobert. During the period of his knightship he was a very
Don Juan for gallantry, and railed against matrimony as conclusively
as a Malthusian. His friends pressed him to marry nevertheless; and
introduced him to a lady with a hundred thousand golden qualities,
and prospects as auriferous as those of Miss Kilmansegg. He took
the lady’s hand with a reluctance that might be called aversion, and
which he did not affect to conceal. When the nuptial ceremony was
concluded, Knight Vandrille, as eccentric as the cavaliers whose
similar conduct I have already noticed, mildly intimated that it was
not his intention to proceed further, and that for his part, he had
renounced the vanities of this world for aye. Taking the lady apart, he
appears to have produced upon her a conviction that the
determination was one he could not well avoid; and we are not told
that she even reproached him for a conduct which seems to me to
have been a thousand times more selfish and inexcusable than that
of the clever but despicable Abelard. The church, however, did not
disapprove of the course adopted, and St. Vandrille, despite his
worse than breach of promise, has been forgiven as knight, and
canonized as saint.
Far more excusable was that little Count of Arian, Elzear, the boy-
knight at the court of Charles II., King of Sicily, whom that monarch
married at the age of thirteen years, to Delphina of Glandeves, a
young lady of fifteen. When I say far more excusable, I do Elzear
some injustice, for the boy was willing enough to be wed, and looked
forward to making his lady proud of his own distinction as a knight.
Delphina, however, it was who proposed that they should part at the
altar, and never meet again. She despised the boy, and the little
cavalier took it to heart—so much so, that he determined to
renounce the career of arms and enter the church. Thereby chivalry
lost a worthy cavalier, and the calendar gained a very active saint.

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