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 GARDNER AND SUTHERLAND’S
CHROMOSOME ABNORMALITIES
AND GENETIC COUNSELING

2
OXFORD MONOGRAPHS ON MEDICAL GENETICS
General Editors:
JUDITH G. HALL PETER S. HARPER LOUANNE HUDGKINS EVAN EICHLER CHARLES J.
EPSTEIN (DECEASED 2011) ARNO G. MOTULSKY (RESIGNED 2011)

1. R. B. McConnell: The genetics of gastrointestinal disorders

2. A. C. Kopéc: The distribution of the blood groups in the United Kingdom
3. E. Slater and V. A. Cowie: The genetics of mental disorders
4. C. O. Carter and T. J. Fairbank: The genetics of locomotor disorders
5. A. E. Mourant, A. C. Kopéc, and K. Domaniewska-Sobezak: The distribution
of the human blood groups and other polymorphisms
6. A. E. Mourant, A. C. Kopéc, and K. Domaniewska-Sobezak: Blood groups and
diseases
7. A. G. Steinbert and C. E. Cook: The distribution of the human immunoglobulin
allotypes
8. D. Tills, A. C. Kopéc, and R. E. Tills: The distribution of the human blood
groups and other polymorphisms: Supplement I
10. D. Z. Loesch: Quantitative dermatoglyphics: Classification, genetics, and
pathology
11. D. J. Bond and A. C. Chandley: Aneuploidy
12. P. F. Benson and A. H. Fensom: Genetic biochemical disorders
13. G. R. Sutherland and F. Hecht: Fragile sites on human chromosomes
14. M. d’A Crawfurd: The genetics of renal tract disorders
16. C. R. Scriver and B. Child: Garrod’s inborn factors in disease
18. M. Baraitser: The genetics of neurological disorders
19. R. J. Gorlin, M. M. Cohen, Jr., and L. S. Levin: Syndromes of the head and
neck, third edition
21. D. Warburton, J. Byrne, and N. Canki: Chromosome anomalies and prenatal
development: An atlas
22. J. J. Nora, K. Berg, and A. H. Nora: Cardiovascular disease: Genetics,
epidemiology, and prevention
24. A. E. H. Emery: Duchenne muscular dystrophy, second edition
25. E. G. D. Tuddenham and D. N. Cooper: The molecular genetics of haemostasis
and its inherited disorders
26. A. Boué: Foetal medicine
27. R. E. Stevenson, J. G. Hall, and R. M. Goodman: Human malformations
28. R. J. Gorlin, H. V. Toriello, and M. M. Cohen, Jr.: Hereditary hearing loss and
its syndromes
29. R. J. M. Gardner and G. R. Sutherland: Chromosomes abnormalities and
genetic counseling, second edition
30. A. S. Teebi and T. I. Farag: Genetic disorders among Arab populations
31. M. M. Cohen, Jr.: The child with multiple birth defects
32. W. W. Weber: Pharmacogenetics

3
33. V. P. Sybert: Genetic skin disorders
34. M. Baraitser: Genetics of neurological disorders, third edition
35. H. Ostrer: Non- Mendelian genetics in humans
36. E. Traboulsi: Genetic factors in human disease
37. G. L. Semenza: Transcription factors and human disease
38. L. Pinsky, R. P. Erickson, and R. N. Schimke: Genetic disorders of human
sexual development
39. R. E. Stevenson, C. E. Schwartz, and R. J. Schroer: X- linked mental
retardation
40. M. J. Khoury, W. Burke, and E. Thomson: Genetics and public health in the
21st century
41. J. Weil: Psychosocial genetic counseling
42. R. J. Gorlin, M. M. Cohen, Jr., and R. C. M. Hennekam: Syndromes of the head
and neck, fourth edition
43. M. M. Cohen, Jr., G. Neri, and R. Weksberg: Overgrowth syndromes
44. R. A. King, J. I. Rotter, and A. G. Motulsky: Genetic basis of common
diseases, second edition
45. G. P. Bates, P. S. Harper, and L. Jones: Huntington’s disease, third edition
46. R. J. M. Gardner and G. R. Sutherland: Chromosome abnormalities and genetic
counseling, third edition
47. I. J. Holt: Genetics of mitochondrial disease
48. F. Flinter, E. Maher, and A. Saggar- Malik: Genetics of renal disease
49. C. J. Epstein, R. P. Erickson, and A. Wynshaw-Boris: Inborn errors of
development: The molecular basis of clinical disorders of morphogenesis
50. H. V. Toriello, W. Reardon, and R. J. Gorlin: Hereditary hearing loss and its
syndromes, second edition
51. P. S. Harper: Landmarks in medical genetics
52. R. E. Stevenson and J. G. Hall: Human malformations and related anomalies,
second edition
53. D. Kumar and S. D. Weatherall: Genomics and clinical medicine
54. C. J. Epstein, R. P. Erickson, and A. Wynshaw-Boris: Inborn errors of
development: The molecular basis of clinical disorders of morphogenesis,
second edition
55. W. Weber: Pharmacogenetics, second edition
56. P. L. Beales, I. S. Farooqi, and S. O’Rahilly: The genetics of obesity syndromes
57. P. S. Harper: A short history of medical genetics
58. R. C. M. Hennekam, I. D. Krantz, and J. E. Allanson: Gorlin’s syndromes of
the head and neck, fifth edition
59. D. Kumar and P. Elliot: Principles and practices of cardiovascular genetics
60. V. P. Sybert: Genetic skin disorders, second edition
61. R. J. M. Gardner, G. R. Sutherland, and L. C. Shaffer: Chromosome
abnormalities and genetic counseling, fourth edition
62. D. Kumar: Genomics and health in the developing world
63. G. Bates, S. Tabrizi, and L. Jones: Huntington’s disease, fourth edition

4
64. B. Lee and F. Scaglia: Inborn errors of metabolism: From neonatal screening
to metabolic pathways
65. D. Kumar and C. Eng: Genomic medicine, second edition
66. R. Stevenson, J. Hall, D. Everman, and B. Solomon: Human malformations
and related anomalies, third edition
67. R. Erickson and A. Wynshaw-Boris: Epstein’s inborn errors of development:
The molecular basis of clinical disorders of morphogenesis, third edition
68. C. Hollak and R. Lachmann: Inherited metabolic disease in adults: A clinical
guide
69. V. P. Sybert: Genetic skin disorders, third edition
70. R. J. M. Gardner and D. J. Amor: Gardner and Sutherland’s chromosome
abnormalities and genetic counseling, fifth edition

5
 GARDNER AND SUTHERLAND’S

Chromosome Abnormalities and

Genetic Counseling
FIFTH EDITION

R. J. McKinlay GARDNER
ADJUNCT PROFESSOR
CLINICAL GENETICS GROUP
UNIVERSITY OF OTAGO, DUNEDIN, NEW ZEALAND

David J. AMOR
LORENZO AND PAMELA GALLI CHAIR
UNIVERSITY OF MELBOURNE
VICTORIAN CLINICAL GENETICS SERVICES
MURDOCH CHILDREN’S RESEARCH INSTITUTE
ROYAL CHILDREN’S HOSPITAL, MELBOURNE, AUSTRALIA

6
Oxford University Press is a department of the University of Oxford. It furthers the University’s
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Published in the United States of America by Oxford University Press

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acquirer.

Library of Congress Cataloging-in-Publication Data

Names: Gardner, R. J. M., author. | Amor, David J., author.
Title: Gardner and Sutherland’s chromosome abnormalities and genetic counseling / R. J. McKinlay
Gardner, David J. Amor.
Other titles: Chromosome abnormalities and genetic counseling | Oxford monographs on medical
genetics ; no. 70.
Description: Fifth edition. | Oxford ; New York : Oxford University Press, [2018] |
Series: Oxford monographs on medical genetics ; no. 70 | Preceded by Chromosome abnormalities
and genetic counseling / R.J. McKinlay Gardner, Grant R. Sutherland, Lisa G. Shaffer. c2012. |
Includes bibliographical references and index.
Identifiers: LCCN 2017034126 | ISBN 9780199329007 (hardcover : alk. paper) | ISBN
9780199329021 (epub)
Subjects: | MESH: Chromosome Aberrations | Genetic Counseling
Classification: LCC RB155.7 | NLM QS 677 | DDC 616/.042—dc23 LC record available at
https://lccn.loc.gov/2017034126

This material is not intended to be, and should not be considered, a substitute for medical or other
professional advice. Treatment for the conditions described in this material is highly dependent on
the individual circumstances. And, while this material is designed to offer accurate information with
respect to the subject matter covered and to be current as of the time it was written, research and
knowledge about medical and health issues is constantly evolving and dose schedules for
medications are being revised continually, with new side effects recognized and accounted for
regularly. Readers must therefore always check the product information and clinical procedures
with the most up-to-date published product information and data sheets provided by the
manufacturers and the most recent codes of conduct and safety regulation. The publisher and the
authors make no representations or warranties to readers, express or implied, as to the accuracy or
completeness of this material. Without limiting the foregoing, the publisher and the authors make
no representations or warranties as to the accuracy or efficacy of the drug dosages mentioned in the
material. The authors and the publisher do not accept, and expressly disclaim, any responsibility for
any liability, loss or risk that may be claimed or incurred as a consequence of the use and/or
application of any of the contents of this material.

7
 This book is dedicated to Jocelyn, Geoffrey, and Craig, their
parents, and all other families who seek our “chromosomal
advice.”

Jocelyn and Geoffrey (with lamb) have a partial trisomy for

chromosome 4 long arm, and Craig, the youngest, had a 46,XY
result on amniocentesis. Their father is a translocation carrier (see
Fig. 5–1, lower). Craig, since married, came to the genetic clinic

8
for confirmatory advice about his low genetic risk.

9
Heredity
Inescapably, this is me—the diagnosis
is cause for anger at those
who brightly say we choose our destinies.
There is no store
of courage, wit or will
can save me from myself and I must face
my children, feeling like
that wicked fairy, uninvited
at the christening, bestowing on my own,
amidst murmurs of apprehension, a most
unwanted gift—that
of a blighted mind. No one
could tell me of this curse when I
was young and dreamt of children
and the graces they would bear. Later,
it seemed that a chill morning
revealed deeper layers
of truth. For my romancing
there is a price to pay—
perhaps my children’s children
will pass this tollgate after me.
My grandmothers gaze down from their frames
on my wall, sadly wondering.
—Meg Campbell

Dear DNA
In real life you’re just
a tangle of white filaments
captured in a test-tube,
and your first photo is not flattering:
grey smudges like tractor tracks,
or a rusty screw. Yet
many say you are beautiful.
Online for a night
with a hundred fantastic portraits

10
and I’m head over heels
In love with you, DNA,
bewitched by your billions
coiled in my cells, transcribing,
replicating, mutating.
I see your never-ending dance.
A length of twisted ladder
briefly unwinds,
both strands duplicate,
each copy drifts away
on its secret mission
to make a thought, feel sunshine,
or digest this morning’s porridge.
Two winding parallel threads,
a tiny tangle of gossamer
designing my life.
DNA, you are astonishing
and I am yours truly.
—Winifred Kavalieris

Genes pass on our kind

But our selves are transmitted
In words left behind.
—J. Patrick Gookin

Curiosity is a virtue, perhaps an unsung and undervalued virtue, which

should be the energizing fuel to the thinking geneticist.
—Willie Reardon

Where is the wisdom we have lost in knowledge?

Where is the knowledge we have lost in information?
—T. S. Eliot

11
 PREFACE TO THE FIFTH EDITION

Chromosomal disorders have been, and will always be, with us; that is a
given. What is changing is our ability to recognize and detect them:
detection both in terms of the subtlety of abnormalities and of the means
we can use to find them. Classical cytogenetics has now well and truly
given way to “molecular karyotyping,” and this has been the extraordinary
development of the early twenty-first century. Readers will now be as
accustomed to molecular nomenclature in defining a segment, such as
chr5:1-18,500,000, as they had been to the classical description,
5p14.1→pter.
The very small deletions and duplications which molecular karyotyping
can now reveal have become familiar to the clinicians and counselors who
see patients and families in the clinic. A large number of these are now on
record, many attracting the nomenclature “copy number variant”: Some
are very well understood, others becoming so, and yet quite a few—
variants of uncertain significance, the acronym “VOUS” in daily parlance
—whose roles in human pathology are imperfectly appreciated. Many are
not in the same mold as the deletions and duplications of classical
cytogenetics, in which the single defect sufficed to cause a particular
phenotype, and always did so: We now need to take account of the concept
of incomplete penetrance, with some microdeletions or duplications not, of
themselves, always leading to an abnormal phenotype. Apparently
clinically normal parents may carry the same alteration as their child with
an abnormal phenotype. Digenic, or “two-hit,” mechanisms may now
require consideration. These were not formerly notions much entering into
the assessment of chromosomal disorders; discussion apropos in the clinic
presents a new challenge.
The number of “new” del/dup syndromes increases almost with each
issue of the clinical genetic journals. We include a mention of a
considerable number of these here (Chapter 14), not intending to create an
encyclopedic resource per se but believing that such a record may provide
a useful first point of contact when these cases are encountered in the
clinic. Copy number variants of uncertain significance, on the other hand,
we mostly take only a broad rather than a detailed view (Chapter 17); the

12
reader will need to consult other repositories for fuller information, as their
interpretations evolve.
The new (or now, established) laboratory methodologies blur the
boundaries between what might have been regarded as the classic
chromosomal abnormalities and Mendelian conditions. Some disorders
recorded as being due not only to segmental deletion/duplication affecting
a single locus but also to point mutation at that locus we continue to treat
as “chromosomal”; and for most, their place in this book is secure. But one
major category, the fragile X syndromes, are now seen as essentially
Mendelian disorders, their historic cytogenetic-based nomenclature
notwithstanding, and they no longer claim their chapter.
Peripheral blood and skin have been the tissues in common usage for
chromosome analysis, with an increasing role for cells got from the
convenient and painless “spit sample.” Prenatal diagnosis has been based
on amniocentesis and chorionic villus sampling, but latterly blastomeres
from early embryos, and fetal DNA in the maternal circulation, have
become targets for testing. Now we can anticipate the potential for whole
genome analysis to be applied to the prenatal diagnosis of the classic
aneuploidies, from a simple maternal blood sample, and this would widen
such testing very considerably. Questions such as these raise ethical issues,
and a literature on “chromosomal ethics” is accumulating.
As we have previously written, however marvelous may be these new
ways to test for chromosomes, the concerns of families remain essentially
the same. We may reproduce here the final paragraph of the Preface of the
first edition of this book, from 1989, as valid now as then:
Families pursue genetic counseling in an effort to demystify the mysterious.
If they did not want to “hear it all,” they would not bother with genetic
counseling. Families want an honest evaluation of what is known and what is
unknown, a clear explanation of all possibilities, both good and bad, and a
sensitive exploration of all available information with which they can make
knowledgeable decisions about future family planning. Thus, Bloch et al.
(1979) succinctly convey the essence of why people go to the genetic
counselor. We hope this book will assist counselors in their task.

Dunedin R.J.M.G.
Melbourne D.J.A.
February 2018

13
 ACKNOWLEDGMENTS

We thank John Barber, Rachel Beddow, Amber Boys, Cyril Chapman,

Jane Halliday, Jan Hodgson, Caroline Lintott, Nicole Martin, Belinda
McLaren, Fiona Norris, Mamoru Ozaki, Mark Pertile, Jenny Rhodes,
Sharyn Stock-Myer, and Jane Watt for their critical advice. We
acknowledge Lisa Shaffer, who was a co-author of the previous edition,
and much of whose work has flowed over into this edition. We have made
much use of the ideograms created by Nicole Chia. The length of the
Reference list, and the frequency with which we acknowledge, in legends
to figures, the courtesy of colleagues whose work we use, speaks for the
debt we owe to our colleagues in clinical cytogenetics worldwide.
Belatedly, R.J.M.G. thanks Ngaire Adams and Dianne Grimaldi, whose
need for chromosomal teaching at Dunedin Hospital in the 1980s provided
the germination for writing this book. We have appreciated the wise
guidance, and the patience and forbearance of Oxford University Press,
from Jeff House when this book made its first appearance, through to Chad
Zimmerman and Chloe Layman in this fifth edition. R.J.M.G. thanks his
wife Kelley for her patient help, once again, in document management;
and the front cover art, and most of the new illustrations in this edition,
have been drawn, or redrawn, by her.

14
 CONTENTS

PART ONE: BASIC CONCEPTS

1. Elements of Medical Cytogenetics
2. Chromosome Analysis
3. The Origins and Consequences of Chromosome Pathology
4. Deriving and Using a Risk Figure

PART TWO: PARENT OR CHILD WITH A CHROMOSOMAL

ABNORMALITY
5. Autosomal Reciprocal Translocations
6. Sex Chromosome Translocations
7. Robertsonian Translocations
8. Insertions
9. Inversions
10. Complex Chromosomal Rearrangements
11. Autosomal Ring Chromosomes
12. Centromere Fissions, Complementary Isochromosomes,
Telomeric Fusions, Balancing Supernumerary Chromosomes,
Neocentromeres, Jumping Translocations, and Chromothripsis
13. Down Syndrome, Other Full Aneuploidies, Polyploidy, and the
Influence of Parental Age
14. Autosomal Structural Rearrangements: Deletions and
Duplications
15. Sex Chromosome Aneuploidy and Structural Rearrangement
16. Chromosome Instability Syndromes

PART THREE: CHROMOSOME VARIANTS

15
17. Normal Chromosomal Variation

PART FOUR: DISORDERS ASSOCIATED WITH ABERRANT

GENOMIC IMPRINTING
18. Uniparental Disomy and Disorders of Imprinting

PART FIVE: REPRODUCTIVE CYTOGENETICS

19. Reproductive Failure
20. Prenatal Testing Procedures
21. Chromosome Abnormalities Detected at Prenatal Diagnosis
22. Preimplantation Genetic Diagnosis

PART SIX: DISORDERS OF SEX DEVELOPMENT

23. Chromosomal Disorders of Sex Development

PART SEVEN: NOXIOUS AGENTS

24. Gonadal Cytogenetic Damage from Exposure to Extrinsic Agents

APPENDICES
A. Ideograms of Human Chromosomes, and Haploid Autosomal
Lengths
B. Cytogenetic Abbreviations and Nomenclature
C. Determining 95 Percent Confidence Limits, and the Standard
Error

References
Index

16
 PART ONE
BASIC CONCEPTS

17
 1
ELEMENTS OF MEDICAL
CYTOGENETICS

CHROMOSOMES WERE first seen and named in the late nineteenth

century. Chromosome is a combination of Greek words meaning colored
(chrom) body (soma); the word was coined by the illustrious German
anatomist Heinrich Wilhelm Gottfried von Waldeyer-Hartz. It was early
appreciated that these brightly staining objects appearing in the cell
nucleus must be the “stuff of heredity,” the very vessels of our genetic
inheritance. Most observers had concluded, in the earlier part of the
twentieth century, that the human chromosome count was 48. It was not
until the 1950s, due to technical advances, and in particular the use of a
hypotonic solution to swell the cells, giving an uncluttered view of the
chromosomes, that Joe Hin Tjio and Albert Levan could recognize that 46
was the correct number. This discovery spurred research into conditions in
which a chromosomal cause had hitherto been suspected, and in 1959 (“the
wonderful year of human cytogenetics”) came the first demonstrations of a
medical application of the new knowledge, with practically simultaneous
discoveries of the chromosomal basis of Down syndrome, Klinefelter
syndrome, and Turner syndrome (Lejeune et al.1 1959; Jacobs and Strong
1959; Ford et al. 1959); these were followed soon thereafter by the
recognition of the other major aneuploidy syndromes. Harper (2006)
records the history, and the personalities behind the history, in his book
First Years of Human Chromosomes—a book that should be read by every
student of medical cytogenetics with an interest in how their discipline
came to be. Harper points out that the practice of genetic counseling came
into its own essentially upon the basis of these chromosomal discoveries:
So to speak, geneticists now had “their organ.”
“Colored bodies” became an especially apt derivation with the
development of various different staining techniques in the 1980s and
1990s, showing different parts of chromosomes in many different colors,

18
whether true or computer-generated false colors. The images produced by
this kaleidoscopic karyotyping could be rather beautiful. Black-and-white
photographs were less splendid but often sufficed (Figure 1–1). Albeit that
molecular methodologies have substantially taken over from classical
cytogenetics, and providing a different view of the genetic material, the
word chromosome will surely last forever.

FIGURE 1–1 The appearance of banded chromosomes, from a classical

cytogenetic study.

Chromosomal Morphology
Chromosomes have a linear appearance: two arms that are continuous at
the centromere. Reflecting the French influence in the establishment of the
cytogenetic nomenclature, the shorter arm is designated p (for petit), and
the longer is q (variously explained as being the next letter in the alphabet,
a mistyping of g (for grand), for queue, or as the other letter in the formula

19
p + q = 1). In the early part of the cell cycle, each chromosome is present
as a single structure, a chromatid, a single DNA molecule. During the cell
cycle, the chromosomes replicate, and two sister chromatids form. Now
the chromosome exists as a double-chromatid entity. Each chromatid
contains exactly the same genetic material. This replication is in
preparation for cell division so that, after the chromosome has separated
into its two component chromatids, each daughter cell receives the full
amount of genetic material. It is during mitosis that the chromosomes
contract and become readily distinguishable on light microscopy.
Blood and buccal mucosal cells are the tissues from which DNA is
extracted in routine chromosome analysis. From blood, the nucleated
white cell is the tested component for microarray analysis, and in classical
cytogenetic analysis, it is the lymphocyte. Buccal mucosal cells and white
blood cells2 are obtained from a saliva sample. The chromosomal status of
each small sample is taken as representative of the constitution of
(essentially) every other cell of the body. In the case of invasive prenatal
diagnosis, the cells from amniotic fluid or chorionic villi are the source
material; these tissues are assumed (with certain caveats) to represent the
fetal chromosomal constitution. Noninvasive prenatal diagnosis exploits
the presence of fetal blood cells and DNA in the maternal circulation.
The 46 chromosomes come in 23 matching pairs and constitute the
genome. One of each pair came from the mother, and one from the father.
For 22 of the chromosome pairs, each member (each homolog) has the
same morphology in each sex: These are the autosomes. The sex
chromosome (or gonosome) constitution differs: The female has a pair of
X chromosomes, and the male has an X and a Y chromosome. The single
set of homologs—one of each autosome plus one sex chromosome—is the
haploid set. The haploid number (n) is 23. The haploid complement exists,
as such, only in the gametocytes (ovum and sperm). All other cells in the
body—the soma—have a double set: the diploid complement (2n) of 46. If
there is a difference between a pair of homologs, in the sense of one being
structurally rearranged, the person is described as a heterozygote.
The chromosomes are classically distinguishable on the basis of their
size, centromere position, and banding pattern. The centromere may be in
the middle, off-center, or close to one end—metacentric, submetacentric,
and acrocentric, respectively. The chromosomes are numbered 1 through
22, and X and Y, and are also assigned to groups A through G, according
to their general size and the position of the centromere. The diagrammatic
representation of the banding pattern is the ideogram (Appendix A). The
numbering is based on size, largest to smallest (to split hairs, this order is

20
not exact; for example, chromosomes 10 and 11 are shorter than
chromosome 12, and chromosome 21 is smaller than 22).
The classical format of a chromosome display, the “karyotype,” has the
chromosomes lined up with p arms upward, in their matching pairs (Figure
1–2). Those coming from a DNA-based view may see the chromosome
lying on its side, and microarray reports usually show a horizontal
depiction of the chromosome arms, with the graph indicating duplications
and deletions by a rise or a fall compared to baseline, respectively
(although no one is proposing that short and long arms be renamed as left
and right!). Karyotypes are described according to a shorthand notation,
the International System of Human Cytogenetic Nomenclature (ISCN
2016); an outline is given in Appendix B.

FIGURE 1–2 Chromosomes arranged as a formal karyotype, from a classical

cytogenetic study.

Chromosomal Structure
Chromatin exists in differently condensed forms: the less condensed

21
euchromatin and the more condensed heterochromatin. Euchromatin
contains the coding DNA—the genes—while heterochromatin comprises
noncoding DNA. Chromosomes are capped at the terminal extremities of
their long and short arms by telomeres, specialized DNA sequences
comprising many repeats of the sequence TTAGGG, that can be thought of
as sealing the chromatin and preventing its fusion with the chromatin of
other chromosomes. The centromere 3 is a specialized region of DNA that,
at mitosis, provides the site at which the spindle apparatus can be anchored
and draw each separated chromatid to opposite poles of the dividing cell.
Centromeric heterochromatin contains “satellite DNA,” so-called because
these DNA species have different buoyant densities and produce distinct
humps on a density gradient distribution. (These are not to be confused
with the satellites on acrocentric chromosomes.) A separate issue, of
considerable academic interest (but which we shall take no further here), is
the “packaging question”: how the centimeters of DNA are compacted into
micron-length chromosomes, and which parts of the nucleus each
chromosome occupies (Annunziato 2008; Lieberman-Aiden et al. 2009).

CHROMOSOME ABNORMALITY
Chromosomes are distributed to each daughter cell during cell division in a
very precise process—precise, but prone to error. From our perspective,
the two cell divisions of meiosis, during which the gametes are formed, are
of central importance. Most of the discipline of medical cytogenetics
focuses on the consequences of disordered meiosis having produced a
chromosomally abnormal gamete, causing a chromosomal abnormality in
the conceptus. A chromosome abnormality that is present from conception
and involves the entire body is a constitutional abnormality. If an
additional cell line with a different chromosomal complement arises before
the basis of the body structure is formed (that is, in embryonic or pre-
embryonic life) and becomes an integral part of the organism,
constitutional mosaicism results. In this book, we concern ourselves
practically solely with constitutional abnormalities. Acquired
chromosomal abnormality of course exists, and indeed it is a major
initiating and sustaining cause in most cancers, a fact first proposed by
Boveri in 1914 and voluminously attested in the work of Mitelman et al.
(2016); but this is more the field of study of the molecular pathologist than
the genetic counselor.
An incorrect amount of genetic material carried by the conceptus
disturbs and distorts its normal growth pattern (from zygote → blastocyst

22
→ embryo → fetus). In trisomy, there is three of a particular chromosome,
instead of the normal two. In monosomy, only one member of the pair is
present. Two of each is the only combination that works properly! It is
scarcely surprising that a process as exquisitely complex as the
development of the human form should be vulnerable to a confused
outflow of genetic instruction from a nucleus with a redundant or
incomplete database.
Trisomy and monosomy for a whole chromosome were the first
cytogenetic mechanisms leading to an abnormal phenotype to be
identified. More fully, we can list the following pathogenetic mechanisms
that arise from chromosomal abnormalities:

1. A dosage effect, with a lack (deletion) or excess (duplication) of

chromosomal material, whether for a whole chromosome or a part of a
chromosome. This is by far the predominant category.
2. A direct damaging effect, with disruption of a gene at the breakpoint
of a rearrangement
3. An effect due to the incongruent parental origin of a chromosome or
chromosomal segment (genomic imprinting)
4. A position effect, whereby a gene in a new chromosomal
environment functions inappropriately
5. Combinations of the above

We discuss these mechanisms in more detail in following chapters.

Autosomal Imbalance
STRUCTURAL IMBALANCE
As noted earlier, imbalance may involve the gain or loss of a whole
chromosome—full aneuploidy—or of part of a chromosome—partial
aneuploidy. The abnormality may occur in the nonmosaic or mosaic state.
Loss (that is, monosomy) of chromosomal material generally has a more
devastating effect on growth of the conceptus than does an excess of
material (that is, trisomy). Certain imbalances lead to certain abnormal
phenotypes. The spectrum is listed in outline in Box 1–1. Most full
autosomal trisomies and virtually all full autosomal monosomies set
development of the conceptus so awry that, sooner or later, abortion occurs
—the embryo “self-destructs” and is expelled from the uterus. This issue is
further explored in Chapter 19. A few full trisomies are not necessarily

23
lethal in utero, and many partial chromosomal aneuploidies are associated
with survival through to the birth of an infant.

Box 1–1 The Spectrum of Effects, in Broad Outline, Resulting from

Constitutional Chromosomal Abnormality

1. Devastation of blastogenesis, with transient implantation or

nonimplantation of the conceptus
2. Devastation of embryogenesis, with spontaneous abortion, usually in
the first trimester
3. Major disruption of normal intrauterine morphogenesis, with
stillbirth or early neonatal death
4. Major disruption of normal intrauterine morphogenesis, but with
some extrauterine survival
5. Moderate distortion of normal intrauterine development, with
substantial extrauterine survival and severe mental retardation
6. Mild distortion of normal intrauterine development, with substantial
extrauterine survival, and considerable intellectual compromise
7. Minimal physical phenotypic effect, varying degrees of intellectual
compromise; possible compromise of fertility
8. No discernible physical phenotypic effect; cognitive function within
the normal range, but less than expected from the family background

Characteristically, “survivable imbalances” produce a phenotype of

widespread dysmorphogenesis, and there may be malformation of internal
organs and limbs. It is often in the facial appearance (facies) that the most
recognizable physical abnormality is seen, with Down syndrome the
classic example, although the physical phenotype in some cases of subtler
deletion or duplication may be rather “bland.” The most complex organ of
all, the brain, is the most vulnerable to a less than optimal genetic
constitution, and some compromise of mental and intellectual functioning,
usually to the extent of an obvious deficit, is nearly invariable, at least in
imbalances of classical size. With several of the (much smaller)
imbalances due to copy number variants, developmental delay or mental
retardation4 with an outwardly normal physical phenotype is well
recognized as a chromosomal presentation. Thus, the central concern of
most people seeking genetic counseling for a chromosomal condition is
that of having a child who might have a physical, intellectual, or severe

24
social handicap.
Historically, the chromosomal basis of many syndromes was identified
following analysis of groups of patients with similar phenotypes. This
“phenotype-first” approach led to the identification of many of the well-
known microdeletion syndromes (and of course such classic conditions as
Down syndrome). With the advent of microarray analysis, new syndromes
came to be identified based on their DNA aberration, a “genotype-first”
approach. Representative examples of these newer syndromes are
reviewed in Chapter 14.

SEX CHROMOSOMAL ABNORMALITY

Sex chromosome (gonosome) imbalance has a much less deleterious effect
on the phenotype than does autosomal aneuploidy. The X chromosome is
one of the larger and is gene-dense; the Y is small, comprising mostly
heterochromatin, and carries very few genes. In both male and female,
one, and only one, completely functioning X chromosome is needed. X
chromosomes in excess of one are inactivated, as the normal 46,XX
female exemplifies; her second X does, however, maintain some segments
genetically active. With X chromosome excess or deficiency, a partially
successful buffering mechanism exists whereby the imbalance is
counteracted, in an attempt to achieve the same effect as having a single
active X. In such states as, for example, XXX, XXY, XXXX, XXYY, and
XXXXX, excess X chromosomes are inactivated. In the 45,X state, the
single X remaining is not subject to inactivation. If an abnormal X
chromosome (e.g., an isochromosome, or a deleted X) is present, then, as a
rule, cells containing this abnormal chromosome as the active X are
selected against, perhaps due to preferential growth of those cells in which
it is the normal X that is the active one. In X imbalance, the reproductive
tract and brain are the organs predominantly affected. The effect may be
minimal. As for Y chromosome excess, such as XYY, there is a rather
limited phenotypic consequence, but again the brain may be a vulnerable
organ.

FUNCTIONAL IMBALANCE
A correct amount of chromatin does not necessarily mean the phenotype
will be normal. Inappropriate inactivation, or activation, of a segment of
the genome can compromise the genetic message. Some segments of the
genome require only monosomic expression, and the homologous segment

25
on the other chromosome is inactivated. If this control fails, both segments
can become activated, or both inactivated, and the over- or under-
expression of the contained loci can cause phenotypic abnormality. The
classic example of this is genomic imprinting according to parent of origin,
and we discuss this concept in Chapter 18. A rather specialized example
arises with the X-autosome translocation. A segment of X chromosome
can fail to be inactivated; or conversely, X-inactivation can spread into an
autosomal segment (Chapter 6).

The Frequency and Impact of Cytogenetic Pathology

According to the window of observation, chromosomal disorders make a
greater or lesser contribution to human mortality and morbidity. Looking
at prenatal existence, the earliest window has been provided by the in vitro
fertilization (IVF) clinic, from the procedure of preimplantation genetic
diagnosis (Chapter 22), at which cells taken from 3- to 5-day-old embryos
are subjected to genetic analysis; and an extraordinary fraction are
chromosomally abnormal. After implantation (about day 6), and through
the first trimester of pregnancy (to week 13), chromosomal mortality is
very high, and aneuploidy is the major single cause of spontaneous
abortion (Chapter 19). Perinatal and early infant death has a significant
chromosomal component, of which trisomies 18 and 21 (although the
latter less so in more recent times) are major elements.
As for morbidity, the brain, as mentioned above, is the most vulnerable
organ, and chromosomal defects are the basis of a substantial fraction of
all intellectual deficit, and many of these retarded individuals will also
have structural malformations that cause functional physical disability.
Among a mentally retarded population, Down syndrome is the
predominant contributor in the fraction who have a classic chromosome
abnormality (Phelan et al. 1996). Development of the heart is particularly
susceptible to chromosomal imbalance, and in a population study from the
US National Center on Birth Defects, 1 in 8 infants with a congenital heart
defect had a chromosomal abnormality, with again trisomy 21 the most
common of these (53%), followed by trisomy 18 (13%), 22q11.2 deletion
(12%), and trisomy 13 (6%) (Hartman et al. 2011).
Adolescence is a period during which many sex chromosome defects
come to light, when pubertal change fails to occur; and in young
adulthood, chromosomal causes of infertility are recognized. Few new
classic cytogenetic defects come to attention later in adult life, but many

26
retarded children survive well into adulthood and some into old age, and
some require lifelong care from their families or from the state. This latter
group imposes a considerable emotional and financial burden. While some
parents and caregivers declare the emotional return they have from looking
after these individuals, for others this responsibility is a source of
continuing, unresolved, if attenuated, grief.
In Table 1–1 we set out the birth incidences of the various categories of
(classical) chromosomal abnormality; these data are from a Danish study,
one of a number that have examined this question in the later decades of
the twentieth century, with largely similar findings in each. Overall,
around 1 in 135 liveborn babies have a classical chromosomal
abnormality, and about 40% of these are phenotypically abnormal due to
the chromosome defect. If we were to look at day-5 blastocysts, the
fraction with abnormality might be close to a half. Fertile adults
(ascertained by virtue of having presented for noninvasive prenatal testing)
have much lower frequencies of sex chromosome aneuploidy (Samango-
Sprouse et al. 2016). If we studied a population of 70-year-olds, we could
expect to see very few individuals with an unbalanced autosomal
karyotype.

Table 1–1. Classical Chromosomal Rearrangements and Imbalances,

Recorded in 34,910 Live Newborns in Århus, Denmark, over a Total
13-Year Period, 1969–1974 and 1980–1988
BIRTH
NO. OF PER FREQUENCY
CASES 1,000a PER GROUP
Sex Chromosomes
Klinefelter Syndrome and Variants
47,XXY 20 1.12b
47,XXY/46,XY 7 0.39
46,XX 2 0.11
1 in 616 ♂
XYY
47,XYY 18 1.01
47,XYY/46,XY 2 0.11

27
 1 in 894 ♂
XXX
47,XXX 17 1.00
1 in 1,002 ♀
Turner Syndrome and Variants
45,X 1 0.06
45,X/46,XX and 45,X/47,XXX 3 0.18
45,X/46,X,r(X) 1 0.06
45,X/46,X,i(Xq)/47,X,i(Xq),i(Xq) 1 0.06
Other Turner variant 2 0.12
1 in 2,130 ♀
Other
45,X/46,XY 1 0.06
46,XX/47,XX,del(Yq) 1 0.06
46,XX/46,XY 1 0.06
Total 77 2.21 1 in 453
Autosomes
Unbalanced Forms
Trisomy 13 2 0.06
Trisomy 18 7 0.20
Trisomy 21 51 1.46
Trisomy 8 1 0.03
Supernumerary marker, ring 25 0.72
Deletions, duplications 6 0.17
1 in 379
Balanced Forms
Robertsonian 13/14 translocation 34 0.97
Other Robertsonian 9 0.26

28
Reciprocal translocations 50 1.43
Inversions (other than of 4 0.11
chromosome 2)
1 in 360
Combined sex plus autosomal 266 7.62 1 in 131
totals
Combined totals, excluding 169 4.84 1 in 207
balanced autosomal forms
Notes: Not included in the 34,910 live newborns listing are four cases of induced
abortion due to sex chromosome prenatal diagnosis, involving the karyotypes
47,XXY, 47,XYY, 47,XXX, and 45,X/46,X,del(Xq), and 15 cases of autosomal-
diagnosis induced abortions, involving the karyotypes +21, +13, +18, and three
different derivative chromosomes. Had these pregnancies proceeded to term, the
frequencies in the relevant group category would have been marginally increased.
These figures might continue to be broadly valid into this century, except that
the category of deletions and duplications will substantially increase due to the
more powerful detection now offered by molecular technology.
a
Per 1,000 male, per 1,000 female, or per 1,000 both, as appropriate. The
gender-specific denominators in this study were 17,872 males and 17,038 females.
b
An increasing incidence of XXY in recent years has been suggested, and an
Australian study, including data up to 2006, arrived at a figure of 1.91 per 1,000
(Herlihy and Halliday 2008; Morris et al. 2008; Herlihy et al. 2010).
Source: From Nielsen and Wohlert (1991)

The finer the cytogenetic focus, the greater the incidence, and it is now a
task for the cytogenetic epidemiologist of this century, in the
microarray/molecular era, to derive new estimates of cytogenetic
abnormalities in the different populations (Rosenfeld et al. 2013). The
brain again declares its susceptibility, with many examples of a brain-only
phenotype (intellectual disability, epilepsy, autism, psychiatric disease)
due to microduplications and microdeletions detectable only on molecular
karyotyping, and chromosomes 15 and 16, in particular, represented.

THE RESEARCH APPLICATION OF CYTOGENETIC

PATHOLOGY
The phenotypes that result from chromosome abnormalities can point the

29
Exploring the Variety of Random
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