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Other companion titles in the Rheumatology series

Ankylosing Spondylitis and the Spondyloarthropathies

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OSTEOPOROSIS AND THE OSTEOPOROSIS OF RHEUMATIC DISEASES ISBN-13: 9780323 034371

A COMPANION TO RHEUMATOLOGY ISBN-10: 0-323-03437-3
Copyright © 2006 Mosby, Inc, an affiliate of Elsevier Inc.

All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means,
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Notice

Knowledge and best practice in this field are constantly changing. As new research and experience broaden
our knowledge, changes in practice, treatment, and drug therapy may become necessary or appropriate.
Readers are advised to check the most current information provided (i) on procedures featured or (ii) by the
manufacturer of each product to be administered, to verify the recommended dose or formula, the method
and duration of administration, and contraindications. It is the responsibility of the practitioner, relying on
his or her own experience and knowledge of the patient, to make diagnoses, to determine dosages and the best
treatment for each individual patient, and to take all appropriate safety precautions. To the fullest extent of
the law, neither the Publisher nor the Authors assume any liability for any injury and/or damage to persons or
property arising out of or related to any use of the material contained in this book.

Library of Congress Cataloging-in-Publication Data

Osteoporosis and the osteoporosis of rheumatic diseases: a companion to Rheumatology /
[editors] Nancy E. Lane, Philip N. Sambrook.–1st
p. ; cm.
Includes bibliographical references and index.
ISBN 0-323-03437-3
1. Osteoporosis. 2. Rheumatism–Complications. I. Lane, Nancy E. II. Sambrook, Philip N. III.
Rheumatology.
[DNLM: 1. Osteoporosis. 2. Rheumatic Diseases–complications. WE 250 085116 2006]
RC931.O73O88 2006
616.7'16–dc22
2005058428

Acquisitions Editor: Kimberly Murphy

Developmental Editor: Denise Lemelledo
Publishing Services Manager: Frank Polizzano
Senior Project Manager: Natalie Ware
Design Direction: Gene Harris

Printed in the United States of America.

Last digit is the print number: 9 8 7 6 5 4 3 2 1

We would like to dedicate this text to our parents (living or blessed memory),
our wives or husbands, and children:
Fred. M. Tileston, Jr., Trevor Lane Tileston, and Reid Lane Tileston.
Brenda L. Sambrook, Andrew M. Sambrook, and Kate L. Sambrook
 Contributors

Jonathan (Rick) Adachi, MD Jean-Pierre Devogelaer, MD

Professor of Medicine, Alliance for Better Bone Professor of Rheumatology, Université Catholique
Health; Chair in Rheumatology, McMaster de Louvain; Associate Head, Department of
University, Hamilton; Director, Hamilton Arthritis Rheumatology, Saint-Luc University Hospital,
Center; Head of Rheumatology, St. Joseph’s Brussels, Belgium
Healthcare, Hamilton, Ontario, Canada The Pathogenesis of Glucocorticoid-Induced
The Use of Calcium Supplementation in the Bone Loss
Management and Prevention of Osteoporosis
Kenneth G. Faulkner, PhD
Kristina Åkesson, MD, PhD Vice President of Business Development, Synarc, Inc.,
Associate Professor, Senior Lecturer, Faculty of San Francisco, California
Medicine, Lund University, Department of Clinical Investigations of Bone: Densitometry
Sciences, Malmo; Senior Consultant, Department of
Orthopedics, Malmo University Hospital, Malmo, Patrick Garnero, PhD, DSC
Sweden Vice President, Molecular Markers, Synarc, and
The Patient with Osteoporosis Senior Research Scientist INSERM 403, Lyon,
France
Yves Boutsen, MD Biochemical Markers of Bone Turnover
Professor, Louvain University, Yvoir, Head,
Department of Rheumatology, University Hospital in Piet P.M.M. Geusens, MD, PhD
Mont-Godinne, Yvoir, Belgium Professor, Department of Rheumatology, University
The Pathogenesis of Glucocorticoid-Induced Bone Loss Hospital, Maastricht, The Netherlands; Professor,
Biomedical Research Institute, Limburgs Universitair
David B. Burr, PhD Centrum, Diepenbeek, Belgium
Professor and Chairman of Anatomy; Professor of The Evaluation of the Patient for Osteoporosis: Case
Orthopedic Surgery and Biomedical Engineering, Finding Using Diagnostic Tests for Treatment
Indiana University-Purdue University, Indianapolis, Interventions
Indiana
Principles of Bone Biomechanics David J. Handelsman, MB, BS, PhD, FRACP
Director, ANZAC Research Institute; Head,
Cyrus Cooper, MA, DM, FRCP, FMedSci Department of Andrology, Concord
Professor of Rheumatology, The MRC Epidemiology Hospital, University of Sydney, Sydney,
Resource Centre, University of Southampton, Australia
Southampton General Hospital, Southampton, Sex Steroids and Skeletal Health in Men
United Kingdom
The Epidemiology of Osteoporotic Fractures Nicholas Harvey, MAMB, B.Chir, MRCP
Clinical Research Fellow, The MRC Epidemiology
Elaine Dennison, MA, MB, B.Chir, MSc, PhD Resource Centre, University of Southampton,
Senior Lecturer, The MRC Epidemiology Resource Southampton General Hospital, Southampton,
Centre, University of Southampton, Southampton United Kingdom vii
General Hospital, Southampton, United Kingdom The Epidemiology of Osteoporotic Fractures
The Epidemiology of Osteoporotic Fractures
 CONTRIBUTORS

Marc C. Hochberg, MD, MPH Daniel Henri Manicourt, MD, PhD

Professor of Medicine and Epidemiology and Professor, School of Medicine, Université Catholique
Preventive Medicine; Head Division of Rheumatology de Louvain, Brussels; Head of Clinic in
and Clinical Immunology, University of Maryland Rheumatology, Saint-Luc University Hospital,
School of Medicine, Baltimore, Maryland Department of Rheumatology, Brussels, Belgium
Recommendations for Performing Bone Densitometry to The Pathogenesis of Glucocorticoid-Induced Bone Loss
Diagnose Osteoporosis and Identify Persons to Be
Treated for Osteoporosis Christian Meier, MD
Clinic for Endocrinology, Diabetology, and
Mary Beth Humphrey, MD, PhD Clinical Nutrition, University of Basel, Basel,
Assistant Professor, Department of Medicine and Switzerland
Microbiology and Immunology, University of Sex Steroids and Skeletal Health in Men
California San Francisco, San Francisco, California
Pathogenesis of Inflammation-induced Bone Loss Paul D. Miller, MD
Clinical Professor of Medicine, University of
Graeme Jones, MBBS, FRACP, MD, MmedSc, Colorado Health Sciences Center, Denver; Medical
FAFPHM Director, Colorado Center for Bone Research,
Professor of Rheumatology and Epidemiology, Lakewood, Colorado
Menzies Research Institute, University of Tasmania, Combination Therapy for Osteoporosis: What Do the
Hobart, Tasmania Data Show Us?
Relevance of Peak Bone Mass to Osteoporosis and
Fracture Risk in Later Life Mary C. Nakamura, MD
Associate Professor of Medicine, in residence,
Dina Kulik Division of Rheumatology, Department of Medicine,
Student in MD Programme, McMaster University, University of California San Francisco; Staff
Hamilton, Ontario, Canada Physician, San Francisco Veterans Affairs Medical
The Use of Calcium Supplementation in the Center, San Francisco, California
Management and Prevention of Osteoporosis Pathogenesis of Inflammation-induced Bone Loss

Nancy E. Lane, MD
Ian R. Reid, MD
Director and Distinguished Professor Aging Center,
Professor of Medicine and Endocrinology, University
Medicine and Rheumatology, University
of Auckland, Auckland, New Zealand
of California at Davis Medical Center, Sacramento,
Bisphosphonates in the Prevention and Treatment
California
of Postmenopausal Osteoporosis
Parathyroid Hormone for the Treatment of
Osteoporosis: The Science and the Therapy;
Corticosteroid-Induced Osteoporosis Evange Romas, MBBS, FRACP, PhD
Senior Lecturer, University of Melbourne; Senior
Peter Y. Liu, MBBS, PhD Consultant, Department of Rheumatology,
Postdoctoral Research Fellow, Department of St. Vincent’s Hospital, Melbourne, Australia
Andrology, Concord Hospital and ANZAC Research The Prevention and Treatment of Inflammation-
Institute, University of Sydney, Sydney, Australia induced Bone Loss: Can It Be Done?
Sex Steroids and Skeletal Health in Men
Graham Russell, PhD, DM, FRCP, PRC Path,
Sharmila Majumdar, PhD F Med Sci
Professor, Department of Radiology, University of Norman Collisson Professor of Musculoskeletal
California San Francisco, San Francisco, California Sciences, Institute Director and Head of
Imaging Bone Structure and Osteoporosis Using MRI Department, The Botnar Research Centre and
Oxford University Institute of Musculoskeletal
Naim M. Maalouf, MD Sciences, Nuffield Department of Orthopedic
Assistant Professor of Internal Medicine, University Surgery, Nuffield Orthopedic Centre, Headington,
of Texas Southwestern Medical Center, Dallas, Texas United Kingdom
Osteoporosis After Solid Organ Transplantation Pathogenesis of Osteoporosis
viii
 Contributors
Philip N. Sambrook, MD FRACP Luigi Sinigaglia, MD
Florance and Cope Professor of Rheumatology, Chair, Department of Rheumatology, Gaetano Pini
University of Sydney; Head, Department of Institute, University of Milan, Milan, Italy
Rheumatology, Royal North Shore Hospital, Epidemiology of Osteoporosis in Rheumatic Diseases
St. Leonard’s, Sydney, Australia
Vitamin D and Its Metabolites in the Prevention and Tim D. Spector, MD, MSc, FRCP
Treatment of Osteoporosis; Selective Estrogen Receptor Consultant Rheumatologist, Twin Research and
Modulators (SERMs); Corticosteroid-Induced Genetic Epidemiology Unit, St. Thomas’ Hospital;
Osteoporosis Honorary Professor in Genetic Epidemiology,
St. Geroge’s Medical School, London, United Kingdom
Ego Seeman, BSc, FRACP, MD The Genetics of Osteoporosis
Professor of Medicine and Endocrinology, Austin and
Repatriatian Medical Center, University of Charles H. Turner, PhD
Melbourne, Melbourne, Australia Professor of Biomedical Engineering and Orthopedic
Exercise and the Prevention of Bone Fragility Surgery, Indiana University-Purdue University
Indianapolis, Indianapolis, Indiana
Principles of Bone Biomechanics
Markus J. Seibel, MD, PhD
Professor and Chair of Endocrinology; Director, Bone Massimo Varenna, MD
Research Program, ANZAC Research Institute, Professor, Department of Rheumatology, Istituto
University of Sydney; Head, Department of Ortopedicao Gaetano Pini, University of Milan,
Endocrinology, Concord Hospital, Sydney, Australia Milan, Italy
Sex Steroids and Skeletal Health in Men Epidemiology of Osteoporosis in Rheumatic Diseases

Elizabeth Shane, MD Sarah Westlake, BM, MRCP

Professor of Clinical Medicine, College of Physicians Specialist Registrar, The MRC Epidemiology
and Surgeons, Columbia University; Attending Resource Centre, University of Southampton,
Physician in Medicine, Columbia University Medical Southampton General Hospital, Southampton,
Center, New York, New York United Kingdom
Osteoporosis After Solid Organ Transplantation The Epidemiology of Osteoporotic Fractures

Sandra J. Shefelbine, BSE, MPhil, PhD Frances M.K. Williams, MBBS, MRCP
Lecturer, Department of Bioengineering, Imperial Honorary Senior Research Fellow, Twin Research and
College of London, London, United Kingdom Genetic Epidemiology Unit, St. Thomas’ Hospital,
Imaging Bone Structure and Osteoporosis Using MRI London, United Kingdom
The Genetics of Osteoporosis
Stuart L. Silverman, MD, FACP, FACR
Clinical Professor of Medicine and Rheumatology, Anthony D. Woolf, BSc, MB, BS, FRCP
Cedars-Sinai Medical Center, University of California Professor of Rheumatology, Institute of Health and
Los Angeles, Greater Los Angeles VA Medical Center, Social Care Research, Peninsula Medical School,
and the OMC Clinical Research Center; Medical Universities of Exeter and Plymouth; Consultant
Director, Fibromyalgia Rehabilitation Program, Rheumatologist, Duke of Cornwall Department of
Cedars-Sinai Medical Center, Los Angeles, California Rheumatology, Royal Cornwall Hospital, Truro,
Calcitonin in the Treatment of Osteoporosis Cornwall, United Kingdom
The Patient with Osteoporosis

ix
 Preface

This monograph takes a very in-depth look at the key with anti-resorptive therapies, is associated with a
aspects of osteoporosis and presents significant reduction in incident fracture risk. These detailed
advances that have occurred in the field over the past reviews also emphasize how these markers can be
five years. Specifically, this book gathers the works of used in combination with bone mineral density
the top practitioners in the field to discuss the epi- measurements to educate patients about their poten-
demiology, pathogenetic mechanisms, clinical aspects tial risk for fracture and their responses to different
of the disease, treatment options, and secondary osteo- osteoporosis therapies.
porosis and the osteoporosis of the rheumatic diseases. In the next section we present the available modali-
We discuss bone biology and the new emerging field ties for the prevention and treatment of osteoporosis.
of osteoimmunology, that connects the field of Among them are the most important aspect of any
immunology with inflammatory bone loss. In addi- treatment program, e.g., calcium and vitamin D sup-
tion, we carefully provide up-to-date reviews on the plementation, followed by the anti-resorptive agents,
epidemiology, pathogenesis, diagnosis, and manage- including the selective estrogen receptor modulators
ment of osteoporosis. The epidemiology of osteoporo- (SERMs), androgens, gonadal steroids, and calcitonin,
sis and the role of bone mineral density in the and lastly, bisphosphonates. Anabolic agents, such as
definition and prediction of fractures are reviewed, as PTH, and the use of combination and sequential ther-
well as the most current information on the geograph- apies are also discussed in depth.
ical distribution of the disease. The role of peak bone Lastly, we offer a broad and informative discussion
mass acquisition in the prevention of osteoporosis, and of the newest area of intense investigation: osteoim-
a thoughtful review on who should be treated for munology and the bone loss that is so prevalent in
osteoporosis are included in the first section. inflammatory conditions like rheumatoid arthritis
Section II covers the pathogenesis of osteoporosis, (RA) and systemic lupus erythematosus (SLE). We
and the biomechanics of bone - information any clini- begin with a review on the epidemiology of osteoporo-
cian needs to know on what makes bone strong and sis in RA, SLE, and ankylosing spondolytic (AS)
why it fractures. patients. The pathogenesis of inflammation-induced
The section on the clinical aspects of the disease bone loss and the treatment of inflammation-induced
covers the latest technologies for imaging bone bone loss are also covered.
structure and biomechanical markers of bone Throughout this book, there has been an emphasis
metabolism. This part of the text is unique in that we on the advances in scientific knowledge as they relate
review not only the use of DXA and QCT, but also to the biology of postmenopausal bone loss and
the latest technologies being applied in clinical inflammation-induced bone loss in both women and
research, including MRI, that can assess bone struc- men, and on the diagnosis and therapy for the preven-
ture and apply sophisticated non-invasive modeling tion and treatment of established disease. Although
to assess bone strength. There has also been a this book presents major advances in the understand-
tremendous increase in the number of biochemical ing and treatment of osteoporosis, many outstanding
tests that measure proteins associated with both questions remain to be addressed. We hope that the
bone formation and resorption. In some studies, next edition of this monograph will answer some of
these biochemical markers of bone turnover appear these questions.
to be surrogate markers for increased risk of fracture. Nancy E. Lane, MD
Also, in some studies, the reduction in thee markers Philip N. Sambrook, MD xi
 Acknowledgments

The editors would like to acknowledge all of the authors who contributed to this monograph
on osteoporosis. In addition, we thank Mollie McGee for her editorial assistance.

xiii
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Color Plates
Color Plate.qxd 4/5/06 10:40 PM Page 2

Figure 1-2. Hip fracture incidence GEOGRAPHICAL VARIATION IN HIP FRACTURE INCIDENCE
around the world. (Data derived
from Kanis JA et al.20) Men Women
1400

Incidence (per 105 Person-years)

1200

1000

800

600

400

200

0
Europe N. America/ Latin Asia Europe N. America/ Latin Asia
Oceania America Oceania America

HIP FRACTURE PROJECTIONS Figure 1-3. Estimated numbers of hip

fractures among men and women in
3,500 Men Women different regions of the world in
1990 1990 and 2050.
3,000
2025

2,500 2050
Hip fractures, 000s

2,000

1,500 Men Women

1,000

500

0
North America, Middle East, Asia,
Europe, Oceania, Latin America,
and Russia and Africa
Region

Figure 1-6. Health-related quality of life

AGE, NUMBER OF VERTEBRAL
related to age and number of vertebral
DEFORMITIES, AND HRQOL
deformities.

45
Mean QUALEFFO
total score

35 Age >71

Age 65–71
25
Age <65
15
*Age p = 0.020
e

es
e
ur

ur

ur

ur

*Fracture p < 0.001

ct

ct

ct

ct
fra

fra

2
fra

fra
o

3
N

≥
Color Plate.qxd 4/5/06 10:40 PM Page 3

PREVALENCE OF VERTEBRAL DEFORMITY Figure 1-7. Prevalence of vertebral deformity,

(EVOS) European Vertebral Osteoporosis Study
(EVOS).
25
Men
Women
20
Prevalence (%)

15

10

0
50 55 60 65 70 75
Age (years)

Figure 1-8. Cumulative incidence of a RISK OF SUBSEQUENT FRACTURE

subsequent vertebral fracture over time
AFTER INITIAL VERTEBRAL FRACTURE
after a baseline event.
100
Men
Women
80
Cumulative incidence (%)

60

40

20

0
0 1 2 3 4 5 6 7 8 9 10
Years following vertebral fracture

3
Color Plate.qxd 4/5/06 10:40 PM Page 4

OSTEOPOROSIS SELF-ASSESSMENT TABLE FOR WOMEN*

90 100 110 120 130 140 150 160 170 180 190 200 210 220 230 240 250 260 270
30 2 3 3 4 5 6 7 8 9 10 11 12 13 13 14 15 16 17 18

33 1 2 3 4 5 6 7 7 8 9 10 11 12 13 14 15 16 16 17

36 0 1 2 3 4 5 6 7 8 9 10 10 11 12 13 14 15 16 17

39 0 1 2 3 3 4 5 6 7 8 9 10 11 12 13 13 14 15 16

41 0 0 1 2 3 4 5 6 7 8 9 9 10 11 12 13 14 15 16

44 0 0 1 2 2 3 4 5 6 7 8 9 10 11 12 12 13 14 15

47 –1 0 0 1 2 3 4 5 6 6 7 8 9 10 11 12 13 14 15

50 –1 0 0 0 1 2 3 4 5 6 7 8 9 9 10 11 12 13 14

53 –2 –1 0 0 1 2 3 3 4 5 6 7 8 9 10 11 12 12 13

56 –3 –2 –1 0 0 1 2 3 4 5 6 6 7 8 9 10 11 12 13

59 –3 –2 –1 0 0 0 1 2 3 4 5 6 7 8 9 9 10 11 12

61 –4 –3 –2 –1 0 0 1 2 3 4 5 5 6 7 8 9 10 11 12
Age (years)

64 –4 –3 –2 –1 –1 0 0 1 2 3 4 5 6 7 8 8 9 10 11

67 –5 –4 –3 –2 –1 0 0 1 2 2 3 4 5 6 7 8 9 10 11

70 –5 –4 –4 –3 –2 –1 0 0 1 2 3 4 5 5 6 7 8 9 10

73 –6 –5 –4 –3 –2 –1 0 0 0 1 2 3 4 5 6 7 8 8 9

76 –7 –6 –5 –4 –3 –2 –1 0 0 1 2 2 3 4 5 6 7 8 9

79 –7 –6 –5 –4 –4 –3 –2 –1 0 0 1 2 3 4 5 5 6 7 8

81 –8 –7 –6 –5 –4 –3 –2 –1 0 0 1 1 2 3 4 5 6 7 8

84 –8 –7 –6 –5 –5 –4 –3 –2 –1 0 0 1 2 3 4 4 5 6 7

87 –9 –8 –7 –6 –5 –4 –3 –2 –1 –1 0 0 1 2 3 4 5 6 7

90 –9 –8 –8 –7 –6 –5 –4 –3 –2 –1 0 0 1 1 2 3 4 5 6

93 –10 –9 –8 –7 –6 –5 –4 –4 –3 –2 –1 0 0 1 2 3 4 4 5

96 –11 –10 –9 –8 –7 –6 –5 –4 –3 –2 –1 –1 0 0 1 2 3 4 5

99 –11 –10 –9 –8 –8 –7 –6 –5 –4 –3 –2 –1 0 0 1 1 2 3 4

Weight (pounds)

High risk Moderate risk Low risk

–4 or less –3 to 1 2 or greater

*Based on Osteoporosis Self-assessment tool (OST) formula:

A OST index = (Weight in kg–age in years) multiply by 0.2 and truncate to integer

Figure 4-1. The Osteoporosis Self-assessment Tool index tables for women and men. A. The Osteoporosis Self-assessment Table for
women.

4
Color Plate.qxd 4/5/06 10:40 PM Page 5

OSTEOPOROSIS SELF-ASSESSMENT TABLE FOR MEN*

90 100 110 120 130 140 150 160 170 180 190 200 210 220 230 240 250 260 270
30 2 3 3 4 5 6 7 8 9 10 11 12 13 13 14 15 16 17 18

33 1 2 3 4 5 6 7 7 8 9 10 11 12 13 14 15 16 16 17

36 0 1 2 3 4 5 6 7 8 9 10 10 11 12 13 14 15 16 17

39 0 1 2 3 3 4 5 6 7 8 9 10 11 12 13 13 14 15 16

41 0 0 1 2 3 4 5 6 7 8 9 9 10 11 12 13 14 15 16

44 0 0 1 2 2 3 4 5 6 7 8 9 10 11 12 12 13 14 15

47 –1 0 0 1 2 3 4 5 6 6 7 8 9 10 11 12 13 14 15

50 –1 0 0 0 1 2 3 4 5 6 7 8 9 9 10 11 12 13 14

53 –2 –1 0 0 1 2 3 3 4 5 6 7 8 9 10 11 12 12 13

56 –3 –2 –1 0 0 1 2 3 4 5 6 6 7 8 9 10 11 12 13

59 –3 –2 –1 0 0 0 1 2 3 4 5 6 7 8 9 9 10 11 12

61 –4 –3 –2 –1 0 0 1 2 3 4 5 5 6 7 8 9 10 11 12
Age (years)

64 –4 –3 –2 –1 –1 0 0 1 2 3 4 5 6 7 8 8 9 10 11

67 –5 –4 –3 –2 –1 0 0 1 2 2 3 4 5 6 7 8 9 10 11

70 –5 –4 –4 –3 –2 –1 0 0 1 2 3 4 5 5 6 7 8 9 10

73 –6 –5 –4 –3 –2 –1 0 0 0 1 2 3 4 5 6 7 8 8 9

76 –7 –6 –5 –4 –3 –2 –1 0 0 1 2 2 3 4 5 6 7 8 9

79 –7 –6 –5 –4 –4 –3 –2 –1 0 0 1 2 3 4 5 5 6 7 8

81 –8 –7 –6 –5 –4 –3 –2 –1 0 0 1 1 2 3 4 5 6 7 8

84 –8 –7 –6 –5 –5 –4 –3 –2 –1 0 0 1 2 3 4 4 5 6 7

87 –9 –8 –7 –6 –5 –4 –3 –2 –1 –1 0 0 1 2 3 4 5 6 7

90 –9 –8 –8 –7 –6 –5 –4 –3 –2 –1 0 0 1 1 2 3 4 5 6

93 –10 –9 –8 –7 –6 –5 –4 –4 –3 –2 –1 0 0 1 2 3 4 4 5

96 –11 –10 –9 –8 –7 –6 –5 –4 –3 –2 –1 –1 0 0 1 2 3 4 5

99 –11 –10 –9 –8 –8 –7 –6 –5 –4 –3 –2 –1 0 0 1 1 2 3 4

Weight (pounds)

High risk Moderate risk Low risk

–2 or less –1 to 3 4 or greater

*Based on Osteoporosis Self-assessment tool (OST) formula:

B OST index = (Weight in kg–age in years) multiply by 0.2 and truncate to integer

Figure 4-1. B. The Osteoporosis Self-assessment Table for men.

5
Color Plate.qxd 4/5/06 10:40 PM Page 6

BONE REMODELING

Quiescence Resorption Resorption Formation

(lining cell) (osteoclasts) cavity (osteoblasts)

New bone packet

(plus lining cells)

Figure 5-1. Bone remodeling. The remodeling cycle within bone involves a similar sequence of cellular activity at both cortical
and trabecular sites. Trabecular surfaces are shown here. An initial phase of osteoclastic resorption is followed by a more
prolonged phase of bone formation mediated by osteoblasts. Under normal conditions, the amount of bone removed during
resorption is replaced completely. (From Hochberg et al, Rheumatology, 3rd ed, 2003.)

6
Color Plate.qxd 4/5/06 10:40 PM Page 7

REMODELING IN TRABECULAR BONE RESORPTION PHASE

Resorption cavities
in normal bone

Resorption cavities are

more frequent and possibly
deeper in osteoporotic
bone. Perforations occur
a

REMODELING IN TRABECULAR BONE FORMATION PHASE

Normal
Resorption cavities
completely replaced
by new bone

Osteoporosis
Resorption cavities are
incompletely replaced
by new bone
b

Figure 5-2. Remodeling in trabecular bone. These figures show remodeling under
normal conditions and in osteoporosis. (a) Resorption phase. (b) Formation phase.
There may be subtle differences between the sexes, with bone thinning
predominating in men because of reduced bone formation. Loss of connectivity
and complete trabeculae predominates in women. (From Hochberg et al,
Rheumatology, 3rd ed, 2003.)

7
Color Plate.qxd 4/5/06 10:40 PM Page 8

CHANGES THROUGHOUT LIFE THAT MAY CONTRIBUTE TO OSTEOPOROSIS AND FRACTURES

Fetal and Inadequate

neonatal factors peak bone mass Aging effects

Bone Effects during Menopause and Low bone mass

mass growth lack of estrogen

Increased
bone loss Men
Genetic
factors
Women
Nutritional and life style factors
Pathogenesis
0 10 20 30 40 50 60 70 80 of fracture
syndromes
Years may differ

Figure 5-3. Changes throughout life that may contribute to osteoporosis and fractures. (From Hochberg et al,
Rheumatology, 3rd ed, 2003.)

EFFECT OF AGE ON FRACTURE RISK

Age (years) Bone mass

Fracture risk 160 (g/cm)
per 1000
person–years 140 80+ <0.6

120 0.60–0.69
100 75–79
0.70–0.79
80 70–74 0.80–0.89
60 0.90–0.99
65–69
40 60–64
55–59
50–54
20 45–49 1.0+
<54
0
<1.0 0.90 0.80 0.70 0.60 <0.60 40 45 50 55 60 65 70 75 80+
–0.99–0.89 –0.79–0.69 –49 –54 –59 –64 –69 –74 –79
Bone mass (g/cm) Age (years)

Figure 5-4. Effect of age on fracture risk. Fracture risk increases with age, independent of bone density, and also
increases with declining bone density irrespective of age. (Adapted with permission from Hui et al.14; from
Hochberg et al, Rheumatology, 3rd ed, 2003.)

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Figure 8-2. Full table dual X-ray absorptiometry

system. (From Hochberg: Rheumatology, 3rd ed, 2003.)

Figure 8-3. Vertebral fracture assessment from a dual x-ray absorptiometry image of the spine. Use of dual-energy images
facilitates the visualization of the lumbar and thoracic spine in a single image. In this example, a fracture has been identified at
T12. (From Hochberg: Rheumatology, 3rd ed, 2003.)

9
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B C
Figure 8-6. A, Quantitative ultrasound device for measuring the heel, which incorporates a real-time image for more accurate
assessment. B, Region of interest (ROI) (red) over calcaneus. C, Patient undergoing scan of calcaneus. (From Hochberg:
Rheumatology, 3rd ed, 2003.)

10
Color Plate.qxd 4/5/06 10:40 PM Page 11

CHANGE IN T-SCORES WITH AGE AT DIFFERENT SKELETAL SITES

Heel Total hip PA spine

Forearm Lateral spine QCT spine
T-score 1

–1

–2

–3
T = –2.5
–4

–5

–6
20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95

Age

Figure 8-7. Change in T-scores with age at different skeletal sites. (From
Hochberg: Rheumatology, 3rd ed, 2003.)

11
Color Plate.qxd 4/5/06 10:40 PM Page 12

7,3

5,8

2,1
8
3,6
6
1,6
4
2
1,2
2 0,6

35,0

17,9
23,4
40
5,6
30 10,5 >2
10-year risk

20 2,7
10,6 1 of 2 Other
risk factors
10 2,8 1,4
0
0
Osteoporosis Osteopenia Normal
B BMD category

Figure 11-2. A. Cumulative incidence of first incident vertebral fracture.14 Risk factors are age over 70 years, a prior nonspinal
fracture after age 50, body mass index (calculated with knee height) in the lowest 40%, current smoker, low level of physical
activity (walks less than 1 block/day and does household chores less than 1 h/day), no moderate- or high-intensity
recreational physical activities, fell one or more times in the first 12 months of follow-up, not currently on estrogen
replacement therapy, low milk consumption (<1 glass/day) when pregnant (or as a teenager for nulliparous women), ever
used aluminum-containing antacids weekly, and paternal history of hip fracture. B. Ten-year risk for hip fracture (in
percentages) according to the presence of low bone mineral density (BMD) and other risk factors (age >80 years, mother with
hip fracture, fracture after 50 years of age, decrease in body length, decreased cognitive functions, slow gait speed,
nulliparity, type 2 diabetes, Parkinson disease, disturbed depth vision). Note that the number of risk factors and low BMD
increase the risk of hip fracture independently and additively.15

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CLINICAL SIGNS OF VERTEBRAL FRACTURES

Loss of body height

Occiput-wall distance >0 cm

Hyperkyphosis
“dowager’s hump”

Decreased rib-pelvis distance

Figure 11-4. Common clinical signs of osteoporosis with vertebral fractures.

PREMENOPAUSAL WOMEN POSTMENOPAUSAL WOMEN

Intervention Intervention
BMD
? + ++ ++

Dose disease
genes

Fracture
threshold

Fracture risk: Time on steroids

Figure 22-1. The degree of bone loss from corticosteroids varies according to dose, underlying disease, and possibly genetic
factors. The case for intervention is strong early (primary prevention) in postmenopausal women but is less clear in
premenopausal women. Because fracture risk is a function of the duration of corticosteroid use, secondary prevention is
appropriate to consider in pre- and postmenopausal women on long-term corticosteroid treatment with low BMD. (From
Sambrook PN: Corticosteroid osteoporosis: practical implications of recent trials. J Bone Miner Res 2000;15:1645-9.)

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Osteoblast/
stromal cells Osteoclast
precursor
?
RANKL

OSCAR/FcRγ
RANK TREM2/DAP12
M-CSF Syk
Integrins
TRAF6
c-fms PLCγ
c-FOS

Ca2+ signal
Differentiation
NFATc1 Resorption
? Migration
Fusion

Figure 25-1. Osteoclastogenesis. Osteoclasts are derived form bone marrow precursor cells in the myeloid lineage.
Mononuclear precursor cells fuse to form multinucleated osteoclasts during differentiation. Macrophage colony-stimulating
factor (M-CSF) and RANKL are essential stimuli for osteoclastogenesis at a number of steps. Mature osteoclasts are
characterized by a multinucleated phenotype, with expression of tartrate resistant acid phosphatase, cathepsin K, αvβ3
integrin (vitronectin receptor) and calcitonin receptor.2,3

IFN-γ

RANKL

RANK

IFN-β

TRAF6 STAT1
STAT1

c-FOS STAT1
STAT2

NF-kB IRF-9
JNK

NFATc1

Figure 25-2. Regulation of osteoclastogenesis by interferon (IFN)--γ and IFN-β. Activated synovial cells express RANKL. If IFN-γ
is also expressed during inflammation, IFN-γ will inhibit osteoclastogenesis by downregulating TRAF6 expression, which is
required for RANK signaling. RANK signals also induce IFN-β, which also downregulates RANK signaling by inhibiting the
expression of c-Fos. Thus, inflammatory signals are significant regulators of osteoclastogenesis and are important in the
regulation of bone remodeling.10,11,138

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PIR-A

SIRPβ
OSCAR
TREM-2 MDL-1

+ – – + –– + –– + –– + ––
Y Y syk
syk
Y Y

FcRγ ITAM
DAP12 ITAM Cellular activation/Ca++
+ RANKL/MCSF

Osteoclast differentiation

Figure 25-3. ITAM-associated receptors expressed on osteoclasts. Immunoreceptors on osteoclasts can be associated with
either the DAP12 or the FcRγ ITAM-signaling chains. Receptors identified on osteoclasts or preosteoclasts by reverse-
transcriptase polymerase chain reaction and/or surface antibody staining include OSCAR and PIRA, which both contain
extracellular immunoglobulin domains and are associated with the FcRγ chain (purple ITAM domains). DAP12-associated
receptors (shaded ITAM domains) include TREM2 and SIRPβ with extracellular immunoglobulin domains and MDL-1 with an
extracellular C-type lectin domain. The receptors pair in the membrane with either DAP12 or FcRγ via complementary
charged amino acid residues in the transmembrane domains of each protein. Upon stimulation of the extracellular domain of
the receptor, DAP12 or FcRγ are tyrosine phosphorylated on residues in the ITAM motif and the syk tyrosine kinase is
recruited to the phosphotyrosines. Activation of the syk tyrosine kinase leads to initiation of intracellular signaling
cascades.152,154,160,169

MCSF
RANKL RANKL
MCSF

Precursor Preosteoclast

RANKL
Activated osteoclast
TRAP+
Cathepsin K
Calcitonin receptor
H+ATPase
αvβ3

Figure 25-4. Model for role of ITAM-associated immune receptors in osteoclastogenesis. Signals mediated by RANK
cooperate with signals from ITAM-bearing adapter chains to stimulate osteoclast differentiation and activation. Upon
simulation of their associated receptor, ITAM adapters are tyrosine phosphorylated and recruit syk kinase, which leads to
activation of PLC-γ and calcium signaling. ITAM adapter mediated signals are required for activation of the critical
osteoclastogenic transcription factor NFATc1. Immunoreceptors that associate with DAP12 may have ligands expressed on
other osteoclast precursor cells, whereas FcRγ associated immunoreceptors are predicted to interact with ligands on
osteoblast or stromal cells.8,152,153 (Modified from Koga et al.152 and Takayanagi.8)

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Figure 26-1. A. Cellular and molecular interactions in the synovial compartment facilitate osteoclast differentiation and focal
bone erosion at the synovial/bone interface. The main stromal support cell is the activated fibroblast-like synoviocytes, which
express membrane-bound macrophage colony-stimulating factor (M-CSF) (not shown) and RANKL. These processes lead to
an imbalance in bone resorption relative to bone formation, exhibited as “extrinsic” focal bone erosion. B. Cellular and
molecular interactions in the subchondral bone marrow compartment facilitate osteoclast differentiation and subchondral
bone erosion. The main stromal support cell is the stromal-osteoblasts which express membrane-bound M-CSF (not shown)
and RANKL. These processes lead to an imbalance in bone resorption relative to formation, exhibited as subchondral bone
erosion and juxta-articular osteoporosis.

16
EPIDEMIOLOGY

1 The Epidemiology of Osteoporotic

Fractures
Nicholas Harvey, Sarah Westlake, Elaine Dennison, and Cyrus Cooper

an essential step in developing strategies to reduce the

SUMMARY burden of osteoporotic fractures in the population.
Osteoporosis is a skeletal disease characterized by
low bone mass and microarchitectural deterioration
DEFINITION OF OSTEOPOROSIS
of bone tissue with a consequent increase in bone
fragility and susceptibility to fracture. It causes a Osteoporosis is a skeletal disease characterized by low
great burden on public health due to morbidity, bone mass and microarchitectural deterioration of
reduced survival, and economic costs associated bone tissue with a consequent increase in bone fragility
with fragility fractures. Vertebral, hip, and wrist
and susceptibility to fracture.2 The term osteoporosis
fractures are the most common of these, and the
was first introduced in France and Germany during
incidence of the first two increase exponentially
with age, being more frequent in women than the last century. It means “porous bone” and initially
men in older age groups. Recent studies of implied a histological diagnosis, but the term was later
radiographically defined vertebral fracture have refined to mean bone that had normal mineralization
indicated that only around 30% of these fractures but was reduced in quantity.
present clinically, and that the true incidence is Historically, the definition of osteoporosis has been
greater than that for hip fracture. There are difficult. A definition based on bone mineral density
differences in fracture propensity between (BMD) may not encompass all the risk factors for frac-
populations of different ethnicity and geographical ture, whereas a fracture-based definition will not
locations. Season also influences fracture incidence, enable identification of at-risk populations. The World
with hip fractures being more frequent in winter Health Organization3 recently resolved this issue by
months. There has been a secular increase in hip defining osteoporosis in terms of BMD and previous
fracture incidence over the last 50 years, which may fracture, as shown in Table 1-1. Thus, the World
be plateauing in Western populations. However,
Health Organization definition does not take into
incidence is set to rise worldwide, mainly as a result
account microarchitectural changes that may weaken
of increases in developing countries, as Western
bone independently of any effect on BMD.
lifestyles are adopted. Recent work has shown that
prevalent fracture is a strong predictor of incident If this definition is applied to a female population
fracture, and that this increased risk occurs rapidly. sample in the United Kingdom, the prevalence of
Understanding the epidemiology of osteoporosis is osteoporosis at the femoral neck rises from 5.1% at 50
an essential step in developing strategies to reduce
the burden of osteoporotic fracture in the
TABLE 1-1 CLASSIFICATION OF OSTEOPOROSIS
population.
Normal BMC or BMD value greater than 0.1
SD below young normal adult mean
Osteoporosis is a major public health problem. The main Osteopenia BMC or BMD 1-2.5 SD below young
contributors to this burden are associated fragility frac- normal adult mean
tures. The increased rates of morbidity and mortality
Osteoporosis BMC or BMD >2.5 SD below the young
consequent to these fractures have a massive impact on normal adult mean
both the health of the population and the economy.
Established Osteoporosis with one or more fragility
There were an estimated 1.66 million hip fractures
osteoporosis fractures
worldwide in 1990,1 1,197,000 in women and 463,000 in
men. The estimated annual cost in Europe is 13 billion BMC = bone mineral density, BMD = bone mineral content, SD =
euros, mainly accounted for by hospitalization after frac- standard deviation.
Data derived from World Health Organization Study Group, 1994.3 1
ture. Understanding the epidemiology of osteoporosis is
THE EPIDEMIOLOGY OF OSTEOPOROTIC FRACTURES

to 54 years to over 60% at age 85 and above. The cor- practitioner records of 6% of the UK population, have
responding estimates for men are 0.4% and 29.1%. given the lifetime risks of any fracture at age 50 years as
53.2% in women and 20.7% in men.6 The following sec-
tions will detail the site-specific epidemiology.
FRACTURE EPIDEMIOLOGY
All Fractures Hip Fracture
Data from the United Kingdom suggest that there is an Hip fractures are the most devastating consequence of
overall fracture incidence of 21.1 in 1000 per year osteoporosis, invariably requiring hospitalization.
(23.5/1000 men and 18.8/1000 women),4 and that there Typically, they result from a fall from standing height
is a bimodal distribution, with peaks in youth and in the or lower, but they can occur spontaneously.10 The
very elderly.5 Any bone will fracture if sufficient force is diagnosis is usually suggested by characteristic clinical
applied. Fractures of long bones predominate in young features and confirmed by a plain radiograph.
people, usually as a result of substantial trauma, and
males are involved more frequently than females. Thus,
it is the magnitude of the trauma, rather than deficient Impact
bone strength, that leads to the fracture in this group. In Hip fractures have major consequences; 5% to 20% of
the elderly, low bone mass is the critical factor, with most people affected will die within 1 year after a hip frac-
fractures occurring as a result of minimal force. The rate ture, and more than 50% of survivors will be incapaci-
of fracture in women increases steeply after the age of 35 tated, many needing nursing home care.11 Table 1-2
years and becomes twice that in men (Figure 1-1).6,7 shows the observed and expected survival rates for men
Only around one-third of vertebral fractures reach and women aged 65 years and older in the GPRD study.
clinical attention,8 and until the advent of studies based
on radiographic assessment of vertebral deformity, it Mortality
was thought that hip and distal forearm fractures were The majority of excess deaths occur within 6 months of
the main contributors to this peak. Figure 1-1 demon- the fracture, and the risk of death diminishes with
strates that the picture is rather different, with the inci- time, so that after 2 years survival probability is com-
dence of radiographically defined vertebral deformity parable with that of similarly aged men and women in
being higher than for hip and wrist fractures at all ages. the general population. The mortality risk differs,
A recent study from Denmark showed that 60-year-old however, according to the age and gender of the person
women, expected to live until the age of 81 years, had an experiencing the hip fracture. In a population-based
estimated residual lifetime risk of radial, humeral, or hip study, a relative survival rate of 92% was found for
fracture of 17%, 8%, and 14%, respectively. The lifetime white hip fracture victims younger than 75 years of age,
risk to those women surviving to the age of 88 years was as compared with 83% in those 75 years of age and
increased to 32%.9 Data from the General Practice older at the time of the fracture.12 Despite their greater
Research Database (GPRD), which includes the general age at the time of fracture, survival was better among

Figure 1-1. Radiographic vertebral,

INCIDENCE OF OSTEOPOROTIC FRACTURES hip, and wrist fracture incidence by
Men Women age and gender. (Data derived from
van Staa TP et al.6 and EPOS Study
400 400 Group.7)
= Hip fracture
= Radiographic vertebral
fracture
Incidence per 10,000/year

300 = Wrist fracture 300

200 200

100 100

0 0
55 4
60 9
65 4
70 9
75 4
80 9
4
+

55 4
60 9
65 4
70 9
75 4
80 9
4
+
–5
–5
–6
–6
–7
–7
–8

–5
–5
–6
–6
–7
–7
–8
85

85
50

50

2 Age group Age group

 Fracture Epidemiology
TABLE 1-2 OBSERVED AND EXPECTED SURVIVAL AFTER FRACTURE AMONG MEN AND WOMEN AGED ≥ 65 YEARS

Radius/Ulna, % Femur/Hip, % Vertebra, %

Observed Expected Observed Expected Observed Expected
Women

At 3 months 98.2 98.6 85.6 97.7 94.3 98.4

At 12 months 94.0 94.4 74.9 91.1 86.5 93.6
At 5 years 75.5 73.8 41.7 60.9 56.5 69.6
Men
At 3 months 97.3 98.0 77.7 97.3 87.8 97.9
At 12 months 89.6 92.4 63.3 90.0 74.3 91.8
At 5 years 62.8 66.4 32.2 58.2 42.1 64.4

Data derived from van Staa TP et al.6

women. In the GPRD study (see Table 1-2), observed woman is accrued as she reaches 80 years old. Data
survival in women 65 years of age and older was 74.9% from the GPRD (Table 1-3) show that the lifetime
at 12 months versus 91.1% expected. For men, these risk of hip fracture for women aged 50 years is 11.4%,
figures were 63.3% and 90.0%, respectively.6 This gen- but the risk over the next 10 years is 0.3% at age 50
der difference has been confirmed in other hospital- and 8.7% at age 80 years.6 This has implications for
based studies and appears to be due to the greater targeting of treatment. Among postmenopausal
frequency of other chronic diseases in men who sus- women in the United States, the likelihood of experi-
tain hip fractures. The majority of deaths after hip frac- encing at least one fall annually rises from about one
ture are due to preexisting comorbidity, such as in five women 60 to 64 years old, to one in three
ischemic heart disease, with the minority a direct result women 80 to 84 years old.10 Comparable data were
of complications or management of the fracture itself. found in the United Kingdom, with one in three
women 80 to 84 years old having fallen in the previ-
Morbidity ous year; this statistic rose to nearly one in two (50%)
In the United States, 7% of survivors of all types of frac- among women aged 85 years and older.15 However,
ture have some degree of permanent disability, and 8% only about 1% of all falls lead to a hip fracture. This
require long-term nursing home care. Overall, a 50- is because the amount of trauma delivered to the
year-old white American woman has a 13% chance of proximal femur depends on various protective
experiencing functional decline after any fracture.13 As responses and the direction of the fall: falling side-
with mortality, hip fractures contribute most to osteo- ways onto the hip is more likely to result in fracture
porosis-associated disability. Patients are prone to than falling forward onto it.16
developing acute complications such as pressure sores, Femoral neck strength is weaker in women than in
bronchopneumonia, and urinary tract infections. men and declines with age in both sexes. Many factors
Perhaps the most important long-term outcome is contribute to bone strength, for example BMD and
impairment of the ability to walk. Fifty percent of peo- microarchitecture, but all are closely correlated with
ple who were ambulatory before the fracture are unable absolute bone mass. Over a lifetime, the BMD of the
to walk independently afterward. Age is an important femoral neck declines an estimated 58% in women and
determinant of outcome, with 14% of 50- to 55-year- 39% in men, whereas bone density of the intertro-
old hip fracture victims being discharged to nursing chanteric region of the proximal femur falls by about
homes, versus 55% of those more than 90 years old.13 53% and 35%, respectively. Each one standard devia-
tion decline in bone mineral density is associated with a
Determinants 1.8- to 2.6-fold increase in the age-adjusted risk of hip
Age fracture, depending on the exact site that is measured.17
There is an exponential increase in hip fracture with
aging (see Figure 1-1). This is due to an age-related Gender
increase in the risk of falling and reduction in bone The incidence of osteoporotic hip fractures is lower in
strength. The majority of fractures occur after a fall men than in women; in 1990, only about 30% of 1.66
from standing height or lower; 90% occur in people million hip fractures worldwide occurred in men.18
older than 50 years and 80% are in women.14 Much In the United Kingdom, the lifetime risk of hip frac- 3
of the lifetime risk of fracture for a 50-year-old ture in men is 3.1% at age 50 (compared with 11.4%
THE EPIDEMIOLOGY OF OSTEOPOROTIC FRACTURES

TABLE 1-3 ESTIMATED RISKS OF FRACTURES AT VARIOUS AGES

Current Age (years) Any Fractures (%) Radius/Ulna (%) Femur/Hip (%) Vertebra (%)
Lifetime risk
50 53.2 16.6 11.4 3.1
60 45.5 14.0 11.6 2.9
Women
70 36.9 10.4 12.1 2.6
80 28.6 6.9 12.3 1.9
50 20.7 2.9 3.1 1.2
60 14.7 2.0 3.1 1.1
Men
70 11.4 1.4 3.3 1.0
80 9.6 1.1 3.7 0.8

10-year risk
50 9.8 3.2 0.3 0.3
60 13.3 4.9 1.1 0.6
Women
70 17.0 5.6 3.4 1.3
80 21.7 5.5 8.7 1.6
50 7.1 1.1 0.2 0.2
Men
60 5.7 0.9 0.4 0.3
70 6.2 0.9 1.4 0.5
80 8.0 0.9 2.9 0.7

Data derived from van Staa TP et al.6

in women), and the 10-year risk is 0.2% at age 50, ris- Geography
ing to 2.9% at 80 years of age.6 Men are relatively pro- There is variation in the incidence of hip fracture within
tected for several reasons: they have a higher peak populations of a given race and gender.25-27 Thus, age-
bone density, they lose less bone during aging, they do adjusted hip fracture incidence rates are higher among
not normally become hypogonadal, they sustain fewer white residents of Scandinavia than comparable sub-
falls, and they have a shorter lifespan. However, this jects in the United States or Oceania. In 1986, the
relationship is not true for all populations: in black Mediterranean Osteoporosis Study (MEDOS) was set
and Asian groups, the incidence in men is slightly up to investigate the incidence of hip fracture in the
higher.19 Mediterranean region. It was discovered that the inci-
dence of hip fracture varied markedly from country to
Ethnicity country, and even within countries. Within Europe, the
Hip fractures are much more frequent among whites range of variation was approximately 11-fold.25 These
than among non-whites. This has been explained by differences were not explained by variation in activity
the higher bone mass observed in blacks compared levels, smoking, obesity, alcohol consumption, or
with whites (Figure 1-2).20 migration status.26 In the United Kingdom, the geo-
There is also some evidence that the rate of bone loss graphical differences were not associated with differ-
is lower in blacks. However, the Bantu people of South ences in water fluoridation or with dietary calcium
Africa have a lower bone mass and a lower fracture rate intake, as assessed by a national food survey.28 A more
than whites.21 Likewise, the incidence of hip fractures recent comparison of studies from several areas of
among women of Japanese ancestry is about one half United Kingdom gives an annual incidence of all frac-
that of their white counterparts, even though their tures between 159 and 288 per 10,000 population for
bone mass is somewhat lower.22 These discrepancies men older than 85 years, and between 281 and 810 per
may be related to the reported lower risk of falling of 10,000 population for women older than 85 years.6
black women compared with white women.23 Asian Studies in the United States confirm this complex
women have shorter femoral necks than white women, pattern. In more than 2000 counties nationwide, the
4 and this shape seems inherently less likely to fracture, age-adjusted incidence of hip fracture in white women
despite a lower bone mineral density.24 older than 65 years of age was negatively associated with
Figure 1-2. Hip fracture incidence

Fracture Epidemiology
GEOGRAPHICAL VARIATION IN HIP FRACTURE INCIDENCE
around the world. (Data derived from
Kanis JA et al.20) Men Women
1400

Incidence (per 105 person-years)

1200

1000

800

600

400

200

0
Europe N. America/ Latin Asia Europe N. America/ Latin Asia
Oceania America Oceania America

latitude (higher in the south), water hardness, and hours have been observed even after adjusting for the growth in
of January sunlight, and positively associated with the elderly population. Although the age-adjusted rate of
poverty levels, proportion of the land in farms, and pro- hip fracture appears to have leveled off in the northern
portion of the population with fluoridated water.29 regions of the United States, in parts of Sweden, and the
United Kingdom, the rates in Hong Kong rose substan-
Season tially between 1966 and 1985. Thus, the above figures
Hip fractures are seasonal, occurring more frequently, potentially represent a significant underestimate of the
in both sexes, during the winter in temperate countries. number of hip fractures in the next half-century.
However, the majority of hip fractures follow falls There are three broad explanations for these trends:
indoors and are not related to slipping on icy surfaces. Firstly, they might represent some increasingly
Explanations for this include abnormal neuromuscular prevalent current risk factor for osteoporosis or falling;
function at lower temperatures and vitamin D defi- physical activity is the most likely candidate. There is
ciency as a result of the winter-time reduction in sun- ample evidence linking inactivity to the risk of hip
light exposure. fracture, whether this effect is mediated through bone
density, the risk of falls, or both. Furthermore, some of
Time trends the steepest secular trends have been observed in Asian
Life expectancy is increasing around the globe and the countries, such as Hong Kong, which have witnessed
number of elderly individuals is rising in every geo- dramatic reductions in the customary activity levels of
graphical region. The world population is expected to their populations in recent decades.
rise from the current 323 million individuals aged 65 Secondly, the elderly population is becoming
years or older, to 1555 million by the year 2050. These increasingly frail. As many of the disorders leading
demographic changes alone can be expected to increase to frailty are independently associated with osteoporo-
the number of hip fractures occurring among people 35 sis and the risk of falling, this tendency might have
years of age and older worldwide: the incidence is esti- contributed to the secular increases in Western nations
mated to rise from 1.66 million in 1990 to 6.26 million in during earlier decades of this century.
2050. Assuming a constant age-specific rate of fracture, Finally, the trends could arise from a cohort phe-
as the number of people older than 65 increases from 32 nomenon—some adverse influence on bone mass or
million in 1990 to 69 million in 2050, the number of hip the risk of falling that acted at an earlier time and is
fractures in the United States will increase threefold.1 In now manifesting as a rising incidence of fractures in
the United Kingdom, the number of hip fractures may successive generations of the elderly.
increase from 46,000 in 1985 to 117,000 in 2016.30
An increasingly elderly population in Latin America Vertebral Fracture
and Asia could lead to a shift in the geographical dis- Definition
tribution of hip fractures, with only one quarter occur- Vertebral fractures have been synonymous with the
ring in Europe and North America (Figure 1-3).1 diagnosis of osteoporosis since its earliest description
Such projections are almost certainly optimistic con- as a metabolic bone disorder.31 However, their epi- 5
sidering that increases in the incidence of hip fractures demiology remains less well characterized than that of
 Figure 1-3. Estimated numbers of
THE EPIDEMIOLOGY OF OSTEOPOROTIC FRACTURES

HIP FRACTURE PROJECTIONS

hip fractures among men and
3,500 women in different regions of the
Men Women
1990 world in 1990 and 2050.
3,000
2025

2,500 2050
Hip fractures, 000s

2,000

1,500 Men Women

1,000

500

0
North America, Middle East, Asia,
Europe, Oceania, Latin America,
and Russia and Africa
Region

hip or wrist fractures, because there is no universally Incidence

accepted definition of a vertebral fracture from thora- The application of recently developed morphometric
columbar radiographs, and because a substantial pro- techniques to various population samples in the
portion of vertebral deformities are asymptomatic. United States has permitted the estimation of the inci-
There is significant variation in vertebral body dence of new vertebral fractures in the general popula-
shape, both within the spine and between individuals. tion (Figure 1-4).
This results in considerable difficulty in deciding Using the data shown, the age-adjusted incidence
whether a vertebral body is deformed. Early epidemio- among white US women aged 50 years and older was
logical studies of vertebral fractures used subjective found to be 18 per 1000 person-years.34 This is more
radiological assessments of wedge, crush, and bicon- than twice the corresponding incidence of hip fracture
cave deformities, but these were poorly reproducible. (6.2 per 1000 person-years). The corresponding figure
These methods gave way to morphometric measure- for vertebral fracture from the European Vertebral
ments of vertebral height, with fractures defined Osteoporosis Study (EVOS, a large pan-European lon-
according to fixed cut-off values.32 gitudinal study) was 10.7 per 1000 person-years.7
Each vertebral body in the spinal column has unique In the GPRD study, the overall incidence standardized
dimensions, however, and recent analyses have to the UK population was 3.2 per 1000 person-years
focused on determining the distribution of vertebral for men and 5.6 per 1000 person-years for women.
dimensions at each spinal level and calculating cut-off This population included all ages from 20 years, hence
values from these.32,33 The most widely adopted the lower overall incidence. It is important to note the
thresholds for defining and grading deformities are as disparity between the incidence of vertebral fractures
follows: moderate (or grade 1) fractures are deformi- identified on radiographs and those reported clinically.
ties that fall between three and four standard devia- In Rochester, Minnesota, the incidence of clinically
tions from the mean value specific to each vertebra; diagnosed vertebral deformities was 30% of that
severe (or grade 2) fractures are those that fall four expected from a study using radiographic diagnosis.
standard deviations or more from this mean. When This implies that as few as one in three vertebral frac-
morphometric studies are performed without refer- tures comes to medical attention.8
ence to clinical presentation, the abnormalities found
are usually referred to as deformities rather than frac- Prevalence
tures. Three broad categories of vertebral fracture have The prevalence of vertebral deformity was investi-
been described: compression (or crush) fractures, in gated in an age-stratified random sample of the popu-
which there is loss of both anterior and posterior ver- lation of Rochester, Minnesota, USA. The prevalence
tebral height; wedge (or partial) fractures, in which was estimated at 25.3 per 100 Rochester women aged
anterior height tends to be lost; and biconcave (bal- 50 years and older (95% confidence interval, 22.3-
6 loon) fractures, in which loss of central bony tissue 28.2).35 More recent data from the EVOS group
leads to concavity of both vertebral end plates. suggested the age-standardized prevalence across
Figure 1-4. The incidence of vertebral

Fracture Epidemiology
4
deformities in a population sample of Overall
women from the United States. (Data Clinically diagnosed
derived from Cooper C et al.8)

Fracture incidence/100 person-years

3

0
50–54 55–59 60–64 65–69 70–74 75–79 80–84 85+
Age group (years)

Europe was 12.2% for men and 12.0% for women ture patients. In the United Kingdom (GPRD study;
aged 50 to 79 years.36 The higher Rochester figure rep- see Table 1-2), the observed survival rate in women
resents the inclusion of women older than 80 years, up 12 months after vertebral fracture was 86.5%, versus
to older than 90 years. Because people in this age 93.6% expected. At 5 years, the survival rate was 56.5%
range have a greatly increased prevalence of vertebral observed and 69.9% expected.6 Furthermore, there does
fracture when compared with people in the the 50- to not appear to be any particular cause of death that
79-year-old age range, the overall figure is signifi- explains this finding. This accords with the observations
cantly higher. of recent US and Swedish studies that low bone density
per se is associated with premature death.39,40 These data
Impact suggest that the association might be due to a number of
Spine fractures cause significant pain, deformity, and factors, such as smoking, alcohol consumption, and
long-term disability. Data from the Study of Osteopo- immobility: these predispose independently to both
rotic Fractures,37 a population-based US study of 9606 bone loss and increased mortality risk.
women 65 years of age and older, showed that women
who had grade 2 deformities were 2.6 times more likely Morbidity
to suffer disability and 1.9 times more likely to report The health impact of vertebral fractures has proved con-
moderate or severe back pain than those with no defor- siderably difficult to quantify. Despite only a minority of
mity. Women with grade 1 deformities did not have vertebral fractures coming to clinical attention, vertebral
significantly elevated risks of these clinical sequelae. fractures account for 52,000 hospital admissions in the
Cross-sectional data from out-patients also support United States and 2188 in England and Wales each year
this notion, with severe vertebral deformity being much among patients aged 45 years and older. The major clin-
more closely associated with adverse outcomes than ical consequences of vertebral fracture are back pain,
moderate deformity.38 kyphosis, and height loss. The pain associated with a
new compression fracture is typically severe and tends
Mortality to decrease in severity over several weeks or months.
Examination of the survival of patients after a clinically This pain is associated with exquisite localized tender-
diagnosed vertebral fracture rather surprisingly reveals ness and paravertebral muscle spasm, which markedly
a similar excess mortality rate at 5 years to that found limits spinal movements. Figure 1-6 shows quality-of-
with hip fractures (Figure 1-5).34 life score against age and number of vertebral frac-
This excess is observed in patients with vertebral frac- tures,41 clearly illustrating the impact of age and number
tures caused by moderate or minimal trauma, but not in of fractures, with higher quality-of-life scores indicating
those whose fractures follow severe trauma. The impair- lower health-related quality of life.
ment of survival after vertebral fracture also markedly A proportion of patients may develop chronic pain
worsens as time from diagnosis of the fracture increases. experienced while standing and during physical stress, 7
This is in contrast to the pattern of survival for hip frac- particularly bending. For example, in the control
 Figure 1-5. Five-year survival following a
THE EPIDEMIOLOGY OF OSTEOPOROTIC FRACTURES

100
clinically diagnosed hip, vertebral or distal
80 forearm fracture in Rochester, MN, USA,
60 1985-1989.
Vertebral
40 Expected
20 Observed

100
80
Survival %

60
Hip
40
20
0

100
80
60
Distal forearm
40
20
0
0 1 2 3 4 5
Years after fracture

AGE, NUMBER OF VERTEBRAL Figure 1-6. Health-related quality of life

DEFORMITIES, AND HRQOL related to age and number of vertebral
deformities.

45
Mean QUALEFFO
total score

35 Age >71

Age 65–71
25
Age <65
15
*Age p = 0.020
e

es
e
ur

ur

ur

ur

*Fracture p < 0.001

ct

ct

ct

ct
fra

fra

fra

fra
o

3
N

group of one treatment study, patients were noted to been found to be worse for patients with more severe
have persistent pain for 6 months after fracture.42 This or multiple deformities.43
chronic pain is believed to arise from spinal extensor
muscle weakness and the altered spinal biomechanics Determinants
that result from vertebral deformation. A number of Age
indices of physical function, self-esteem, body image, Most studies agree that the prevalence of vertebral frac-
and mood also appear to be adversely affected in tures rises with age among women. In an age-stratified
patients with vertebral fractures. Whenever self-report random sample of 762 Rochester women who under-
8 scales of functional status or quality of life have been went thoracolumbar radiography, the prevalence
applied to patients with vertebral fractures, scores have of one or more deformities increased from 7.6% at
 Ethnicity

Fracture Epidemiology
50 to 54 years to 64.3% in those 90 years of age and
older. In Europe, the prevalence for men and women, There are few studies assessing the influence of ethnicity
respectively, was 9.9% and 5.0% at 50 to 54 years of on vertebral fracture prevalence, although one study
age, rising to 18.1% and 24.7% at 75 to 79 years of age found vertebral deformities in around 5% of selected
(Figure 1-7).36 white women aged 45 years and older but in none of the
137 black women studied.44 This finding is in accord
Gender with the often-replicated observation that hip fracture
Although it is generally believed that vertebral fractures incidence rates are markedly higher among whites.
are much more common in women than in men, his- However, recent data from Japan suggest that prevalence
torically there has been little epidemiological evidence rates for vertebral deformity in Asian women may be
to support this notion. However, more recent evidence similar to those observed in white populations.45
from EVOS has shown a twofold greater incidence of
vertebral fractures in women than men (relative risk Previous fracture
2.3 at age 50-54 years and 2.9 at age 70-74 years).7 In Previous fracture is increasingly recognized as an
this population, the incidence of vertebral fracture in important determinant of future fracture risk, inde-
men was 1.7 per 1000 person-years at 50 to 54 years of pendent of BMD. A previous hip fracture increases the
age and rose to 14.6 per 1000 person years at 75 to 79 odds of an incident hip fracture by six- to eightfold,46
years of age. In the GPRD data, overall incidence in and a forearm fracture increases the risk of subsequent
men was 3.2 per 10,000 person-years versus 5.6 per hip fracture by 1.4 and 2.7 times in women and men,
10,000 person-years for women.6 Overall, however, the respectively.47 The corresponding figures for subse-
picture for prevalence differs: men aged 50 to 64 years quent vertebral fracture are 5.2 and 10.7. Prevalent
had a higher prevalence of deformity compared with vertebral deformity predicts incident hip fracture with
similarly aged women, with the reverse being the case a rate ratio of 2.8 to 4.5, and this increases with the
for those aged 65 years.36 Whereas 90% of vertebral number of vertebral deformities.48 Previous hip frac-
fractures in women occurred as a result of moderate or ture strongly predicts multiple (more than two) verte-
minimal trauma in this study, an appreciable propor- bral deformities in men (odds ratio 10.2), and
tion of fractures in men (37%) occurred as a result of incident vertebral fracture is predicted by the mor-
severe trauma, for example, road traffic accidents. phometry and number of the baseline deformities
The most frequent vertebral levels involved are L1, (Table 1-4).49 The incidence of new vertebral fracture
T12, and T8. These correspond with the most biome- within a year of an incident vertebral fracture is
chanically compromised regions of the thoracolumbar 19.2%,50 which reinforces the importance of prompt
spine: the midthoracic region, where dorsal kyphosis is therapeutic action on discovering vertebral deformi-
most pronounced, and the thoracolumbar junction, ties. Figure 1-8 summarizes the cumulative incidence
where the relatively rigid thoracic spine meets the of a subsequent vertebral fracture over time after a
freely moving lumbar segment. baseline event.51,52

Figure 1-7. Prevalence of vertebral PREVALENCE OF VERTEBRAL DEFORMITY (EVOS)

deformity, European Vertebral Osteoporosis
Study (EVOS). 25
Men
Women
20
Prevalence (%)

15

10

0
50 55 60 65 70 75
Age (years) 9
 THE EPIDEMIOLOGY OF OSTEOPOROTIC FRACTURES

TABLE 1-4 VERTEBRAL DEFORMITY AND RISK

women, aged 60 years and older, presenting with thoracic
OF VERTEBRAL FRACTURE and lumbar vertebral fractures between 1950 and 1952
and between 1982 and 1983, in Malmö, Sweden, were
Relative Risk of 95% Cl
studied.54 Among women, the incidence rates during the
Subsequent Fracture
1982 to 1983 period were higher than those during the
Number of Deformities 3.2 2.1-4.8 1950 to 1952 period at all ages over 60 years. Among
1 9.8 23.3
men, the increase was only apparent above the age of 80
2 6.1-15.8 15.3-35.4
≥3
years. The prevalence of radiographic vertebral deformi-
Position of height loss ties in two samples of 70-year-old Danish women studied
Anterior/middle 5.9 4.1-8.6 in 1979 and 1989 were found to be virtually identical.55
Posterior/middle 1.6 0.8-3.2 The secular tendency reported from Rochester, with
a rise in incidence between 1950 and 1964, followed by a
Data derived from Lunt M et al.51
plateau, is consistent with both these reports.

Time trends Geographical

The impact of osteoporotic fractures is set to rise in the The EVOS study found a threefold difference in the
future, commensurate with the increasing number of prevalence of vertebral deformities between countries,
elderly people in the population. Little is known about with the highest rates in Scandinavia. The prevalence
secular increases in the age-adjusted incidence of verte- range between centers was 7.5% to 19.8% for men and
bral fractures. In Rochester, Minnesota, there was no sig- 6.2% to 20.7% for women. The differences were not as
nificant increase in the incidence of clinically diagnosed great as those seen for hip fracture in Europe, and
vertebral fractures between 1950 and 1989.53 However, some of the differences could be explained by levels of
when categorized into subgroups, a significant increase physical activity and body mass index.36 More recent
in the incidence of fractures after moderate or minimal data from EVOS showed a correspondingly higher
trauma in postmenopausal women is revealed. This incidence of vertebral fracture in Scandinavia (age-
increase occurred between 1950 and 1964, with a plateau standardized incidence 17.7 per 1000 person-years)
in age-adjusted incidence thereafter. Rates for severe than in Western Europe (age-standardized incidence
trauma fractures and for vertebral fractures from any 10.2 per 1000 person-years7).
cause among younger men and women remained stable.
This rise in the incidence of moderate trauma fractures
in women paralleled that for hip fractures in Rochester. Distal Forearm Fracture
An increase in the prevalence of osteoporosis over this Definition
period is consistent with these trends. The most common distal forearm fracture is Colles frac-
Two European studies have also investigated secular ture. This fracture lies within 1 inch of the wrist joint
trends in the incidence of vertebral fractures. Men and margin and is associated with dorsal angulation and

RISK OF SUBSEQUENT FRACTURE Figure 1-8. Cumulative incidence of a

AFTER INITIAL VERTEBRAL FRACTURE subsequent vertebral fracture over time
after a baseline event.
100
Men
Women
80
Cumulative incidence (%)

60

40

20

0
0 1 2 3 4 5 6 7 8 9 10
10 Years following vertebral fracture
 Fractures in Children
displacement of the distal fragment of the radius and outdoors during episodes of icy weather. This seasonal
with a fracture of the ulnar styloid. Distal forearm frac- variation has been found to exist in northern Europe
tures nearly always follow a fall on an outstretched arm. but is not apparent in southern Europe.

Impact
Despite the fact that only around one-fifth of all
COST OF OSTEOPOROTIC FRACTURES
patients with distal forearm fractures are hospitalized, The total cost of osteoporosis is difficult to assess because
they account for some 50,000 hospital admissions and it includes the costs of in-patient and out-patient medical
more than 400,000 physician visits in the United States care, loss of working days, chronic nursing home care,
each year, and 10,000 hospital admissions in the and medication. The direct costs of osteoporosis
United Kingdom. Admission rates appear to vary stem mainly from the management of patients with hip
markedly with age, such that only 16% of those occur- fractures.
ring in women 45 to 54 years old require in-patient care In the United Kingdom, hip fracture patients occupy
as compared with 76% of those occurring in women 85 one-fifth of all orthopedic beds. In 1994, the direct cost
years old and older. There is a 30% increase of algodys- in England and Wales was £750 million,61 and a more
trophy after these fractures, as well as a risk of neu- recent estimate puts the figure at £942 million.62 In
ropathies and post-traumatic arthritis. Wrist fractures France, an estimated 56,000 hip fractures annually cost
do not appear to increase mortality risk. Although wrist about 3.5 billion francs. The cost of fractures in the
fractures may affect some activities such as writing or United States may be as much as $20 billion per year,
meal preparation, overall, few patients are completely with hip fractures accounting for more than one-third
disabled, despite more than one half reporting only fair of the total. Table 1-5 summarizes the impact of osteo-
to poor function at 6 months.13,56-58 porotic fractures in Europe in the 1990s, reaching a
total cost of around €13 billion.63
Determinants The greatest expense is incurred by the in-patient,
Age out-patient, and nursing home care of patients with hip
Distal forearm fractures display a different pattern of fractures. About 10% of women who sustain a hip frac-
incidence from that of the other osteoporotic fractures ture become functionally dependent in the activities of
(see Figure 1-1). In white women, incidence rates daily living (taking prefracture functional status into
increase linearly between 40 and 65 years of age and account), and 19% require long-term nursing home
then stabilize. In men, the incidence remains constant care because of the fracture.13 Nursing home care is
between 20 and 80 years of age. The reason for the extremely expensive, accounting for more than one-
plateau in female incidence remains obscure but may half of the total annual cost of hip fractures. At least
relate to a change in the pattern of falling with advanc- 60,000 nursing home admissions are attributed to hip
ing age. The slower gait and impaired neuromuscular fractures each year in the United States. As many as 8%
coordination of elderly women make them more likely of all nursing home residents have had a hip fracture.
to fall on their hip rather than on their wrist. However,
more recent studies have shown a gentle progressive
increase in incidence after menopause,59 suggesting that FRACTURES IN CHILDREN
there has been a change in the pattern of incidence with There has been much less investigation of the role of
age, the explanation for which is not clear. bone fragility in childhood fractures, probably because
of the perception that the primary determinant of
Gender fracture in this age group is trauma. Most evidence
The age-adjusted female-to-male ratio of 4:1 for distal
forearm fractures is more marked than that of either
hip or vertebral fractures. Fifty percent occur in women TABLE 1-5 IMPACT OF OSTEOPOROSIS-RELATED
older than 65 years. After the age of 35 years, the age- FRACTURES IN UNITED KINGDOM
adjusted incidence of wrist fracture is 36.8 per 10,000
person-years in women and 9.0 per 10,000 person-years Hip Spine Wrist
in men. The incidence in men is low and does not rise Lifetime risk (%)
much with aging.60 Women 14 28 13
Men 3 6 2
Season Cases/year (n) 70,000 120,000 50,000
Hospitalization (%) 100 2-10 5
There is a winter peak in the incidence of Colles frac-
Relative survival 0.83 0.82 1.00
ture that is more pronounced than the peak observed
Costs All sites combined ~ £1.7 billion
11
in hip fracture and also is more closely related to falls
 THE EPIDEMIOLOGY OF OSTEOPOROTIC FRACTURES

comes from two large studies, based in the United the discordance between height gain and accrual of vol-
Kingdom and Sweden, which describe the epidemiol- umetric bone density is greatest.64
ogy of fractures in childhood.64-66 In the series from As with fractures in the elderly, there appears to be a
Malmö, Sweden, data were collected over 30 years on geographical variation in childhood fracture incidence.
all childhood fractures by radiograph retrieval. Based There was an almost 50% increased incidence in
on 8500 incident fractures, the overall incidence of Northern Ireland, Scotland, Wales, and the north of
fracture was 212 per 10,000 girls and 257 per 10,000 England when compared with London and the south-
boys, with 27% of girls and 42% of boys sustaining a east of England. This could be due to socioeconomic
fracture between birth and 16 years of age. Fractures of fractures, with a greater risk of accidents in lower social
the distal radius occurred most commonly, followed classes.64
by fractures of the phalanges of the hand.65 A follow- Childhood fractures are a significant problem, and
up study in Malmö between 1993 and 1994 found the evidence is accumulating to suggest that bone fragility,
incidence of fracture had decreased by almost 10% as well as propensity to trauma, play an important role
since the original study.67 in their pathogenesis. Further work in this area may
In the United Kingdom, the GPRD was used to allow children with low bone mass to be identified in
investigate the epidemiology of fracture in childhood childhood and strategies put in place to reduce their
between 1988 and 1998.64 The overall incidence of risk of further fractures in later life.
fracture was 133.1 per 10,000 children. The gender dif-
ferences were similar to those found in the Malmö CONCLUSION
study, with fractures being more common among boys
than girls, with an incidence of 161.6 per 10,000 and Osteoporosis is a disease that has a huge effect on pub-
102.9 per 10,000, respectively. Again, the most com- lic health. The impact of osteoporotic fracture is mas-
mon fracture site in children of both sexes was the sive, not just for individuals, but also for the health
radius/ulna, with a total of 39.3 per 10,000 per year. service, the economy, and the population as a whole.
Historically, most work has focused on the impact of Strategies to reduce the burden of this widespread dis-
trauma in the etiology of childhood fractures, contrast- ease are thus urgently needed.
ing with the role of bone fragility in the elderly.
However, several recent studies have documented lower ACKNOWLEDGMENTS
area and volumetric bone mineral density in children
with distal forearm fractures than age- and sex-matched We are grateful to the Medical Research Council, the
control subjects.68 The age and sex distribution of frac- Wellcome Trust, the Arthritis Research Campaign, the
tures may also suggest an influence of bone fragility. In National Osteoporosis Society, and the Cohen Trust
the GPRD, fracture incidence peaked at 14 years in boys for support of our research program into the develop-
and 11 years in girls. Thus, peak fracture rate was found mental origins of osteoporotic fracture. The manu-
to be highest in both sexes at the start of puberty, when script was prepared by Mrs. G. Strange.

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38. Ross PD, Ettinger B, Davis JW, et al: Evaluation of adverse health Kleerekoper M, ed. Drug therapy for osteoporosis. Oxon, Taylor
outcomes associated with vertebral fractures. Osteoporos Int & Francis, 2005:1-18.
1991;1:134-140. 64. Cooper C, Dennison EM, Leufkens HG, et al: Epidemiology of
39. Browner WS, Seeley DG, Vogt TM, Cummings SR: Non-trauma childhood fractures in Britain: a study using the general practice
mortality in elderly women with low bone mineral density. research database. J Bone Miner Res 2004;19: 1976-1981.
Study of Osteoporotic Fractures Research Group. Lancet 65. Landin LA: Epidemiology of children’s fractures. J Pediatr
1991;338:355-358. Orthop B 1997;6:79-83.
40. Johansson SJ, Gardsell P, Mellstrom,D, et al: Bone mineral 66. Landin LA: Fracture patterns in children: analysis of 8,682
measurment is a predictor of survival. Bone Miner 1992;17:166. fractures with special reference to incidence, etiology and
41. Oleksik A, et al: Health-related quality of life in postmenopausal secular changes in a Swedish urban population 1950-1979.
women with low BMD with or without prevalent vertebral Acta Orthop Scand Suppl 1983;202:1-109.
fractures. J Bone Miner Res 2000;15:1384-1392. 67. Tiderius CJ, Landin L, Duppe H: Decreasing incidence of
42. Ringe JD: Proceedings of the International Symposium on fractures in children: an epidemiological analysis of 1,673
Osteoporosis Vol 2. Christiansen C, Johansen JS, Riggs BJ, eds. fractures in Malmö, Sweden, 1993-1994. Acta Orthop Scand
Copenhagen: Osteopress, 1987:1262-1264. 1999;70:622-626.
43. Kanis JA, McCloskey EV: Epidemiology of vertebral osteoporosis. 68. Jones IE, Taylor RW, Williams SM, et al: Four-year gain in bone
Bone 1992;13(Suppl 2):S1-10. mineral in girls with and without past forearm fractures: a DXA
44. Smith RW Jr, Rizek J: Epidemiologic studies of osteoporosis in study. Dual energy X-ray absorptiometry. J Bone Miner Res 13
women of Puerto Rico and southeastern Michigan with special 2002;17:1065-1072.
 EPIDEMIOLOGY

2 The Genetics of Osteoporosis

Frances M.K. Williams and Tim D. Spector

OSTEOPOROSIS GENES AND THEIR

SUMMARY IDENTIFICATION
Osteoporosis is well known to be highly influenced
Osteoporosis is a skeletal condition characterized by
by genetic factors. Bone mineral density (BMD)—
its main risk factor—has also been shown to be diminished bone mineral density and deterioration in
highly heritable. Other known risk factors for bone microarchitecture. The main clinical endpoint is
osteoporotic fractures, such as reduced bone fracture. Genetic factors have long been recognized to
quality, femoral neck geometry, and bone turnover, play an important role in both osteoporosis and its
are now also known to be heritable. Different associated phenotypes, which include bone mineral
approaches are currently being used to identify the density (BMD), bone mass, broadband ultrasound
many genes responsible, including linkage studies attenuation, and velocity of sound, to name but a few.
in humans and experimental animals as well as Twin and family studies have estimated that 50% to
candidate gene studies and alterations in gene 85% of the variance in bone mass is genetically deter-
expression. Linkage studies have identified multiple mined.1-4 Similar studies have shown evidence of sig-
quantitative trait loci (QTLs) for regulation of BMD nificant genetic effects on other determinants of
and, along with twin studies, have indicated that the fracture risk, including quantitative ultrasonographic
QTL effects are dependent both on the sex of the
properties of bone,5 several aspects of femoral neck
subject and on the site of osteoporosis. For the most
geometry,5 muscle strength,6 bone turnover markers,7,8
part, the genes responsible for BMD regulation in
these QTLs have not been identified. Many studies
body mass index,9 and age at menopause.10
have used the candidate gene approach. The Unfortunately, there are few data describing the her-
vitamin D receptor gene (VDR), the collagen type I itability of osteoporotic fracture, mainly because
alpha I gene (COLIA1), and the estrogen receptor recruiting adequate numbers of subjects with fracture is
gene alpha (ER ) have been widely investigated and difficult and expensive. Several studies have shown that
found to play roles in regulating BMD. Their a family history of fracture is a risk factor for fracture,
effects, however, are modest and probably independent of BMD.11-14 One small twin study from
account together for less than 5% of the heritable Finland found identical twins to have only slightly
contribution to BMD. The low-density lipoprotein higher rates of concordance for fracture than noniden-
receptor-related protein-5 (LRP-5) gene was tical twins,15 suggesting that environmental factors are
identified by linkage and confirmed in association important. This illustrates the important difference
studies and has been shown to be physiologically between associated phenotypes, osteoporosis, and frac-
important in the Wnt signaling pathway. Genes vary ture: associated phenotypes have been found to be
in their influence of particular intermediate
highly heritable but identifying the genes responsible
phenotypes, and we know that not all genes
does not necessarily identify genes for other associated
influencing BMD will be important in fractures.
Susceptibility to osteoporosis is mediated, in all phenotypes or, indeed, those influencing fracture.
likelihood, by multiple genes each having small Another such example is that of genes influencing bone
effect. The number of genes involved in density and wrist fracture. A larger UK twin study than
osteoporosis may be too great for us to previously performed recently reported both wrist
understand precisely how they all work together, BMD and wrist fracture to be independently heritable.
but their identification leads to greater However, only a modest genetic overlap was found
understanding of the physiological pathways between BMD and velocity of sound properties of bone
involved, pathways that could yield novel and genes influencing fracture.16
therapeutic targets. Several approaches are being employed currently in
the search for genes that contribute to osteoporosis in
14 the general population.17 Rare monogenic conditions
affecting bone have already been used to cast light on
 Other Methods of Identifying Genes in Osteoporosis
Osteogenesis imperfecta describes a heterogeneous
TABLE 2-1 MAIN QUANTITATIVE TRAIT LOCI FINDINGS
FOR BONE MINERAL DENSITY (BMD) IN HUMANS group of monogenic disorders characterized by multi-
ple bone fractures. Most forms of osteogenesis imper-
Study Locus BMD Affected fecta are caused by mutations in the type I collagen
Bone
genes COLIA1 and COLIA2. The genes that encode
Devoto et al. (1998)31 1p36 3.51 Hip type I collagen have many different mutations, hence
2p23 2.29 Hip the heterogeneous nature of the disorder from mild to
4q33 2.95 Hip
extremely severe. Osteoporosis-pseudoglioma syn-
Nui et al. (1999)33 2p21 2.15 Wrist
Koller et al. (2000)34; 1q21 3.86 Spine
drome is a rare, autosomal recessive disorder charac-
Econs et al. (2004)68 terized by juvenile-onset osteoporosis and blindness
1q 3.6 Spine due to persistent vascularization of the eye. Initial link-
5q33 2.23 Hip age studies mapped osteoporosis-pseudoglioma
Karasik et al. (2002)42 6p21 2.93 Spine syndrome to chromosome 11q12-13.18 Subsequent
21q22 3.14 Hip work showed the disease to be caused by inactivating
Wilson et al. (2003)38 3p21 2.7 Spine mutations in the low-density lipoprotein-related
1p36 2.4 Hip
receptor-5 (Lrp-5).19 Another phenotype, autosomal
Styrkarsdottir et al. 20p12 3.18 Hip
(2003)39
dominant high-bone-mass, maps to the same region20
20p12 2.89 Spine and was reported independently to be caused by an
Ralston et al. (2005)40 10q21 4.4 Hip in young activating mutation of the same receptor.21
men Osteoporosis has been reported in association with
20q13 3.2 Spine in young homozygous inactivating mutations of the estrogen
women receptor and aromatase genes, emphasizing the impor-
tance of estrogen in the attainment and maintenance
of peak bone mass. Mutations in the latency-activating
genes that may influence population osteoporosis. peptide domain of the transforming growth factor
Looking to the future, the most important approaches beta-1 gene are associated with Camurati-Engelmann
include candidate gene association studies and linkage disease, a condition characterized by increased BMD in
studies. All three methods are discussed here (Table 2-1). the diaphysis of long bones.22 Mutations of the
TCIRG1 gene, which encodes a subunit of the osteo-
GENES OF RARE MONOGENIC DISEASES clast proton pump, have been shown to be responsible
for the autosomal recessive condition osteopetrosis.23
Osteoporosis and fragility fractures are features of sev- The important question is whether the genetic clues
eral rare monogenic diseases and provide an obvious obtained from these rare disorders cast any light on the
place to start the search for genes influencing osteo- problem of osteoporosis in the normal population.
porosis in the general population. Such conditions are There is evidence that some do contribute to regulation
not always informative, however. They include osteo- of “normal” BMD. For example, lipoxygenase LRP-5
genesis imperfecta, the osteoporosis-pseudoglioma gene polymorphisms have been shown recently to be
syndrome, and syndromes associated with inactivating associated with bone mineral content, bone area, and
mutations of the estrogen receptor alpha and aro- stature, particularly in males.24 Several groups have
matase genes (Figure 2-1). reported polymorphisms in the transforming growth
factor beta gene to be associated with BMD and osteo-
porotic fracture,25,26 and polymorphisms of the TCIRG1
genes (subunit of osteoclast proton pump) have been
Genes
found to be associated with BMD in normal subjects.27

Bone density Bone structure

OTHER METHODS OF IDENTIFYING GENES
Bone size Muscle strength IN OSTEOPOROSIS

Coordination Insulation Linkage Studies

Linkage disequilibrium refers to the phenomenon
Early menopause Bone turnover whereby genes lying close together tend to be inherited
together. Evidence suggests that linkage disequilibrium
Fracture is influenced greatly and variably by both the chromo-
somal region and the human population studied. It can 15
Figure 2-1. Genetic factors influencing fracture. extend to 350 Kb or further.28 Using this effect, linkage
Exploring the Variety of Random
Documents with Different Content
The text on this page is estimated to be only 26.56%
accurate

CH. i.] of (tttopia* 119 despyte), but also all hys owne
soldiours. Thus the worke, beyng diuyded into so great a numbre of
workemen, was with exceding maruelous spede dyspatched. In so
muche that the borderers, whiche at the fyrst began to mocke and
to gieste at thys vayne enterpryse, then turned theyr laughter to
marueyle at the successe, and to feare. There be in the Ilande .liiii.1
large and faire cities or shiere townes, agreyng all together in one
tonge, in lyke maners, institucions, and lawes. They be all set and
situate a lyke, and in all poyntes fashioned a lyke, as farfurth as the
place or plotte suffereth. Of thi.es cyties they that be nighest
together be xxiiii. myles a sonder. Again there is none of them
distaunt from the next aboue one dayes iorneye a fote. There cum
yearly to Amaurote out of euery cytie .iii. olde men, wyse and well
experienced, there to entreate and sed suos praeterea milites omnes
adiungeret, in tantam hominnm multitudinem opere distribute,
incredibili celeritate res perfecta ; finitimosque a (qui initio uanitatem
incoepti riserant) admiratione successus ac terrore perculerit. 7°
Insula ciuitates habet | quatuor et quinquaginta,
OppidaVtopiaeinsuiae. [72J spatiosas omnes ac magnificas, lingua,
moribus, in... ... . , . . Similitude concorstitutis, legibus prorsus
nsdem. idem situs omnium, diam facit eadem ubique quatenus per
locum licet rerum facies. Harum quae proximae inter suntb, millia
quatuor Vrbium inter seme_ _ diocre mteruallum. ac uiginti
separant. Nulla rursus est tarn deserta, e qua non ad aliam urbem
pedibus queat unius itinere diei perueniri. Ciues quaque ex urbe
terni senes ac rerum periti tractatum de a que om. A. Legend, ut
finitimos b inter se sunt, A. 1 In England and Wales together
Richemond, in place of it, keeps up the we new reckon fifty-two
shires ; but English number to forty. As underin Harrison's England
(ed. by Furni- sheriff of London, More may have vail, 1877), pp. 96,
97, the number is been often reminded that the City given as fifty-
three. Monmouthshire was a county in itself; and thus, is there
classed as a Welsh county, perhaps, his number of fifty-four was
making thirteen ; and the county of made up.
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1 20 Cfte 0econD TBofee CCH. i. debate of the common

matters of the lande. For thys cytie (because it standeth iust in the
myddes of the Ilande, and is therfore moste mete for the
embassadours of all partes of the realme) is taken for the chiefe and
head cytie. The precinctes and boundes of the shieres be so
commodiously appoynted out, and set furth for the cyties, that
neuer a one a of them all hath of anye syde lesse then xx. myles of
grounde, and of som syde also muche more \ as of that part where
the cyties be of farther distaunce a sonder. None of the cities desire
to enlarge the boundes and lymites of their shieres 2. For they count
them selfes rather the good husbandes, then the owners of their
landes. They haue in the countrey in all partes of the shiere howses
or fermes buylded, wel appointed and furnyshed with all sortes of
instrumentes and tooles belongyng to husbandrie. Thies houses be
inhabited of the cytezens, whiche cum thyther to dwel by course. No
howsholde " that none. rebus insulae communibus quotannis
conueniunt Amaurotum. Nam ea urbs (quod tanquam in umbilico
terrae sita maxime iacet omnium partium legatis opportuna) prima
princepsque Distributio agrorum. \ A • • , . . ., habetur. Agri ita
commode ciuitatibus assignati sunt, ut ab nulla parte minus soli
quam xxa passuum millia una quaeuis habeat, ab aliqua multo etiam
amplius ; uidelicet qua parte longius urbes inter se disiunguntur.
Nulli urbi cuAt nine hodie pestis ° ' rerum prope omnium, pido
promouendorum finium. Quippe quos habent, agricolas magis eorum
se, quam dominos, putant. Prima cura Habent ruri per omnes agros
commode dispoagricolationis. , ... . sitas domos, rusticis instruments
mstructas. Hae habitantur ciuibus per uices eo commigrantibus.
Nulla familia rusa xn., A. 1 But yet, as said before, so as calls
attention to this love of territorial not to exceed a day's journey on
aggrandizement as one of the great foot. plagues of the time. See
above, p. 81, • The marginal note in the Latin for examples.
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CH. i.] of ftltopia, 121 or ferme in the countrey hath fewer

then .xl.1 persones, men and women, besydes two bonden men,
whiche be all vnder the rule and order of the good man and the
good wyfe of the house, beynge bothe very sage and discrete3
persones. And euery .xxx. fermes or famelies haue one heade ruler,
whiche is called a Phylarche2, being as it were a hed baylyffe. Out of
euery one of thies famelies or fermes cummeth euery yeare into the
cytie .xx. per sones whiche haue contynewed .ii. yeres before in the
countrey. In their place so manye freshe be sent thither out of the
citie3, whiche of them that haue bene there a yeare all ready, and
be therfore expert and conninge in husbandry, shalbe instructed and
taught ; and they the next yeare shall teache other. This order is
vsed, for feare that other skarsenes of victualles or some other like
incommoditie shuld chaunce through lacke of knowledge, yf they
should be al together newe and fresh and vnexperte in husbandrie.
This maner and fassion of yearlye chaunginge and renewinge the
occupiers of husbandrie, a discrete and aunciente. tica in uiris
mulieribusque pauciores habet quam quadraginta, praeter duos
asscriptitios seruos, quibus pater materque familias graues ac maturi
praeficiuntur ; et singulis tricenis familiis philarchus unus. E quaque
familia uiginti quotannis in urbem remigrant, hi qui biennium ruri
compleuere. In horum locum totidem recentes ex urbe 73
subrogantur, ut ab his qui annum | ibi fuere, atque ideo rusticarum
peritiores rerum, instituantur ; alios anno sequente docturi : ne, si
pariter omnes ibi noui agricolationisque 4 rudes essent, aliquid in
annona per imperitiam peccaretur. Is innouandorum agricolarum
mos etsi solemnis sit, ne quisquam inuitus asperiorem uitam cogatur
1 In Dibdin's edition (Boston re- •• The benefit of such an
alternaprint, 1878, p. 234) this is for some tion of town and country
life, where reason given as ' fifty persons.' attainable, is obvious. See
W. 2 See the note below, p. 124. The Morris's News from Nowhere,
1890, description of this officer as a sort of p. 19. head bailiff, is
inserted by Robynson 4 The word agricolatio is found in from what
More says a little later on. Columella.
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122 cfre seconD TBofee CCH. T. though it be solempne and

customablie vsed, to thintent that no man shall be constrayned
against his wil to contynewe longe in that harde and sharpe l kynde
of lyfe, yet manye of them haue suche a pleasure and delete in
husbandrye, that they obteyne a longer space of yeares. Thies
husbandmen plowe and till the grounde, and bryde 2 vp cattell, and
make a readye woode, whiche they carrye to the cytie, other by
lande or by water, as they maye moste conuenyently. They brynge
vp a greate multytude of pulleyne, and that by a meruelous policie.
For the hennes doo not syt vpon the egges : but by kepynge them in
a certayne equall heate, they brynge lyfe into them, and hatche
them 3. The chykens, assone as they be come owte of the shell,
followe men and women in steade of the hennes. a prouide and
make. continuare diutius ; multi tamen, quos rusticae rei studium
natura delectat, plures sibi annos impetrant. Agricolae terram
c°lunt> nutriunt animalia, ligna comparant, atque in urbem qua
commodum est terra mariue conuehunt. Pullorum infinitam educant
multitudinem, mirabili artificio. Neque enim incubant oua gallinae ;
sed magnum eorum fouendloua numerum calore quodam aequabili
fouentes animant educantque. Hi simul atque e testa prodiere,
homines uice matrum comitantur et agnoscunt. 1 Lit. 'the rougher
life' — of the Hows in that Cytee, that is fulle of husbandman. smale
Furneys ; and thidre bryngen 2 That is, breed, Wommen of the Toun
here Eyren of 3 The now familiar process of arti- Hennes, of Gees
and of Dokes, for to ficial incubation is alluded to by Bacon ben put
in to tho Furneyses. And as something which rested only on thei that
kepen that House coveren hearsay. ' Eggs, as is reported by hem
with Hete of Hors Dong, with some, have been hatched in the
warmth outen Henne, Goos or Doke or any of an oven.' Nat. Hist.
Cent. ix. § 856. other Fowl; and at the ende of But Pliny had referred
to it long before 3 Wekes or of a Monethe, thei comen as practised
in Egypt. Hist. Nat. x. ayen and taken here chickenes 54. There is a
curious passage relat- and norissche hem and bryngen hem ing to
the same subject in The Voiage forthe.' Even Sir John, however, and
Travaile of Sir John Maundeville, does not cite the additional marvel
ed. 1883, p. 49, where, speaking of with which More concludes his
Cairo, he says : ' There is a comoun description.
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CH. i.] ofQtopia, 123 They bryng vp very fewe horses ; nor
non, but very fearce ones l ; and for none other vse or purpose, but
only to exercyse their youthe in rydynge and feates of armes2. For
oxen be put to all the labour of plowynge and drawyng. Whiche they
graunte to be not so good as horses asa sodeyne brunt, and (as we
saye) at a dead lifte 3 ; but yet they holde opinion, that oxen wyll
abyde and sufifre much more laboure and payne b then horses wyl.
And they thinke that they0 be not in daunger and subiecte vnto so
manye dysseases, and that they bee kepte and maynteyned wyth
muche lesse coste and charge ; and fynally that they be good for
meate when they be past labour. They sowe corne onlye for bread.
For their drynke is other wyne made of grapes, or els of apples or
peares4, a at a. b payne and hardnes. c oxen. Equos alunt perquam
paucos, nee nisi ferocientes 5, neque alium in usum quam
exercendae rebus equestribus iuuentuti. Nam omnem sen colendi
sed uehendi laborem boues Vsas equorum. obeunt ; quos, ut
fatentur equis impetu cedere, sic Vsus boum patientia uincere, nee
tot obnoxios morbis putant ; ad haec minore impendio et operae et
sumptus ali, ac denique laboribus emeritos in cibum tandem usui
esse. Semente in solum panem utuntur. Nam aut uuarum Cibus ac
potus. uinum bibunt, aut pomorum pirorumue, aut denique 1
Burnet's rendering, ' full of mettle,' 3 'Sodeyne brunt ' and ' dead
lifte' is better. (that is, a lift or pull when there is 2 The thought may
have been sug- no way or momentum on the load to gested by a
passage in the Republic, make it easier) represent the single Bk.V.
§467(tr.byDaviesandVaughan): word impetus in the Latin. ' We must
put them [the children] on 4 Burnet, more concisely : ' Wine,
horseback at the earliest possible age ; Cyder, or Perry.' and when
we have taught them to ride, 5 A word found in some MSS. of we
must take them to see the fighting, Quintilian, Instit. x. 3. 10,
instead of mounted, not on spirited animals, or efferentes se, as an
epithet of equos. good chargers, but on horses selected The
Comucopiae gives it. for speed and docility.'
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124 Cbe seconti T5ofee CCH.I. or els it is cleane water; and

many tymes methe made of honey or liqueresse sodde in water l, for
therof they haue great store. And though they knowe certeynlye (for
they knowe it perfetly in dede\ how much victayles the cytie with the
hole countrey or shiere rounde a boute it dothe spende ; yet they
sowe much more corne, and bryed vp muche more cattell, then
serueth for their own vse. And the ouerplus they parte a amonge
their borderers. What soeuer necessary thynges be lackynge in the
countrey, all suche stuffe they fetche out of the citie ; where without
anye exchaunge they easelye obteyne it of the magistrates of the
citie. For euerye moneth manye of them goo into the cytie on the
hollye daye. When theyr haruest daye draweth nere and is at hande,
then the Philarches2, whiche n partynge the overplus. aquam
nonnunquam meram ; saepe etiam qua mel aut glycyrizam
incoxerint, cuius baud exiguam habent copiam. Quum exploratum
habeant (habent | enim certissimum) quantum annonae consumat
74 urbs, et circumiectus urbi conuentus, tamen multo Modus
sementis. _ j j amplius et sementis faciunt et pecudum educant,
quam quod in suos usus sufficiat, reliquum impartituri finitimis.
Quibuscunque rebus opus est, quae res ruri non habentur, earn
supellectilem omnem ab urbe petunt, et sine ulla rerum
commutatione a magistratibus urbanis nullo negocio consequuntur.
Nam illo singulo 3 quoque lThe drink here described as made angel
guest : — by an infusion of honey or liquorice, ' for drink the grape
may have been a kind of mead, as She crushes, inoffensive must,
and Robynson takes it. Harrison, in his tneaths Description of
England, Bk. II. (ed. From many a berry, and from sweet 1877, p.
161). speaks slightingly of kernels pressed a beverage known by this
name, made She tempers dulcet creams.' by the Essex goodwives
'with honi- 2 The change of spelling (see above, combs and water/
but not to be com- p. 121) is only capricious, and not pared with the
true metheglin, with meant to indicate a derivation from which mead
is sometimes identified.
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CH.I.] of Qtopia. 125 be the bed officers and bayliffes of

husbandrye, sende woorde to the magistrates of the citie, what
numbre of haruest men is nedefull to bee sente to them out of the
cytie. The whiche companye of haruest men, beyng there a readye
at the daye appoynted, almoste in one fayre daye dispatcheth all the
haruest woorke. n there omitted. mense plerique ad festum diem
conueniunt. Quum frumentandi dies instat, magistratibus urbanis
agricolarum phylarchi denunciant, quantum ciuium numerum ad se
Mutua opera , . i r quantum ualeat. mitti conuemat ; quae multitude
irumentatorum, quum ad ipsum diem opportune adsit, uno prope
sereno die tota frumentatione defunguntur.
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126 Cf)C SeCOnt) TBOfeC [Q..II. A t\)t tvties and namely of

Amaurote. S for their Cyties, he thata knoweth one of them knoweth
them all : they be all so lyke one to an other, as ferfurth as the
nature of the place pennytteth. I wyll descrybe therfore to yowe one
or other of them, for it skylleth not greatly whych ; but which rather
then Amaurote1? Of them all this is the worthiest and of moste
dignitie. For the resydwe knowledge it for the head cytie, because
there is the councell house. Nor to me any of them al is better
beloued, as wherin I lyued fyue hole yeares together. " who so. DE
VRBIBVS, AC NOMINA TIM DE AMAVROTO. VRBium qui unam norit,
omnes nouerit : ita sunt inter se (quatenus loci natura non obstat)
omnino similes. Depingam igitur unam quampiam (neque enim
admodum refert quam) 2. Sed quam potius quam Amaurotum ? qua
nee ulla Amauroti pn- . . ... mariae Vtopien- dignior est, quippe cui
senatus gratia reliquae defesium urbis runt 3, nee ulla mihi notior, ut
in qua annos quinque descriptio. perpetuo uixerim. 1 The name is
evidently derived London in More's time, as now, was from apavpos,
' dim,' whence apavpoaais, subject to fogs; and possibly there '
obscuration,' &c. Baumstark, in his may have been some thought of
this Thomas Morus, 1879, p. 90, oddly in the author's mind, as his
Amaurotum interprets the word by i mauerlos,' is evidently drawn
with reminiscences ' without walls,' though he adds just of London.
But most likely the name after that ' die Stadt ist mit Thiirmen, was
only meant to convey the same Bollwerken und Mauern befestigt.'
impression of vagueness or non-existA passage in Mr. John Watney's
ence as Utopia itself. Account of the Hospital of St. Thomas 2 An
anglicism. of Aeons, 1892, p. 115, shows that 3 Defence in the
sense of ' defer to/ is
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CH. ii.] of Qtopia* 127 The cytie of Amaurote standeth

vpon the syde of a low hill, in fashion almoste four square. For the
bredeth of it begynneth a litle benethe the toppe of the hyll, and
styll contyneweth by the space of twoo miles vntyll it cum to the
ryuer of Anyder. The lenghte of it whiche lyeth by the ryuers syde is
sumwhat more. The ryuere of Anyder1 rysethe .xxiii. myles aboue
Amaurote owte of a lytle sprynge. But beynge increasede by other
small floodesa and broukes that runne into yt, and amonge othere
.ii. sumwhat bygge ons, before the cytye yt ys halfe a myle brode,
and farther broder. And .lx. h myles beyonde the citye yt falleth into
the Ocean sea. By al that space that lyethe betwene the sea and the
cytye, and a good sorte of c myles also aboue the cytye, the water
ebbethe and flowethe .vi. houres togethere wyth a swyfte tyde.
Whan the sea flowethe in for the lenghte of xxx. myles, yt fyllethe all
the Anyder wyth salte water, a riuers. b fortie. c and certen. Situm
est igitur Amaurotum in leni deiectu montis, figura fere quadrata.
Nam latitude eius paulo infra collis incoepta uerticem, 75 milli bus
passuum duobus ad flumen Anydrum pertinet, secundum ripam
aliquanto longior. Oritur Anydrus milibus octoginta supra
Amaurotum, modico fonte, sed aliorum occursu fluminum, atque in
his duorum ... . . Anydri fluminis etiam mediocnum, auctus, ante
urbem ipsam quingen- descriptio tos in latum passus extenditur. Mox
adhuc amplior, sexaginta milia prolapsus, excipitur oceano. Hoc toto
spacio, quod urbem ac mare interiacet, ac supra urbem quoque idem
fit apud aliquot milia, sex horas perpetuas influens aestus ac Anglos
in flumine refluus alternat celeri flumine. Quum sese pelagus
Thamysi. infert, triginta in longum milia, totum Anydri alueum suis
occupat late Latin. The construction probably blance is pointed out in
the marginal arose from an ellipse of honorem. note which follows.
But the measure1 Anyder, or rather Anydrus, "Aw- ments would not
by any means agree. Spos, ' waterless,' is a name in keeping From
London Bridge to the Nore is with the rest. The description of it,
about 45 miles, not 60 ; and the length in some particulars, would
accord with of stream above bridge to its source is that of the
Thames ; and this resem- about 160 miles, not 24.
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accurate

1 28 Cf)e seconD TBofce [CH. n. and dryuethe backe the

fresshe water of the ryuer. And sumwhat furthere yt chaungethe the
swetenes of the freshe water wyth saltnes. But a letell beyonde that,
the ryuer waxeth swet, and runneth forby l the city fresh and
pleisaunt. And when the sea ebbeth, and goyth backe agayn, the
freshe water followeth yt almoste euen to the verye falle in to the
sea. There goeth a brydge ouer the ryuer made not of pyles or of
tymber, but of stonewarke 2, with gorgious and substariciall archeis
at that parte of the cytye that is farthest from the sea ; to the intent
that shyppes maye goo a alonge forbie all the syde of the cytie
without lette. They haue also an other ryuere, whiche in dede is not
very great. But it runneth gentelly and pleasauntlye 3. ft passe.
undis, profligate retrorsum fluuio. Turn aliquanto ultra liquorem eius
salsugine corrumpit ; dehinc paulatim dulcescens amnis syncerus
urbem perlabitur, ac refugientem uicissim purus et incorruptus ad
ipsas propre fauces insequitur. Vrbs aduersae fluminis ripae, non pilis
ac sublicibus ligneis sed ex . opere lapideo egregie arcuato ponte,
commissa est, ab Londinum cum ea parte quae longissime distat a
mari, quo naues Amauroto con- totum id latus urbis possint
inoffensae praeteruehi. uemt. Habent alium praeterea fluuium a,
baud magnum quidem ilium, sed perquam placidum ac iucundum.
Nam ex eodem a gurgitem, A. 1 The German vorbei, ' past.' water-
courses mingling with it, ought 2 According to Maitland, Hist, of to
have been, but never was. A few London, 1739, p. 34, the old
London years before, however, in 1502, scared Bridge, of stone, was
begun in perhaps by the plague of 1500, which 22 Hen. II, and
finished 10 John drove the court to Calais, the citizens (1209). had
done something. ' At this time,' 3 A reminiscence to some extent of
says Maitland (ubi sup.}, 'Fleet Ditch, the Flete river. Our barbarous
treat- being choked with mud and dirt, was ment of rivers and
streams is of very render d intirely useless; wherefore old standing,
and More's description it was now effectually cleans'd, and of this
tributary of the Anyder sets the navigation thereof restored to forth
what the Flete, with the other Holbourn-Bridge, as formerly.'
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CH. Hi of Qtopia, 129 For it ryseth euen out of the same

hyll that the cytie standeth vpon, and runneth downe a slope
through the myddes of the citie into Anyder. And bicause it ryseth a
lytle without the citie, the Amaurotians haue inclosed the head
sprynge of it with stronge fences and bulwarkes, and so haue ioyned
it to the cytie. Thys is done to the intente that the water should not
be stopped, nor turned a waye, or poysoned, if their enemyes
should chaunce to come vpon them 1. From thence the water is
deryued and brought a downe in cannellis of brycke dyuers wayes
into the lower partes of the cytie. Where that cannot be done, by
reason that the place wyll not suffer it, there they gather the rayne
water in greate cisternes2, which doth them as good seruice. The
cytie is compassed aboute wyth a highe and thycke walle b, full of
turrettes and bulwarkes. A drye dyche, but deape and brode and
overgrowen with busshes, briers, and thornes 3, goeth about .iii.
sydes or quarters of the cytie. To the fowrth syde the ryuer it selfe
serueth for a dytche. a conueied. b stone walle. scaturiens rnonte, in
quo ciuitas collocatur, mediam illam per deuexa perfluens Anydro
miscetur. Eius fluuii caput fontemque, quod paulo extra urbem
nascitur, munimentis 'f?,ua( potabilis. amplexi Amaurotam mnxerunt
oppido, ne si qua uis 76 hoistium ingruat, intercipi atque auerti
aqua, neue corrumpi queat. Inde canalibus coctilibus diuersim ad
inferiores urbis partes aqua diriuatur. id sicubi locus fieri uetat,
cisternis capacibus collecta pluuia tantundem usus adfert. Murus
altus ac latus oppidum cingit, turribus ac propugnaculis frequens,
arida fossa, sed alta lataque, ac ueprium sepibus impedita, tribus ad
lateribus circumdat moenia. Moenmm mummentum. quarto flumen
ipsum pro fossa est. Plateae cum ad 1 Comp. 2 Kings xviii. 17. 3 The
ditch or moat surrounding 2 For an example of this on a large the
Tower of London may have been scale, see Davis : Carthage and her
in M ore's mind. This was not, remains, 1861, p. 393. We have not
however, drained and planted till yet learnt to husband our rain-
water.
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130 €&e seconti TBofce CCH.H. The stretes be appoynted

and set forth verye commodious and handsome, bothe for carriage
and also agaynst the wyndes. The houses be of fayre and gorgious
buyldyng, and ina the streete syde they stonde ioyned together in a
longe rowe throughe the hole streate without anye parti tion or
separacion1. The stretes be twenty fote brode 2. On the backe syde
of the houses, through the hole lengthe of the strete, lye large
gardeynes, whyche be closed in b rounde about with the backe parte
of the stretes. Euery house hath two doores ; one into the strete,
and a posternne doore on the backsyde into the gardyne. Thyes
doores be made with two leaues, neuer locked nor bolted, so easye
to be opened that they wil followe the least drawing of a fynger and
shutte agayne by themselfesc. Euerye man thatd wyll maye goo yn,
for there is nothynge wythin the howses that ys pryuate, or annye
mannes owne 3. And euerye .x. yeare they chaunge their howses by
lotte. * on. b [whyche ... in] inclosed. c alone. d [Euery . . . that]
Whoso. uecturam, turn aduersus uentos, descriptae commode.
aedificia Piateae neutiquam sordida, quorum longa et totum per
cuiusmodi. uicum perpetua series aduersa domorum fronte
conAedificia. spicitur. has uicorum frontes uia distinguit pedes
^dhaerIntl»US mgmti lata- Posterioribus aedium partibus, quanta
est Haec sapiunt Ulc* l°ngitudo, hortus adiacet, latus, et uicorum
tergis communitatem undique circumseptus. Nulla domus est, quae
non, Piatonis. ut hostium in plateam, ita posticum in hortum habeat.
Quin bifores quoque facili tractu manus apertiles, ac dein sua sponte
coeuntes, quemuis intromittunt. ita nihil usquam priuati est. Nam
domos ipsas uno quoque decennio sorte commutant. a adhaerentes.
1 This is a lax rendering. The sense 3 Community of dwelling-houses
was is :' a long row of buildings, stretching included in the general
communism the whole length of the streets, makes of the Republic. '
No one,' so it was a fine spectacle, as the fronts of the provided, '
should have a dwelling or houses face you.' storehouse, into which
all who please 2 See the Introduction, § 2, may not enter.' —
DaviesandVaughan's p. xxx. translation, p. 116
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CH.II.] ofOtopta, 131 They sett great stoore be theyr

gardeins. In them they haue vyneyardes1, all manner of frute,
herbes, and flowres, so pleisaunte, so well furnished, and so fynelye
kepte, that I neuer sawe thynge more frutefull nor better trymmed
in anny place. Their studye and delygence herin cummeth not only
of pleasure, but also of a certeyne stryffe and contentyon that is
betwene strete and strete, concernynge the trymmynge,
husbanding, and furnyshyng of their gardeyns, euery man for hys
owne part. And verily yow shall not lyghtly fynde in all the citye
annye thynge that is more commodyous, other for the proffyte of
the citizins, or for pleasure. And therfore it may seme that the first
fownder of the city mynded nothynge so muche as he dyd a thies
gardeyns. For they say that kyng Vtopus himself, euen at the first
begenning, appointed and drew furth the platte fourme of 11 he dyd
omitted. Hos hortos magnifaciunt. in his uineas, fructus, herbas,
floras, habent, tanto nitore cultuque, ut nihil fructuosius usquam
uiderim, nihil elegantius. qua in re studium Vtllltas hortorum etiam
Maroni horum non ipsa uoluptas modo, sed incorum quoque
praedicata?. inuicem de suo cuiusque horti cultu certamen accendit.
et certe non aliud quicquam temere urbe tota reperias, sine ad usum
77 ciuium, siue ad uoluptatem com]modius. eoque nullius rei, quam
huiusmodi hortorum, maiorem habuisse curam uidetur is qui
condidit. Nam totam hanc urbis figuram, iam inde ab initio
descriptam ab 1 The London of More's time was the latter end of last
century. See not without its vineyards, unlikely as Faulkner's
Hammersmith, p. 42. that may now seem. Vine Street, '2 The
reference is to Virg. Georg. iv. Saffron Hill, took its name from the
118: — adjacent vineyard of Ely Place. There Forsitan et pingues
hortos quae cura was another at Westminster, near colendi St.
John's Church. Vinegar-yard, Ornaret, canerem, &c. Drury Lane, is
the Vinegarth yard. This part of his subject, which Virgil An extensive
vineyard, where wine left unfinished, was followed out by was made
and sold, existed near what Columella, and after him by Ren6 is now
Addison Road Station, till Rapin. K 2
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132 €f)e seconD IBofce CCH.H. the city into this fasion and
figure that it hath nowe ; but the gallaunt garnishing, and the
bewtiful setting furth of it, wherunto he sawe that one mans age
wold not suffice, that he left to his posterity. For their Cronicles,
which they kepe written with al deligent circumspection, conteining
the history of M .viic. Ix.1 years, euen from the fyrste conquest of
the Hand, recorde and witnesse that the howses in the beginning
were verye lowe, and lyke homelye cotages, or poore shepparde
howses, made at all aduentures of euerye rude pyece of woodea
that came fyrste to handes, wyth mudde walles, and rydged rooffes
thatched ouer with straw2. But nowe the houses be curiously
builded, after a gorgiouse and gallaunt sort, with .iii. storries one
ouer another 3. The owte sydes of the a tymber. ipso Vtopo ferunt.
Sed ornatum, caeterumque a cultum, quibus unius actatem hominis
baud suftecturam uidit, posteris adiiciendum reliquit. Itaque scriptum
in annalibus habent, quos- ab capta usque insula niille
septing^ntorum ac sexaginta annorum complectentes historiam
diligenter et religiose perscriptos adseruant, aedes initio humiles, ac
veluti casas et tuguria fuisse, e b quolibet ligno temere factas,
parietes luto obductos, culmina in aciem fastigiata stramentis
operuerant. At nunc omnis domus uisenda forma tabulatorum trium.
ft ornatum caeterumque ont. A. b om. A. 1 That is, 1760. 3
According to Martin (Mediaeval 2 Even as late as Evelyn's time, this
Houses and Castles in England, 1862, description would apply to
many parts p. 9) the addition of even a second of England. Salisbury
he describes, storey was of comparatively recent in 1653, as a city
which at small cost introduction. l Late in the fifteenth 'might be
purg'd and render'd infi- and at the beginning of the sixteenth nitely
agreeable, and made one of the century the houses of the preceding
sweetest townes ; but now the common period were almost
universally altered, buildings are despicable and the streets The hall
was divided into two stories. dirty.' Uppingham about the same
Being no longer required for the entertime is remarkable for being '
well tainment of a feodal retinue, a smaller builte of stone, which is
a rarity in height was sufficient ; and the altered that part of
England, where most of customs of the time rendered addithe rural
parishes are but of mud.' — tional bed-room accommodation
necesDiary, ed. 1890, pp. 233, 235. sary. Both purposes were
answered
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CH.II] of CJtopia, 133 walles be made other of harde Flynte

or of plauster, or elles of brycke ; and the ynner sydes be well
strengthened with tymber woorke l. The rooffes be playne and flatte,
couered with a certayne kinde of plaster, that is of no coste, and yet
so tempered that no fyre can hurte or peryshe it, and withstandeth
the violence of the weether better then anye leade. They kepe the
wynde out of their windowes with glasse 2, for it is there much vsed
; and sumwhere also with fyne lynnen clothe dipped in oyle or
parietum facies, aut silice, aut cementis aut latere coctili constructae,
in aluuma introrsus congesto rudere. Tecta in planum subducta,
quae intritisb quibusdam insternunt, nullius impendii, sed ea
temperatura quae nee igni obnoxia sit, et tolerandis tern- vitreae aut
pestatum iniuriis plumbum superet. Ventos e fenestris linteatae
fenesuitro (nam eius ibi creberrimus usus est) expellunt ;
traeinterim3 etiam lino tenui, quod perlucido oleo aut succino
perlinunt. a Loco verborum aut caementis . . . aluum exhibet A. aut
lapide duro aut denique coctile \_sic\ constructae in alueum. Insetit
B. denique ante coctili. b sementis (i. q. caementis\ A. by inserting a
floor at the level of the farm-houses much before the reign bed-
room. From this to the so-called of James I. They are mentioned in
Elizabethan house the transition was a lease dated 1614. In the
houses almost imperceptible.' of richer people they were probably 1
It is interesting to compare with introduced in the reign of Henry
VIII. this what Harrison wrote in 1577, in ' Of old time,' says
Harrison, ' our his Description of England, Bk. II. c. 10 countrie
houses, in steed of glasse, (pp. 233 sqq. in Dr. Furnivall's reprint, did
vse much lattise, and that made 1877). The houses then were still
either of wicker or fine rifts of oke mostly of timber. The ' certayne
kinde in chekerwise.' It is not clear what of plaster' spoken of in the
text, is period Harrison meant by 'of old called plaster of Paris by
Harrison, time,' but he mentions a specimen of made of 'fine
alabaster burned, whereof glazing with beryl as still extant at in
some places we haue great plentie, Sudley castle. As for the use of i
panels and that verie profitable against the of home,' he says that
they are now rage of fire.' A kind of stucco is ' quite laid downe in
euerie place,' also described in Erasmus's Dialogue, and lattices less
used, glass being so Convivium Religiosum. plentiful. Description of
England, as a Eden (State of the Poor, i. p. 77) before, pp. 236, 23.
infers from Harrison's description, in :i Interim, in the sense of
interthe chapter just referred to, that glass dum, is found in Seneca
and Quiawindows were not introduced into tilian.
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1 34 Cf)e seconn I5ofee CCH. n. ambre ; and that for twoo

commodities. For by thys meanes more lyght cummeth in, and the
wynde is better kept out. gemino nimirum commodo. Si quidem ad
eum modum fit, ut et plus lucis transmittat, et uentorum minus
admittat.
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