Studies on growth spurt and aging in higher primates
STUDIES ON GROWTH SPURT AND AGING
IN HIGHER PRIMATES
TETRI WIDIYANI
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
STATEMENT LETTER
I hereby declare that dissertation entitled Studies on Growth Spurt and
Aging in Higher Primates is original result of my own research supervised by
supervisory committee and has never been submitted in any form at any
institution before. All information from other authors cited here are mentioned in
the text and listed in the reference at the end part of the dissertation.
Bogor, February 9th, 2012
Tetri Widiyani
Student ID G362070041
ABSTRACT
TETRI WIDIYANI. Studies on Growth Spurt and Aging in Higher Primates.
Supervised by BAMBANG SURYOBROTO, SRI BUDIARTI and ALEX
HARTANA
Growth is the best global indicator of children’s well-being. It is the
single measurement that best defines the health and nutritional status of
children, just as it provides an indirect measurement of the quality of life of an
entire population. The pattern of human growth reflects the biocultural
evolution of our species. The human pattern of growth and development
(ontogeny) appears to differ markedly from patterns of ontogeny in other
primate species. Three studies are reported here which deal to the growth and
development of human and chimpanzee (Pan troglodytes). These three studies
allow us to contrast the phenomena of adolescence growth spurt and female
elderly bone loss in chimpanzee and human as chimpanzee is the closest species
to humans within extant nonhuman primates. In the first, a cross-sectional study
of growth of the body size and somatotype of 363 Javanese girls and 299
Javanese boys aged 4 to 20 years from Magelang Regency, Indonesia was
described. In the second, cross-sectional and longitudinal studies in the growth
of chimpanzee second metacarpal bone linear dimensions from individuals aged
0 to 43.6 years were used for comparison. While in the third, cross-sectional and
longitudinal studies in the growth of chimpanzee body size (body mass and
anterior trunk length) and second metacarpal bone mineral content were
derived. In measuring the second metacarpal dimensions and mineral content, a
total of 568 radiographs of chimpanzee's proximodistal left hands were used.
They were taken from 68 females and 49 males aged 0 to 43.62 years old. We
applied an image analysis system, Scion Image Release Alpha 4.0.3.2 software
for Windows to measure bone linear dimensions and bone mineral content.
Humans present complex and sinuous growth curves for both body weight and
height. A clear growth spurt could be demonstrated by cross-sectional analysis
in our girl subjects at around aged 11.5 years and in our boy subjects at around
aged 12.5 years. In longitudinal series, not in cross-sectional, several
representative chimpanzees of both sexes showed a pre-adult growth spurt on
the body sizes, bone dimensions and bone mineral content. They ranged at age
4.5 to 8.5 years. This underscore the fact that adolescent growth spurt in linear
dimension was not a universal feature of anthropoid primate ontogeny. Bone
loss is a well established characteristic of human female aging. Based on crosssectional analyses the sequential decline of bone mass in female chimpanzee
may be said to be genuine. On the other hand, we found in adulthood through
elderly, male chimpanzees show a longer plateau than female chimpanzee, that
is, bone mineral content is maintained in male.
Keywords: growth, Javanese children, growth spurt, chimpanzee, second
metacarpal bone, bone loss
ii
ABSTRAK
TETRI WIDIYANI. Studi Lonjak Pertumbuhan dan Penuaan pada Primata
Tingkat Tinggi. Dibimbing oleh BAMBANG SURYOBROTO, SRI
BUDIARTI dan ALEX HARTANA
Pertumbuhan merupakan indikator terbaik untuk menggambarkan status
kesehatan dan gizi anak-anak serta kualitas hidup dalam suatu populasi
penduduk. Pola pertumbuhan manusia, mencerminkan evolusi biokultural
spesies manusia yang nampaknya berbeda dari spesies primata lainnya.
Simpanse (Pan troglodytes) digunakan dalam penelitian ini karena merupakan
spesies terdekat dengan manusia yang belum punah. Penelitian ini terdiri dari 3
bagian yang mengkaji pertumbuhan dan perkembangan manusia dan simpanse.
Bagian pertama merupakan studi cross-sectional untuk pertumbuhan ukuran
dimensi tubuh (bobot badan dan tinggi badan) serta somatotipe dari 363 anak
perempuan dan 299 anak laki-laki Jawa usia 4 sampai 20 tahun, di Kabupaten
Magelang, Indonesia. Bagian kedua adalah studi cross-sectional dan
longitudinal untuk pertumbuhan dimensi linear tulang metakarpal kedua
(panjang, lebar dan tebal korteks) pada simpanse. Bagian ketiga merupakan
studi cross-sectional dan longitudinal untuk pertumbuhan dimensi badan (massa
tubuh dan panjang badan anterior) serta kandungan mineral korteks tulang
metakarpal kedua pada simpanse. Pengukuran dimensi tulang dan kandungan
mineral korteks metakarpal kedua dilakukan secara radiografi pada 568 foto
radiograf tangan kiri dari 68 simpanse betina dan 49 simpanse jantan usia 0
sampai 43,6 tahun. Pengukuran tersebut dilakukan menggunakan software
pengolah gambar Scion Image Release Alpha 4.0.3.2. Rangkaian penelitian ini
memungkinkan untuk membandingkan fenomena lonjak pertumbuhan (growth
spurt) pada tahap remaja dan pengeroposan tulang (bone loss) pada wanita dan
simpanse betina di masa tua. Hasil penelitian ini menunjukkan bahwa manusia
mempunyai kurva pertumbuhan yang kompleks untuk ukuran bobot badan dan
tinggi badan. Lonjak pertumbuhan yang jelas (dibuktikan dengan analisis crosssectional) terjadi pada usia sekitar 11,5 tahun untuk anak perempuan dan sekitar
12,5 tahun untuk anak laki-laki. Pada simpanse, lonjak pertumbuhan tidak dapat
dilihat dengan studi cross-sectional, tetapi hanya dapat dilihat dengan
menggunakan studi longitudinal. Lonjak pertumbuhan ini terlihat pada semua
parameter yang diukur pada simpanse jantan dan betina usia 4,5 sampai 8,5
tahun. Beberapa simpanse betina mengalami bone loss, sejak usia 20 tahun.
Berbeda dengan manusia, simpanse tidak mengalami menopause yang
merupakan penanda penuaan. Simpanse jantan tidak menunjukkan fenomena
tersebut, kandungan mineral tulang tetap dipertahankan.
Kata kunci: pertumbuhan, anak-anak Jawa, lonjak pertumbuhan, simpanse,
tulang metacarpal kedua, bone loss
SUMMARY
TETRI WIDIYANI. Studies on Growth Spurt and Aging in Higher Primates.
Supervised by BAMBANG SURYOBROTO, SRI BUDIARTI and ALEX
HARTANA
Growth is the best global indicator of children’s well-being. It is the single
measurement that best defines the health and nutritional status of children, just as
it provides an indirect measurement of the quality of life of an entire population.
The pattern of human growth reflects the biocultural evolution of our species. The
human pattern of growth and development (ontogeny) appears to differ markedly
from patterns of ontogeny in other primate species. Humans present complex and
sinuous growth curves for both body mass and stature. Many bodily proportions
change dramatically during ontogeny as we reach sizes that are among the largest
of living primates. Perhaps most obviously, humans grow for a long time, with the
interval between birth and maturation exceeding that of all other primate species.
In human, growth is spurted to attain the genetically determined target size in
adult. Growth spurt of body size is a modular and highly evolvable feature of
ontogeny. Therefore the first and major interest in the evolution of growth and
development study is whether non-human primate species have an adolescent
growth spurt corresponding to that of human. Growth spurt could predict the
abnormal development which occurred during pre-adult phases.
Bone mineral loss is a well established characteristic of human aging. It is
found in all human populations. Thus, it is often considered to be a universal
aspect of human ontogeny, although women experience a greater decline in bone
mass during aging than men do. It is well-known that menopause had a major
effect to the evidence of bone loss in many older women. With demographic
shifting into older cohort in population pyramid, bone porosity raises medical
concern. Historically, some species of non-human primates were also generally
considered to exhibit age-related bone loss although they never had menopause.
Comparative investigation on age change of bone mineral content (BMC) in nonhuman primates is therefore necessary for the evolutionary consideration of
growth (ontogeny) and aging and to find suitable model to study bone loss.
In considering the evolution of biological characteristics of primates and
the interrelationships of species-specific life history, ecology, and life-style,
comparison of growth and development of several primates are essential.
Specifically, to understand the evolutionary characteristic of human life history
we investigate the growth pattern of the closest species to humans within extant
nonhuman primates, the chimpanzee (Pan troglodytes). Longitudinal and crosssectional data for body sizes (body mass (BM) and anterior trunk length (ATL)),
second metacarpal dimensions (bone length, bone width and cortical thickness)
and second metacarpal BMC (metacarpal cortical index (MCI) and cortical
density) were collected from chimpanzees belong to Primate Research Institute of
Kyoto University, Japan Monkey Center (Inuyama) and Kumamoto Primates
Research Park, Sanwa Kagaku Kenkyusho Co. Ltd. in Japan. Bone dimensions
and mineral content were measured from the radiographs of chimpanzee's
x
proximodistal left hands using an image analysis system, Scion Image Release Alpha
4.0.3.2 software.
We evaluated the growth pattern of Javanese population in updating data
for infants, children and adolescence cross-sectionally to overcome the cost and
the long time period required for a longitudinal study in human growth. We
selected children (aged 4 to 20 years) from Magelang Regency, Central Java
Province Indonesia. They were observed from the viewpoint of anthropometrical
characteristics. Body size of girls at the age of 4 years were 13 kg in body weight
and 100 cm in body height, while the boys’s were 15 kg in body weight and 100
cm in body height. Girls’s increased to 47 kg in body weight and 150 cm in body
height, while boys’s increased to 58 kg in body weight and 167 cm in body height
at the age of 20 years. They were shorter and lighter than reference children from
U.S., Japan, and Yogyakarta but they improved when compared with those of the
same ethnic of Bantul and with the different ethnic of rural India. A clear
adolescence growth spurt was demonstrated by cross-sectional analysis in body
weight and height of both sexes. They did not differ to the results on growth
velocity standards which were constructed longitudinally. Nevertheless velocity
peak of our children subjects was less than that of reference children which came
from well-off population. There was a clear age-related change in their
somatotype. At the age of 4 years, the physique of both sexes is found to be
mesomorph-endomorph (somatotype score 4-4-2 in girl or 3-4-2 in boy).
Thereafter it is transformed into ectomorphic-endomorph (4-2-3) in girls and to
mesomorph-ectomorph (1-3-5) in boys at the age of 20 years.
Chimpanzee exhibited an initial increase in bone dimensions and BMC
with age. Bone length and width accelerated for the first 8 years of age, whereas
cortical thickness accelerated longer until around 14 years of age. MCI increased
for first 6 to 7 years of age, whereas cortical density increased for a longer period
than MCI, until around 10 years of age. Sexual difference in bone length, cortical
thickness and BMC, which was greater in males than in females, has been
apparent significantly except in bone width which was unclear. Bone dimensions
maturated at about 13 years of age while BMC maturated at around age 10 to 12
years for MCI and 16 years for cortical density. During adulthood through aging,
bone length and width tended to plateau for both sexes. Cortical thickness in
female chimpanzees tended to decrease, but in males increasing instead. Crosssectional analyses of chimpanzee in body mass also showed a pre-adult growth
spurt but in ATL, three bone dimensions and BMC, the spurt could not be seen.
However, by longitudinal analyses all parameters showed spurts in several
chimpanzee individual of both sexes. It was found that there was a wide interindividual age variation in this growth spurts. During aging, the BMC of many
females declined but males’s continued its plateau phase or increase instead.
Some female chimpanzees even experienced bone loss earlier, approximately
since age 20 years.
Keywords: growth, Javanese children, anthropometric measurement, growth
spurt, cross-sectional study, longitudinal study, chimpanzee, second metacarpal
bone, radiography, aging, bone loss
xi
Copyright © 2012. Bogor Agricultural University.
All Rights Reserved
Prohibited to cite all or a part of this dissertation without referring to and
mentioning the source. Citation permits to the purposes of education, research,
scientific paper, report, or critism writing only; and it does not defame the name
and honor of Bogor Agricultural University.
Prohibited to republish and reproduce all or a part of this dissertation without
permission of Bogor Agricultural University.
STUDIES ON GROWTH SPURT AND AGING
IN HIGHER PRIMATES
TETRI WIDIYANI
Dissertation
submitted in partial fulfillment of the requirements for a Doctoral Degree in
Animal Bioscience Major of Graduate School of Bogor Agricultural University
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
ii
Examiners in the Close examination:
1. Prof. Ir. Wasmen Manalu, Ph.D. (Professor of Faculty of Veterinery,
Bogor Agricultural University)
2. Dr. Astuti Lamid, M.CN. (Researcher of Center for Applied Health
Technology and Clinical Epidemiology, Research and Development
of Indonesian Health Ministry)
Examiners in the Open examination:
1. Prof. Yuzuru Hamada, D.Sci. (Professor of Primate Research
Institute, Kyoto University)
2. Prof. Dr. dr. Agus Purwadianto, S.H., M.Si., Sp.F (K). (Professor of
Faculty of Medicine, Indonesia University and Expert Staff of
Indonesian Health Ministry)
iii
Title
: Studies on Growth Spurt and Aging in Higher Primates
Name
: Tetri Widiyani
Student ID
: G362070041
Major
: Animal Biosciences
Endorsed by,
Supervisory Committee
Dr. Bambang Suryobroto
Chairman
Dr. dr. Sri Budiarti
M.Sc.
Member
Prof. Dr. Ir. Alex Hartana,
Member
Head of Animal Bioscience Major
Dean of Graduate School,
Dr. Bambang Suryobroto
M.Sc.Agr.
Dr. Ir. Dahrul Syah,
Examination date: January 17, 2012
Graduation date:
PREFACE
This dissertation is submitted in partial fulfillment of the requirements for
a Doctoral Degree for the author in Graduate School of Bogor Agricultural
University. It represents a culmination of work and learning that has taken place
over a period of almost five years (2007 – 2011). The work addresses three topics
related to the evolutionary of growth and development. Author had granted
Scholarship for Post-graduate Study (BPPS) during periods 2007 to 2010 and
Scholarship of Sandwich-Like Program in 2008 from the Indonesian Ministry of
Education, Directorate General of Higher Education (DIKTI). A portion of
dissertation (topic I) entitled The Growth of Body Size and Somatotype of
Javanese Children Aged 4 to 20 Year was published in Hayati Journal of
Biosciences Vol. 18 No. 4, December 2011.
This work could only be succeeded thanks to the invaluable contribution
of many people. First and foremost I am grateful for the generous support of my
supervisory chair, Dr. Bambang Suryobroto, who has been with me throughout
the years as mentor, editor and friend and introduced me to Professor Dr.Yuzuru
Hamada from Primate Research Institute Kyoto University. I am glad I could
work in Hamada’s laboratory to study the evolutionary growth and aging of
chimpanzee. It was a great learning experience doing collaboration research with
international researcher who is very competent in evolutionary morphology field.
I also extend special thanks to both co-adviser, Dr. dr. Sri Budiarti and Professor
Dr. Alex Hartana, who guided me through the process of developing confidence
as an academic.
I am very grateful to Rector of Sebelas Maret University for the
permission to pursue doctoral study in Graduate School of Bogor Agricultural
University. I am also grateful to the Government of Magelang Regency for the
permission of this study and to the school principals, teachers and all the children
subjects for all their support throughout the study in Magelang. Thanks to all staff
of Primate Research Institute Kyoto University Japan for their help and
permission throughout study there.
xviii
There are many other people without whom I would never have made it to
the end of a successful graduate career. Thanks to people at Zoo Corner ‘Z-Co’
(Kanthi A. Widayati, M.Si., E. Nunuz Rohmatullayaly, S.Si., Sarah Nila, S.Si.,
Islamul Hadi, M.Si., J.J. Elda Irma Kawulur, M.Si., Puji Rianti, M.Si., Gres
Maretta, M.Si., Indra, S.Si., Reny Kristianti Aryo, S.Si., Norita Widya Pangestika,
S.Si., Sekar Sukmaningrasa, M.Si., Yuliadi Zamroni, M.Si., Dr. Achmad
Farajallah, M.Si., Dr. Rika Raffiudin, Dr. Bambang Kiranadi, Mrs. Anik, Mrs.
Tini Wahyuni, Mr. Adi Surachman, Mr. Agus, and so on) for opportunities to
share thoughts and fun. Thanks to people at Pondok Putri Arum and Wisma Intan
for making me feel at home far away from home. In addition, thank you to friends
on Twitter and Facebook for making it less lonely during working at Inuyama
Japan and Bogor.
My highest expression of gratefulness is for my family. I thank my parents
(‘mamah’ dr. Kustiyah Marwi and ‘ibuk’ Tuti Sriani) for life and the strength and
determination to live it. My special thanks to my husband Eko Kurniawan and my
daughter Aulia Alifiani for the unconditional love and unfailing patience and
support. This dissertation is equally their achievement. Therefore, above all, I
thank God Allah SWT since this work would not be possible without His
almighty.
Bogor, February 2012
Tetri Widiyani
xix
CURRICULUM VITAE
The author was born in Surakarta, Central Java at December 24, 1971 by
Tuti Sriani. Author married with Eko Kurniawan, S.T. at August 10, 2002 and had
a daughter, Aulia Alifiani. Bachelor degree was earned from Department of
Zoology, Faculty of Biology, Gadjah Mada University in the beginning of 1998.
In the middle of 1998, she obtained DUE scholarship from the Indonesian
Ministry of Education, Directorate General of Higher Education (DIKTI) for
pursuing Master Degree at Graduate School of Gadjah Mada University on
Biology field and graduated at May 2001.
Since March 1, 2000 she has working as a lecturer at Department of
Biology, Faculty of Mathematics and Natural Science, Sebelas Maret University
Surakarta, Central Java. The main course which lectured is Animal Structure and
Development.
Other
courses
were
Animal
Eco-morphology,
Animal
Microtechnique, Teratology, and Experimental Anatomy. From the middle 2007
to the middle 2010, author got Scholarship for Graduate Study (BPPS) from the
Indonesian Ministry of Education, Directorate General of Higher Education
(DIKTI) for pursuing a Doctoral Degree at Graduate School of Bogor Agricultural
University on the Major of Animal Bioscience.
During November 2008 to February 2009, she did a collaboration research
with Primate Research Institute, Kyoto University Japan in the Sandwich-like
Program which funded by Indonesian Ministry of Education, Directorate General
of Higher Education (DIKTI). A paper entitled The Growth of Body Size and
Somatotype of Javanese Children Aged 4 to 20 Years which was a partial of
Doctorate theses of her was published in Hayati Journal of Biosciences Vol. 18
No. 4, December 2011. Author has a membership in Asia-Pacific Chemical,
Biological and Environmental Engineering Society (APCBEES).
xxi
CONTENTS
Page
CONTENTS.....................................................................................................XXI
LIST OF TABLES..........................................................................................xxiii
GENERAL INTRODUCTION.............................................................................1
Background.....................................................................................................1
Objectives and Benefits..................................................................................3
LITERATURE STUDIES....................................................................................5
Growth and Development...............................................................................5
Bone growth and maturation..........................................................................7
Radiography in bone aging assessment..........................................................9
Chimpanzee..................................................................................................14
THE GROWTH OF BODY SIZE AND SOMATOTYPE OF JAVANESE
CHILDREN AGE 4 TO 20 YEARS IN MAGELANG REGENCY..................19
Abstract.........................................................................................................19
Introduction...................................................................................................19
Materials and Methods.................................................................................21
Subjects ..................................................................................................21
Measurements ........................................................................................22
Data analysis...........................................................................................23
Result............................................................................................................24
Sociodemographic characteristic............................................................24
Body sizes...............................................................................................26
Somatotype.............................................................................................31
Discussion.....................................................................................................33
Conclusion....................................................................................................37
AGE-RELATED CHANGES OF SECOND METACARPAL LENGTH,
WIDTH AND CORTICAL THICKNESS IN CHIMPANZEES.......................39
Abstract.........................................................................................................39
Introduction...................................................................................................39
Materials and methods..................................................................................41
Result............................................................................................................45
Cross-sectional analysis on age-related changes of bone length and
width.......................................................................................................45
Cross-sectional analysis on age-related changes of cortical thickness...49
Longitudinal analysis on age-related changes of bone dimensions........51
Longitudinal analysis on growth velocity of bone dimensions .............57
Discussion.....................................................................................................65
Conclusion....................................................................................................67
AGE-RELATED CHANGES OF MINERAL CONTENT IN THE CORTICAL
BONE OF CHIMPANZEE’S SECOND METACARPAL................................69
Abstract.........................................................................................................69
Introduction...................................................................................................69
Materials and Methods.................................................................................72
Result............................................................................................................77
xxii
Cross-sectional analysis on age-related changes of metacarpal cortical
index.......................................................................................................77
Cross-sectional analysis on age-related changes of cortical density......80
Relationship between MCI, cortical density and body size....................82
Longitudinal age-related changes of MCI..............................................84
Longitudinal age-related changes of cortical density.............................89
Cross-sectional and longitudinal analysis on growth of body mass and
anterior trunk length ..............................................................................91
Discussion.....................................................................................................94
Conclusion..................................................................................................100
GENERAL DISCUSSION...............................................................................101
GENERAL CONCLUSION.............................................................................107
REFERENCES.................................................................................................109
xxiii
LIST OF TABLES
Page
TABLE 1 SOCIODEMOGRAPHIC CHARACTERISTIC OF CHILDREN
INCLUDED THE STUDY.............................................................26
TABLE 2 PREVALENCE OF UNDERWEIGHT, NORMAL, OVERWEIGHT,
AND OBESE ACCORDING TO BODY MASS INDEX (BMI)
PERCENTILES AND PREVALENCE OF UNDERFAT,
HEALTHY, OVERFAT, AND OBESE ACCORDING TO
PERCENTAGE OF BODY FAT (PBF) PERCENTILES AMONG
CHILDREN SUBJECTS LIVED IN MAGELANG REGENCY..30
TABLE 3 CHIMPANZEE SUBJECTS FOR THE STUDY.............................43
TABLE 4 NUMBER OF RADIOGRAPHS .....................................................44
TABLE 5 SUMMARY OF GROWTH SPURT IN THE SECOND
METACARPAL BONE LENGTH CHIMPANZEE ....................60
TABLE 6
SUMMARY OF GROWTH SPURT IN THE SECOND
METACARPAL BONE WIDTH OF CHIMPANZEE FROM
LONGITUDINAL DATA..............................................................61
TABLE 7 SUMMARY OF GROWTH SPURT IN THE SECOND
METACARPAL CORTICAL THICKNESS OF CHIMPANZEE
FROM LONGITUDINAL DATA.................................................61
TABLE 8 NUMBER OF RADIOGRAPHS ......................................................77
TABLE 9
SUMMARY OF THE SECOND METACARPAL CORTICAL
INDEX (MCI) GROWTH SPURT IN CHIMPANZEES FROM
THE LONGITUDINAL STUDY...................................................89
TABLE 10 SUMMARY OF THE BODY MASS (BM) GROWTH SPURT IN
CHIMPANZEES FROM THE LONGITUDINAL STUDY.........92
TABLE 11 SUMMARY OF THE ANTERIOR TRUNK LENGTH (ATL)
GROWTH SPURT IN CHIMPANZEES FROM THE
LONGITUDINAL STUDY............................................................93
TABLE 12 COMPARISON OF GROWTH SPURTS OF CHIMPANZEE IN
SEVERAL CHARACTERS ........................................................102
TABLE 13 COMPARISON OF BODY HEIGHT AND BODY WEIGHT
GROWTH SPURTS IN JAVANESE CHILDREN FROM THE
PRESENT STUDY WITH DIFFERENT ETHNIC GROUPS....104
xxiv
xxv
LIST OF FIGURES
Page
FIGURE 1 MEASUREMENTS MADE IN RADIOGRAMMETRY OF THE
METACARPAL...........................................................................11
FIGURE 2 DENSITOMETRIC PATTERN OF A CROSS-SECTIONAL MIDSHAFT BONE..............................................................................12
FIGURE 3 SCHEMATIC REPRESENTATION OF A STEP WEDGE AND
BELOW IT THE RADIOGRAPHIC IMAGE IT WOULD BE
EXPECTED TO PRODUCE (SYMMONS 2004). .....................13
FIGURE 4
MAP OF MAGELANG REGENCY IN CENTRAL JAVA
PROVINCE INDONESIA SHOWING THE STUDY SITES (▼).
.......................................................................................................22
FIGURE 5 GROWTH CHART OF BODY WEIGHT IN GIRLS (LEFT,
SOLID LINES) AND BOYS (CENTER, DASHED-LINES) AGE
4 TO 20 YEARS LIVED IN MAGELANG REGENCY.............27
FIGURE 6 GROWTH CHART OF BODY HEIGHT IN GIRLS (LEFT, SOLID
LINES) AND BOYS (CENTER, DASHED-LINES) AGE 4 TO
20 YEARS LIVED IN MAGELANG REGENCY......................28
FIGURE 7 GROWTH CHART OF BODY MASS INDEX IN GIRLS (LEFT,
SOLID LINES) AND BOYS (CENTER, DASHED-LINES) AGE
4 TO 20 YEARS LIVED IN MAGELANG REGENCY.............29
FIGURE 8 GROWTH CHART OF BODY FAT IN GIRLS (LEFT, SOLID
LINES) AND BOYS (CENTER, DASHED-LINES) AGE 4 TO
20 YEARS LIVED IN MAGELANG REGENCY......................30
FIGURE 9 THE 50TH PERCENTILE VALUES OF SOMATOTYPE
COMPONENTS SCORE IN CHILDREN AGE 4 TO 20 YEARS
LIVED IN MAGELANG REGENCY. ........................................32
FIGURE 10 SOMATOPLOT OF THE 50TH PERCENTILE SOMATOTYPE
SCORE (BOLD NUMBERS) OF GIRLS (LEFT) AND BOYS
(RIGHT) LIVED IN MAGELANG REGENCY BY AGE, 4 TO
20 YEARS. ..................................................................................32
FIGURE 11 CORRELATION OF ENDOMORPHY COMPONENT OF
SOMATOTYPE TO THE BODY MASS INDEX (BMI) AND
PERCENTAGE OF BODY FAT (PBF) IN GIRLS (○) AND
BOYS (×). ..................................................................................33
FIGURE 12 COMPARISON OF BODY HEIGHT (TOP) AND BODY
WEIGHT (BOTTOM) IN JAVANESE CHILDREN FROM THE
PRESENT STUDY WITH DIFFERENT ETHNIC GROUPS. . .35
xxvi
FIGURE 13 A RADIOGRAPH OF CHIMPANZEE LEFT HAND (A) WITH A
TRANSPARENT
RULER
TO
SCALE
LINEAR
MEASUREMENTS EXHIBITS THE POSITION OF SECOND
METACARPAL BONE................................................................42
FIGURE 14 AGE-RELATED CHANGE OF THE SECOND METACARPAL
LENGTH IN FEMALE (LEFT) AND MALE (CENTER)
CHIMPANZEES FROM THE CROSS-SECTIONAL STUDY..45
FIGURE 15 VELOCITY CURVES FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL LENGTH IN FEMALE AND
MALE CHIMPANZEES PREDICTED FROM THE 50TH
PERCENTILE OF THE CROSS-SECTIONAL AGE-CHANGE
CURVE. .......................................................................................46
FIGURE 16 AGE-RELATED CHANGE OF THE SECOND METACARPAL
WIDTH IN FEMALE (LEFT) AND MALE (CENTER)
CHIMPANZEES FROM THE CROSS-SECTIONAL STUDY..47
FIGURE 17 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL WIDTH IN FEMALE AND
MALE CHIMPANZEES PREDICTED FROM THE 50TH
PERCENTILE OF THE CROSS-SECTIONAL AGE-CHANGE
CURVE. .......................................................................................48
FIGURE 18 AGE-RELATED CHANGE OF THE RATIO BONE WIDTH TO
BONE LENGTH IN FEMALE (LEFT) AND MALE (CENTER)
SECOND METACARPAL CHIMPANZEES FROM THE
CROSS-SECTIONAL STUDY. ..................................................49
FIGURE 19 AGE-RELATED CHANGE OF THE CORTICAL THICKNESS
IN FEMALE (LEFT) AND MALE (CENTER) SECOND
METACARPAL CHIMPANZEES FROM THE CROSSSECTIONAL STUDY..................................................................50
FIGURE 20 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE CORTICAL THICKNESS SECOND METACARPAL IN
FEMALE AND MALE CHIMPANZEES PREDICTED FROM
THE 50TH PERCENTILE OF THE CROSS-SECTIONAL AGECHANGE CURVE.......................................................................50
FIGURE 21 CURVES OF AGE-RELATED CHANGE IN THE SECOND
METACARPAL BONE LENGTH FROM LONGITUDINAL
STUDY.........................................................................................52
FIGURE 22 CURVES OF AGE-RELATED CHANGE IN THE SECOND
METACARPAL BONE WIDTH FROM LONGITUDINAL
STUDY.........................................................................................55
FIGURE 23 CURVES OF AGE-RELATED CHANGE IN THE SECOND
METACARPAL
CORTICAL
THICKNESS
FROM
LONGITUDINAL STUDY..........................................................56
xxvii
FIGURE 24 VELOCITY CURVE OF THE SECOND METACARPAL BONE
LENGTH GROWTH OF MALE CHIMPANZEES FROM
LONGITUDINAL STUDY..........................................................59
FIGURE 25
VELOCITY CURVE OF THE SECOND METACARPAL
BONE WIDTH GROWTH OF FEMALE CHIMPANZEES
FROM LONGITUDINAL STUDY..............................................62
FIGURE 26
VELOCITY CURVE OF THE SECOND METACARPAL
CORTICAL
THICKNESS
GROWTH
OF
FEMALE
CHIMPANZEES FROM LONGITUDINAL STUDY.................64
FIGURE 27 PROCEDURE TO MEASURE CORTICAL DENSITY (NOT TO
SCALE). .......................................................................................75
FIGURE 28 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL INDEX (MCI) IN FEMALE (LEFT) AND MALE
(CENTER) CHIMPANZEES FROM THE CROSS-SECTIONAL
STUDY.........................................................................................78
FIGURE 29 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL INDEX (MCI) IN FEMALE AND MALE
CHIMPANZEES AGE 0 TO 18 YEARS DERIVED FROM THE
50TH PERCENTILE. ..................................................................79
FIGURE 30 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL INDEX (MCI) IN
FEMALE AND MALE CHIMPANZEES FROM THE CROSSSECTIONAL STUDY..................................................................80
FIGURE 31 CURVES OF AGE-CHANGE OF THE CORTICAL DENSITY IN
THE SECOND METACARPAL IN FEMALE (LEFT) AND
MALE (CENTER) CHIMPANZEES FROM THE CROSSSECTIONAL STUDY. ................................................................81
FIGURE 32 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL DENSITY IN FEMALE AND MALE
CHIMPANZEES AGE 0 TO 18 YEARS DERIVED FROM THE
50TH PERCENTILE. ..................................................................81
FIGURE 33 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL DENSITY IN
FEMALE AND MALE CHIMPANZEES FROM THE CROSSSECTIONAL STUDY..................................................................82
FIGURE 34 PLOTTING OF AGE AVERAGES OF METACARPAL
CORTICAL INDEX (MCI), CORTICAL DENSITY (CD),
ANTERIOR TRUNK LENGTH (ATL), AND BODY MASS
(BM) IN FEMALE (RED BLOCKED CIRCLES) AND MALE
CHIMPANZEES (BLACK BLOCKED CIRCLES) DURING
AGE 0 TO 12 YEARS (LEFT) AND AFTER AGE 12 YEARS
(RIGHT). ......................................................................................83
xxviii
FIGURE 35 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL INDEX OF CHIMPANZEE FROM THE
LONGITUDINAL STUDY WITH INCLUDING THE 25TH
AND 75TH PERCENTILE OF STANDARD CHARTS WHICH
HAD GOTTEN FROM THE CROSS SECTIONAL ANALYSES.
.......................................................................................................85
FIGURE 36 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL INDEX (MCI) IN
FEMALE CHIMPANZEES FROM THE LONGITUDINAL
STUDY.........................................................................................87
FIGURE 37 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL INDEX (MCI) IN
MALE CHIMPANZEES FROM THE LONGITUDINAL
STUDY.........................................................................................88
FIGURE 38 AGE-RELATED CHANGE OF MINERAL DENSITY IN THE
SECOND METACARPAL CORTEX OF CHIMPANZEE FROM
THE LONGITUDINAL STUDY WITH INCLUDING THE
25TH AND 75TH PERCENTILE OF STANDARD CHARTS
(DASHED LINE FOR FEMALE OR DOTTED LINE FOR
MALE) WHICH HAD GOTTEN FROM THE CROSS
SECTIONAL ANALYSES, N=NUMBER OF DATA,
F=FEMALE SUBJECT AND M=MALE SUBJECT..................90
FIGURE 39 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
MINERAL DENSITY IN THE SECOND METACARPAL
CORTEX OF THREE REPRESENTATIVES CHIMPANZEE.. 91
FIGURE 40 VELOCITY CURVE FOR THE BODY MASS (A AND C) AND
ANTERIOR TRUNK LENGTH (B AND D) GROWTH FROM
THE CROSS-SECTIONAL STUDY (A AND B) AND
LONGITUDINAL STUDY (C AND D) IN FEMALE (F) AND
MALE (M) CHIMPANZEES.......................................................93
FIGURE 41 COMPARISON OF GROWTH VELOCITY OF BODY HEIGHT
AND BODY WEIGHT IN JAVANESE CHILDREN FROM THE
PRESENT STUDY (RED LINES) WITH JAVANESE
CHILDREN FROM THE LONGITUDINAL STUDY (BLUE
LINES) AND BELGIAN CHILDREN FROM THE
LONGITUDINAL STUDY (BLACK LINES)..........................103
LIST OF ABBREVIATIONS
ANOVA
analysis of variance
ATL
anterior trunk length
BM
body mass
BMC
bone mineral content
BMD
bone mineral density
BMI
body mass index
CT
cortical thickness
FM
fat mass
FFM
fat free mass
HSD
honest significant difference
HWR
height weight ratio
IDR
Indonesian Rupiah
MCI
metacarpal cortical index
NCHS
National Center for Health Statistics
NHES
National Health Examination Surveys
NHANES
National Health and Nutrition Examination
PBF
percentage of body fat
WHO
World Health Organization
GENERAL INTRODUCTION
Background
The pattern of human growth reflects the biocultural evolution of our
species (Bogin 1999). The human pattern of growth and development
(ontogeny) appears to differ markedly from patterns of ontogeny in other
primate species. Humans present complex and sinuous growth curves for both
body mass and stature. Many bodily proportions change dramatically during
ontogeny as we reach sizes that are among the largest of living primates.
Perhaps most obviously, humans grow for a long time, with the interval
between birth and maturation exceeding that of all other primate species (Leigh
2001). In considering the evolution of biological characteristics of primates and
the interrelationships of species-specific life history, ecology, and life-style,
comparison of growth and development of those primates are essential.
Specifically, to understand the evolutionary characteristic of human life history
we need knowledges of growth and development of the closest species to
humans within extant nonhuman primates, the chimpanzee (Pan troglodytes)
(Perelman et al. 2011). At present, the knowledge of growth and development
of chimpanzee is scarce because the population accessible for the study is small,
as chimpanzees are large animals with a long lifespan and growth period.
Growth can be studied in several ways. The two basic approaches are
cross-sectional and longitudinal studies. In a cross-sectional study, individuals
are usually measured or observed only once at their given age and the total
sample may then be categorized arbitrarily into different age cohorts to produce
age-related progress of body properties. Cross-sectional analyses are
economical because the study can be carried on in a short time period. A
longitudinal study, on the other hand, involves repeated observations on the
same individuals at specific intervals over a long period of time (Malina et al.
2004). It is more difficult to conduct longitudinal than cross-sectional study
because it needs patience and takes a long time to be completed. Therefore there
are more cross-sectional studies than longitudinal studies of child growth.
Nevertheless, Hamada and Udono (2002) stated that cross-sectional analysis is
2
not suitable for a fined-tuned and short-duration phenomenon such as the
growth spurt. The adolescent growth spurt in linear dimension was regarded as
unique to humans until it was also found to occur in non-human primates
(Tanner et al. 1990; Hamada et al. 1999). Nevertheless, although growth in
linear dimension is accelerated at chimpanzee puberty, the acceleration is not as
great as that in humans (Hamada and Udono 2002). It is vital to develop a way
of showing whether the chimpanzee has a real spurt or not, and of
discriminating a true spurt from acceleration due to ontogenetic plasticity.
The growth of children is important for the health of the new generation.
It most accurately reflects the health of a population (Onis and Blössner 2003)
and, in all its aspects, is of priority concern to the World Health Organization
(Onis et al. 2007). There are large between-population variation and it is now
clear that a portion of these differences is of genetic origin and a portion (in the
developing countries a large portion) is of environmental origin (Eveleth and
Tanner 1990; Ulijaszek 1993; Bogin 1999). Ulijaszek (2006) summarized
several known environmental factors that influence growth of children
postnatally. They include nutrition, infection, interactions between the two,
psychosocial stress, altitude, and climate. Most of these factors are conditioned
by socioeconomic status.
We evaluated the growth pattern of Javanese population in updating data
for infants, children and adolescence cross-sectionally to overcome the cost and
the long time period required for a longitudinal study in human growth. We
selected children (aged 4 to 20 years) from Magelang Regency, Central Java
Province
Indonesia.
They
were
observed
from
the
viewpoint
of
anthropometrical characteristics. We aim to show growth spurt of body size. A
longitudinal study in chimpanzee was used for a comparison. We analyzed the
growth pattern of body size and of the second metacarpal bone derived from a
longitudinal, repeated measurement of chimpanzee individuals aged 0 to 43.6
years. The longitudinal approach was expected to reveal growth spurt in this
species. The longer period covering older age in chimpanzee allowed us to
observe age-related changing in aging individuals. Human bone is characterized
by a gradual decrease in adulthood and a rapid loss of bone mineral content in
3
postmenopausal women (Schneider et al. 1997; Osei-Hyiaman et al. 1998;
Warming et al. 2002; Ahlborg et al. 2003; Finkelstein et al. 2008; Min et al.
2010). Menopause is not a typical characteristic of chimpanzee life histories
(Thompson et al. 2007; Lacreuse et al. 2008), so it is a point of interest to see
whether or not chimpanzee experience bone loss while aging.
Objectives and Benefits
Comparative studies on growth and aging of several primates are
important to understand the evolutionary characteristic of human life history
and to provide models and insights to efforts in increasing the quality of life.
Therefore the objectives of the study are:
1. a. To evaluate the growth of body size (height and weight) in the Javanese
children aged 4 to 20 years and to compare to that of several reference
populations.
b. To evaluate the growth of body shape (somatotype) in the Javanese
children aged 4 to 20 years.
2. a. To evaluate growth of body size (anterior trunk length and body mass) in
the chimpanzee aged 0 to 43.6 years
b. To evaluate the age-related changes of the mid shaft second metacarpal
dimensions (length, width and cortical thickness) for female and male
chimpanzee aged 0 to 43.6 years using radiographs.
c. To delineate the cross-sectional and longitudinal age-related changes in
the mineral content at the mid-shaft of the second metacarpal of
chimpanzee aged 0 to 43.6 years using radiographs.
3. a. To define whether the chimpanzee has a real growth spurt in its second
metacarpal dimensions and mineral content.
b. To define whether the chimpanzee experiences bone loss in aging.
LITERATURE STUDIES
Growth and Development
Growth of an individual is a dynamic process that is characterized by
physiological changes in infancy, childhood, and adolescence. These growth
periods relate to differences in various underlying genetic, hormonal and
nutritional factors and ultimately lead to differences in skeletal maturation and
development in an individual child. In a child who is physically and emotionally
healthy, and is adequately nourished, growth will proceed at a normal rate.
However, normal growth is not a uniform process and is dependent on the sex
and racial as well as ethnic background of the child. Environmental change is
also a determinant of later physiological and pathological events in growth
process (Gokhale and Kirschner 2003; Dominé et al. 2006).
Growth during infancy phase, up to the age of 2–3 years, is more rapid
than at any other time (Malina et al. 2004). It is a continuation of fetal growth.
In the neonatal phase, growth is dependent upon maternal, placental and fetal
factors (Godfrey et al. 1996). Maternal factors include maternal nutrition,
maternal size, infections and environmental exposure. Placental factors include
vascular abnormalities, placental hormones and hypoxia. Chromosomal
abnormalities or syndromes within the fetus itself also influence the fetal growth
(Resnik 2002).
The childhood phase begins around the preschool years and continues
until puberty. Many hormones, primarily growth hormone, influence skeletal
and somatic growth during this phase. Thyroxine, glucocorticoids, insulin,
oestrogens and androgens along with polypeptide growth factors also contribute
to growth. Therefore nutrition is an important component of this phase.
However, overfeeding during this phase has important implications, since it
may lead to childhood obesity and, subsequently, to obesity in adulthood, with
associated health risks (Cameron and Demerath 2002; Gokhale and Kirschner
2003).
Adolescence is the phase that begins with the onset of pubertal changes
and extends until growth and maturation are completed in adulthood. Puberty is
defined as the transient period between childhood and adulthood during which
6
reproductive function is attained. During this period, the secondary sexual
characteristics appear, the adolescent growth spurt occurs, the gonads start to
produce mature gametes (sperm or oocytes) capable of fertilization, and major
psychological changes occur. It is generally considered that human puberty is
the result of two independent physiological processes, namely gonadarche and
adrenarche. Gonadarche refers to the activation of the ovary or testis at the end
of the prepubertal phase of development and leads to the dramatic increase in
gonadal steroid production and the completion of gametogenesis. The unfolding
of gonadarche is manifested by thelarche and menarche in girls, or by testicular
enlargement and virilization in boys. Adrenarche, on the other hand, refers to
the maturation of the adrenal cortex that leads to increased secretion of adrenal
androgens and is manifested by the appearance of sexual hair, a process termed
pubarche. It is interesting to note that adrenarche appears to be peculiar to man
and the Great Apes and the absence of adrenarche in humans do not appear to
prevent fertility or markedly to influence the timing and tempo of gonadarche.
The secretory products of the hypothalamic-pituitary-gonadal axis are the
primary modulators of the somatic changes that appear during puberty in higher
primates including man. Growth hormones are also necessary to realize the full
growth promoting effects of gonadal steroids (Terasawa and Fernandez 2001;
Garnett et al. 2004; Plant and Barker-Gibb 2004; Ebling 2005; Patton and Viner
2007).
Physical development reflects the overall patterns of growth and
morpho-functional maturation of a child. The linear dimensions of the body are
the essential indicators of physical development. The physical changes that
occur include growth acceleration and the changes in fat, muscle, and bone
mass. Anthropometry is used in characterizing growth and well-being not only
for individual assessments but also for reflecting the health status and social and
economic circumstances of populations throughout the life cycle. Actual height,
weight,
and
other
anthropometrics
dimension
including
skinfolds,
circumferences, and breadths serve useful purpose in assessing growth, body fat
distribution, and for provision of reference data. The World Health Organization
(WHO) provides a guidance on the appropriate use and interpretation of
7
anthropometric indices. WHO adopts the reference growth charts of the
National Center for Health Statistics (NCHS) of US for international use. The
most commonly used anthropometric indexes for assessing child growth are
weight-for-height,
height-for-age,
weight-for-age,
and
mid-upper-arm
circumference. Whereas for adolescents are height-for-age, body mass index
(BMI)-for-age, and triceps and subscapular skinfold thicknesses-for-age (Onis
and Habitch 1996; Scheplyagina and Moisseyeva 2005; Borghi et al. 2006).
Evaluation of growth potential has been determining by the bone
maturation. Growth processes are characterized with age by the bone size
enlargement, the bone mineral accrual and increase of the bone mineral density
(BMD) (the bone mass). Growth velocity in standing height is the most valid
representation of rate of overall bone growth. Regional segment lengths (such as
sitting height) and limb lengths are used as measures of bone length and growth
in the axial and appendicular skeletons. Bone growth in width has received
much less attention, even though it is of paramount importance for skeletal
development. It is well known that body weight is positively associated with
bone mass. During puberty, completion of skeletal growth is occurred and
accompanied by a marked peak height velocity and increase in skeletal mass.
Approximately half of maximal adult bone mass is accumulated. It is caused by
changes in both modeling and remodeling that occur simultaneously during this
period of life. In addition, there is some suggestion that both enhanced bone
formation and decreased bone resorption contribute to the increment in bone
density. Many cross-sectional studies reported data on bone growth in relation
to age and sex (Libanati et al. 1999; Du et al. 2003; Flores-Mir et al. 2004;
Scheplyagina and Moisseyeva 2005; Nyati et al. 2006; Wells 2007).
Bone growth and maturation
Skeleton is the permanent supportive framework of the body, yet it
grows in length and width while maintaining general shape throughout life.
Skeletal maturity is a good indicator of qualitative age changes in the body
because the process goes through the same stages among different individuals.
These characteristics of the changes in morphology and the fusion of epiphyses
8
with respective diaphyse are regarded as "physiological age" or "biological age"
(Tothill 1989; Gilli 1996; Flores-Mir et al. 2004). The skeleton is composed
mostly of bone tissue
IN HIGHER PRIMATES
TETRI WIDIYANI
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
STATEMENT LETTER
I hereby declare that dissertation entitled Studies on Growth Spurt and
Aging in Higher Primates is original result of my own research supervised by
supervisory committee and has never been submitted in any form at any
institution before. All information from other authors cited here are mentioned in
the text and listed in the reference at the end part of the dissertation.
Bogor, February 9th, 2012
Tetri Widiyani
Student ID G362070041
ABSTRACT
TETRI WIDIYANI. Studies on Growth Spurt and Aging in Higher Primates.
Supervised by BAMBANG SURYOBROTO, SRI BUDIARTI and ALEX
HARTANA
Growth is the best global indicator of children’s well-being. It is the
single measurement that best defines the health and nutritional status of
children, just as it provides an indirect measurement of the quality of life of an
entire population. The pattern of human growth reflects the biocultural
evolution of our species. The human pattern of growth and development
(ontogeny) appears to differ markedly from patterns of ontogeny in other
primate species. Three studies are reported here which deal to the growth and
development of human and chimpanzee (Pan troglodytes). These three studies
allow us to contrast the phenomena of adolescence growth spurt and female
elderly bone loss in chimpanzee and human as chimpanzee is the closest species
to humans within extant nonhuman primates. In the first, a cross-sectional study
of growth of the body size and somatotype of 363 Javanese girls and 299
Javanese boys aged 4 to 20 years from Magelang Regency, Indonesia was
described. In the second, cross-sectional and longitudinal studies in the growth
of chimpanzee second metacarpal bone linear dimensions from individuals aged
0 to 43.6 years were used for comparison. While in the third, cross-sectional and
longitudinal studies in the growth of chimpanzee body size (body mass and
anterior trunk length) and second metacarpal bone mineral content were
derived. In measuring the second metacarpal dimensions and mineral content, a
total of 568 radiographs of chimpanzee's proximodistal left hands were used.
They were taken from 68 females and 49 males aged 0 to 43.62 years old. We
applied an image analysis system, Scion Image Release Alpha 4.0.3.2 software
for Windows to measure bone linear dimensions and bone mineral content.
Humans present complex and sinuous growth curves for both body weight and
height. A clear growth spurt could be demonstrated by cross-sectional analysis
in our girl subjects at around aged 11.5 years and in our boy subjects at around
aged 12.5 years. In longitudinal series, not in cross-sectional, several
representative chimpanzees of both sexes showed a pre-adult growth spurt on
the body sizes, bone dimensions and bone mineral content. They ranged at age
4.5 to 8.5 years. This underscore the fact that adolescent growth spurt in linear
dimension was not a universal feature of anthropoid primate ontogeny. Bone
loss is a well established characteristic of human female aging. Based on crosssectional analyses the sequential decline of bone mass in female chimpanzee
may be said to be genuine. On the other hand, we found in adulthood through
elderly, male chimpanzees show a longer plateau than female chimpanzee, that
is, bone mineral content is maintained in male.
Keywords: growth, Javanese children, growth spurt, chimpanzee, second
metacarpal bone, bone loss
ii
ABSTRAK
TETRI WIDIYANI. Studi Lonjak Pertumbuhan dan Penuaan pada Primata
Tingkat Tinggi. Dibimbing oleh BAMBANG SURYOBROTO, SRI
BUDIARTI dan ALEX HARTANA
Pertumbuhan merupakan indikator terbaik untuk menggambarkan status
kesehatan dan gizi anak-anak serta kualitas hidup dalam suatu populasi
penduduk. Pola pertumbuhan manusia, mencerminkan evolusi biokultural
spesies manusia yang nampaknya berbeda dari spesies primata lainnya.
Simpanse (Pan troglodytes) digunakan dalam penelitian ini karena merupakan
spesies terdekat dengan manusia yang belum punah. Penelitian ini terdiri dari 3
bagian yang mengkaji pertumbuhan dan perkembangan manusia dan simpanse.
Bagian pertama merupakan studi cross-sectional untuk pertumbuhan ukuran
dimensi tubuh (bobot badan dan tinggi badan) serta somatotipe dari 363 anak
perempuan dan 299 anak laki-laki Jawa usia 4 sampai 20 tahun, di Kabupaten
Magelang, Indonesia. Bagian kedua adalah studi cross-sectional dan
longitudinal untuk pertumbuhan dimensi linear tulang metakarpal kedua
(panjang, lebar dan tebal korteks) pada simpanse. Bagian ketiga merupakan
studi cross-sectional dan longitudinal untuk pertumbuhan dimensi badan (massa
tubuh dan panjang badan anterior) serta kandungan mineral korteks tulang
metakarpal kedua pada simpanse. Pengukuran dimensi tulang dan kandungan
mineral korteks metakarpal kedua dilakukan secara radiografi pada 568 foto
radiograf tangan kiri dari 68 simpanse betina dan 49 simpanse jantan usia 0
sampai 43,6 tahun. Pengukuran tersebut dilakukan menggunakan software
pengolah gambar Scion Image Release Alpha 4.0.3.2. Rangkaian penelitian ini
memungkinkan untuk membandingkan fenomena lonjak pertumbuhan (growth
spurt) pada tahap remaja dan pengeroposan tulang (bone loss) pada wanita dan
simpanse betina di masa tua. Hasil penelitian ini menunjukkan bahwa manusia
mempunyai kurva pertumbuhan yang kompleks untuk ukuran bobot badan dan
tinggi badan. Lonjak pertumbuhan yang jelas (dibuktikan dengan analisis crosssectional) terjadi pada usia sekitar 11,5 tahun untuk anak perempuan dan sekitar
12,5 tahun untuk anak laki-laki. Pada simpanse, lonjak pertumbuhan tidak dapat
dilihat dengan studi cross-sectional, tetapi hanya dapat dilihat dengan
menggunakan studi longitudinal. Lonjak pertumbuhan ini terlihat pada semua
parameter yang diukur pada simpanse jantan dan betina usia 4,5 sampai 8,5
tahun. Beberapa simpanse betina mengalami bone loss, sejak usia 20 tahun.
Berbeda dengan manusia, simpanse tidak mengalami menopause yang
merupakan penanda penuaan. Simpanse jantan tidak menunjukkan fenomena
tersebut, kandungan mineral tulang tetap dipertahankan.
Kata kunci: pertumbuhan, anak-anak Jawa, lonjak pertumbuhan, simpanse,
tulang metacarpal kedua, bone loss
SUMMARY
TETRI WIDIYANI. Studies on Growth Spurt and Aging in Higher Primates.
Supervised by BAMBANG SURYOBROTO, SRI BUDIARTI and ALEX
HARTANA
Growth is the best global indicator of children’s well-being. It is the single
measurement that best defines the health and nutritional status of children, just as
it provides an indirect measurement of the quality of life of an entire population.
The pattern of human growth reflects the biocultural evolution of our species. The
human pattern of growth and development (ontogeny) appears to differ markedly
from patterns of ontogeny in other primate species. Humans present complex and
sinuous growth curves for both body mass and stature. Many bodily proportions
change dramatically during ontogeny as we reach sizes that are among the largest
of living primates. Perhaps most obviously, humans grow for a long time, with the
interval between birth and maturation exceeding that of all other primate species.
In human, growth is spurted to attain the genetically determined target size in
adult. Growth spurt of body size is a modular and highly evolvable feature of
ontogeny. Therefore the first and major interest in the evolution of growth and
development study is whether non-human primate species have an adolescent
growth spurt corresponding to that of human. Growth spurt could predict the
abnormal development which occurred during pre-adult phases.
Bone mineral loss is a well established characteristic of human aging. It is
found in all human populations. Thus, it is often considered to be a universal
aspect of human ontogeny, although women experience a greater decline in bone
mass during aging than men do. It is well-known that menopause had a major
effect to the evidence of bone loss in many older women. With demographic
shifting into older cohort in population pyramid, bone porosity raises medical
concern. Historically, some species of non-human primates were also generally
considered to exhibit age-related bone loss although they never had menopause.
Comparative investigation on age change of bone mineral content (BMC) in nonhuman primates is therefore necessary for the evolutionary consideration of
growth (ontogeny) and aging and to find suitable model to study bone loss.
In considering the evolution of biological characteristics of primates and
the interrelationships of species-specific life history, ecology, and life-style,
comparison of growth and development of several primates are essential.
Specifically, to understand the evolutionary characteristic of human life history
we investigate the growth pattern of the closest species to humans within extant
nonhuman primates, the chimpanzee (Pan troglodytes). Longitudinal and crosssectional data for body sizes (body mass (BM) and anterior trunk length (ATL)),
second metacarpal dimensions (bone length, bone width and cortical thickness)
and second metacarpal BMC (metacarpal cortical index (MCI) and cortical
density) were collected from chimpanzees belong to Primate Research Institute of
Kyoto University, Japan Monkey Center (Inuyama) and Kumamoto Primates
Research Park, Sanwa Kagaku Kenkyusho Co. Ltd. in Japan. Bone dimensions
and mineral content were measured from the radiographs of chimpanzee's
x
proximodistal left hands using an image analysis system, Scion Image Release Alpha
4.0.3.2 software.
We evaluated the growth pattern of Javanese population in updating data
for infants, children and adolescence cross-sectionally to overcome the cost and
the long time period required for a longitudinal study in human growth. We
selected children (aged 4 to 20 years) from Magelang Regency, Central Java
Province Indonesia. They were observed from the viewpoint of anthropometrical
characteristics. Body size of girls at the age of 4 years were 13 kg in body weight
and 100 cm in body height, while the boys’s were 15 kg in body weight and 100
cm in body height. Girls’s increased to 47 kg in body weight and 150 cm in body
height, while boys’s increased to 58 kg in body weight and 167 cm in body height
at the age of 20 years. They were shorter and lighter than reference children from
U.S., Japan, and Yogyakarta but they improved when compared with those of the
same ethnic of Bantul and with the different ethnic of rural India. A clear
adolescence growth spurt was demonstrated by cross-sectional analysis in body
weight and height of both sexes. They did not differ to the results on growth
velocity standards which were constructed longitudinally. Nevertheless velocity
peak of our children subjects was less than that of reference children which came
from well-off population. There was a clear age-related change in their
somatotype. At the age of 4 years, the physique of both sexes is found to be
mesomorph-endomorph (somatotype score 4-4-2 in girl or 3-4-2 in boy).
Thereafter it is transformed into ectomorphic-endomorph (4-2-3) in girls and to
mesomorph-ectomorph (1-3-5) in boys at the age of 20 years.
Chimpanzee exhibited an initial increase in bone dimensions and BMC
with age. Bone length and width accelerated for the first 8 years of age, whereas
cortical thickness accelerated longer until around 14 years of age. MCI increased
for first 6 to 7 years of age, whereas cortical density increased for a longer period
than MCI, until around 10 years of age. Sexual difference in bone length, cortical
thickness and BMC, which was greater in males than in females, has been
apparent significantly except in bone width which was unclear. Bone dimensions
maturated at about 13 years of age while BMC maturated at around age 10 to 12
years for MCI and 16 years for cortical density. During adulthood through aging,
bone length and width tended to plateau for both sexes. Cortical thickness in
female chimpanzees tended to decrease, but in males increasing instead. Crosssectional analyses of chimpanzee in body mass also showed a pre-adult growth
spurt but in ATL, three bone dimensions and BMC, the spurt could not be seen.
However, by longitudinal analyses all parameters showed spurts in several
chimpanzee individual of both sexes. It was found that there was a wide interindividual age variation in this growth spurts. During aging, the BMC of many
females declined but males’s continued its plateau phase or increase instead.
Some female chimpanzees even experienced bone loss earlier, approximately
since age 20 years.
Keywords: growth, Javanese children, anthropometric measurement, growth
spurt, cross-sectional study, longitudinal study, chimpanzee, second metacarpal
bone, radiography, aging, bone loss
xi
Copyright © 2012. Bogor Agricultural University.
All Rights Reserved
Prohibited to cite all or a part of this dissertation without referring to and
mentioning the source. Citation permits to the purposes of education, research,
scientific paper, report, or critism writing only; and it does not defame the name
and honor of Bogor Agricultural University.
Prohibited to republish and reproduce all or a part of this dissertation without
permission of Bogor Agricultural University.
STUDIES ON GROWTH SPURT AND AGING
IN HIGHER PRIMATES
TETRI WIDIYANI
Dissertation
submitted in partial fulfillment of the requirements for a Doctoral Degree in
Animal Bioscience Major of Graduate School of Bogor Agricultural University
GRADUATE SCHOOL
BOGOR AGRICULTURAL UNIVERSITY
BOGOR
2012
ii
Examiners in the Close examination:
1. Prof. Ir. Wasmen Manalu, Ph.D. (Professor of Faculty of Veterinery,
Bogor Agricultural University)
2. Dr. Astuti Lamid, M.CN. (Researcher of Center for Applied Health
Technology and Clinical Epidemiology, Research and Development
of Indonesian Health Ministry)
Examiners in the Open examination:
1. Prof. Yuzuru Hamada, D.Sci. (Professor of Primate Research
Institute, Kyoto University)
2. Prof. Dr. dr. Agus Purwadianto, S.H., M.Si., Sp.F (K). (Professor of
Faculty of Medicine, Indonesia University and Expert Staff of
Indonesian Health Ministry)
iii
Title
: Studies on Growth Spurt and Aging in Higher Primates
Name
: Tetri Widiyani
Student ID
: G362070041
Major
: Animal Biosciences
Endorsed by,
Supervisory Committee
Dr. Bambang Suryobroto
Chairman
Dr. dr. Sri Budiarti
M.Sc.
Member
Prof. Dr. Ir. Alex Hartana,
Member
Head of Animal Bioscience Major
Dean of Graduate School,
Dr. Bambang Suryobroto
M.Sc.Agr.
Dr. Ir. Dahrul Syah,
Examination date: January 17, 2012
Graduation date:
PREFACE
This dissertation is submitted in partial fulfillment of the requirements for
a Doctoral Degree for the author in Graduate School of Bogor Agricultural
University. It represents a culmination of work and learning that has taken place
over a period of almost five years (2007 – 2011). The work addresses three topics
related to the evolutionary of growth and development. Author had granted
Scholarship for Post-graduate Study (BPPS) during periods 2007 to 2010 and
Scholarship of Sandwich-Like Program in 2008 from the Indonesian Ministry of
Education, Directorate General of Higher Education (DIKTI). A portion of
dissertation (topic I) entitled The Growth of Body Size and Somatotype of
Javanese Children Aged 4 to 20 Year was published in Hayati Journal of
Biosciences Vol. 18 No. 4, December 2011.
This work could only be succeeded thanks to the invaluable contribution
of many people. First and foremost I am grateful for the generous support of my
supervisory chair, Dr. Bambang Suryobroto, who has been with me throughout
the years as mentor, editor and friend and introduced me to Professor Dr.Yuzuru
Hamada from Primate Research Institute Kyoto University. I am glad I could
work in Hamada’s laboratory to study the evolutionary growth and aging of
chimpanzee. It was a great learning experience doing collaboration research with
international researcher who is very competent in evolutionary morphology field.
I also extend special thanks to both co-adviser, Dr. dr. Sri Budiarti and Professor
Dr. Alex Hartana, who guided me through the process of developing confidence
as an academic.
I am very grateful to Rector of Sebelas Maret University for the
permission to pursue doctoral study in Graduate School of Bogor Agricultural
University. I am also grateful to the Government of Magelang Regency for the
permission of this study and to the school principals, teachers and all the children
subjects for all their support throughout the study in Magelang. Thanks to all staff
of Primate Research Institute Kyoto University Japan for their help and
permission throughout study there.
xviii
There are many other people without whom I would never have made it to
the end of a successful graduate career. Thanks to people at Zoo Corner ‘Z-Co’
(Kanthi A. Widayati, M.Si., E. Nunuz Rohmatullayaly, S.Si., Sarah Nila, S.Si.,
Islamul Hadi, M.Si., J.J. Elda Irma Kawulur, M.Si., Puji Rianti, M.Si., Gres
Maretta, M.Si., Indra, S.Si., Reny Kristianti Aryo, S.Si., Norita Widya Pangestika,
S.Si., Sekar Sukmaningrasa, M.Si., Yuliadi Zamroni, M.Si., Dr. Achmad
Farajallah, M.Si., Dr. Rika Raffiudin, Dr. Bambang Kiranadi, Mrs. Anik, Mrs.
Tini Wahyuni, Mr. Adi Surachman, Mr. Agus, and so on) for opportunities to
share thoughts and fun. Thanks to people at Pondok Putri Arum and Wisma Intan
for making me feel at home far away from home. In addition, thank you to friends
on Twitter and Facebook for making it less lonely during working at Inuyama
Japan and Bogor.
My highest expression of gratefulness is for my family. I thank my parents
(‘mamah’ dr. Kustiyah Marwi and ‘ibuk’ Tuti Sriani) for life and the strength and
determination to live it. My special thanks to my husband Eko Kurniawan and my
daughter Aulia Alifiani for the unconditional love and unfailing patience and
support. This dissertation is equally their achievement. Therefore, above all, I
thank God Allah SWT since this work would not be possible without His
almighty.
Bogor, February 2012
Tetri Widiyani
xix
CURRICULUM VITAE
The author was born in Surakarta, Central Java at December 24, 1971 by
Tuti Sriani. Author married with Eko Kurniawan, S.T. at August 10, 2002 and had
a daughter, Aulia Alifiani. Bachelor degree was earned from Department of
Zoology, Faculty of Biology, Gadjah Mada University in the beginning of 1998.
In the middle of 1998, she obtained DUE scholarship from the Indonesian
Ministry of Education, Directorate General of Higher Education (DIKTI) for
pursuing Master Degree at Graduate School of Gadjah Mada University on
Biology field and graduated at May 2001.
Since March 1, 2000 she has working as a lecturer at Department of
Biology, Faculty of Mathematics and Natural Science, Sebelas Maret University
Surakarta, Central Java. The main course which lectured is Animal Structure and
Development.
Other
courses
were
Animal
Eco-morphology,
Animal
Microtechnique, Teratology, and Experimental Anatomy. From the middle 2007
to the middle 2010, author got Scholarship for Graduate Study (BPPS) from the
Indonesian Ministry of Education, Directorate General of Higher Education
(DIKTI) for pursuing a Doctoral Degree at Graduate School of Bogor Agricultural
University on the Major of Animal Bioscience.
During November 2008 to February 2009, she did a collaboration research
with Primate Research Institute, Kyoto University Japan in the Sandwich-like
Program which funded by Indonesian Ministry of Education, Directorate General
of Higher Education (DIKTI). A paper entitled The Growth of Body Size and
Somatotype of Javanese Children Aged 4 to 20 Years which was a partial of
Doctorate theses of her was published in Hayati Journal of Biosciences Vol. 18
No. 4, December 2011. Author has a membership in Asia-Pacific Chemical,
Biological and Environmental Engineering Society (APCBEES).
xxi
CONTENTS
Page
CONTENTS.....................................................................................................XXI
LIST OF TABLES..........................................................................................xxiii
GENERAL INTRODUCTION.............................................................................1
Background.....................................................................................................1
Objectives and Benefits..................................................................................3
LITERATURE STUDIES....................................................................................5
Growth and Development...............................................................................5
Bone growth and maturation..........................................................................7
Radiography in bone aging assessment..........................................................9
Chimpanzee..................................................................................................14
THE GROWTH OF BODY SIZE AND SOMATOTYPE OF JAVANESE
CHILDREN AGE 4 TO 20 YEARS IN MAGELANG REGENCY..................19
Abstract.........................................................................................................19
Introduction...................................................................................................19
Materials and Methods.................................................................................21
Subjects ..................................................................................................21
Measurements ........................................................................................22
Data analysis...........................................................................................23
Result............................................................................................................24
Sociodemographic characteristic............................................................24
Body sizes...............................................................................................26
Somatotype.............................................................................................31
Discussion.....................................................................................................33
Conclusion....................................................................................................37
AGE-RELATED CHANGES OF SECOND METACARPAL LENGTH,
WIDTH AND CORTICAL THICKNESS IN CHIMPANZEES.......................39
Abstract.........................................................................................................39
Introduction...................................................................................................39
Materials and methods..................................................................................41
Result............................................................................................................45
Cross-sectional analysis on age-related changes of bone length and
width.......................................................................................................45
Cross-sectional analysis on age-related changes of cortical thickness...49
Longitudinal analysis on age-related changes of bone dimensions........51
Longitudinal analysis on growth velocity of bone dimensions .............57
Discussion.....................................................................................................65
Conclusion....................................................................................................67
AGE-RELATED CHANGES OF MINERAL CONTENT IN THE CORTICAL
BONE OF CHIMPANZEE’S SECOND METACARPAL................................69
Abstract.........................................................................................................69
Introduction...................................................................................................69
Materials and Methods.................................................................................72
Result............................................................................................................77
xxii
Cross-sectional analysis on age-related changes of metacarpal cortical
index.......................................................................................................77
Cross-sectional analysis on age-related changes of cortical density......80
Relationship between MCI, cortical density and body size....................82
Longitudinal age-related changes of MCI..............................................84
Longitudinal age-related changes of cortical density.............................89
Cross-sectional and longitudinal analysis on growth of body mass and
anterior trunk length ..............................................................................91
Discussion.....................................................................................................94
Conclusion..................................................................................................100
GENERAL DISCUSSION...............................................................................101
GENERAL CONCLUSION.............................................................................107
REFERENCES.................................................................................................109
xxiii
LIST OF TABLES
Page
TABLE 1 SOCIODEMOGRAPHIC CHARACTERISTIC OF CHILDREN
INCLUDED THE STUDY.............................................................26
TABLE 2 PREVALENCE OF UNDERWEIGHT, NORMAL, OVERWEIGHT,
AND OBESE ACCORDING TO BODY MASS INDEX (BMI)
PERCENTILES AND PREVALENCE OF UNDERFAT,
HEALTHY, OVERFAT, AND OBESE ACCORDING TO
PERCENTAGE OF BODY FAT (PBF) PERCENTILES AMONG
CHILDREN SUBJECTS LIVED IN MAGELANG REGENCY..30
TABLE 3 CHIMPANZEE SUBJECTS FOR THE STUDY.............................43
TABLE 4 NUMBER OF RADIOGRAPHS .....................................................44
TABLE 5 SUMMARY OF GROWTH SPURT IN THE SECOND
METACARPAL BONE LENGTH CHIMPANZEE ....................60
TABLE 6
SUMMARY OF GROWTH SPURT IN THE SECOND
METACARPAL BONE WIDTH OF CHIMPANZEE FROM
LONGITUDINAL DATA..............................................................61
TABLE 7 SUMMARY OF GROWTH SPURT IN THE SECOND
METACARPAL CORTICAL THICKNESS OF CHIMPANZEE
FROM LONGITUDINAL DATA.................................................61
TABLE 8 NUMBER OF RADIOGRAPHS ......................................................77
TABLE 9
SUMMARY OF THE SECOND METACARPAL CORTICAL
INDEX (MCI) GROWTH SPURT IN CHIMPANZEES FROM
THE LONGITUDINAL STUDY...................................................89
TABLE 10 SUMMARY OF THE BODY MASS (BM) GROWTH SPURT IN
CHIMPANZEES FROM THE LONGITUDINAL STUDY.........92
TABLE 11 SUMMARY OF THE ANTERIOR TRUNK LENGTH (ATL)
GROWTH SPURT IN CHIMPANZEES FROM THE
LONGITUDINAL STUDY............................................................93
TABLE 12 COMPARISON OF GROWTH SPURTS OF CHIMPANZEE IN
SEVERAL CHARACTERS ........................................................102
TABLE 13 COMPARISON OF BODY HEIGHT AND BODY WEIGHT
GROWTH SPURTS IN JAVANESE CHILDREN FROM THE
PRESENT STUDY WITH DIFFERENT ETHNIC GROUPS....104
xxiv
xxv
LIST OF FIGURES
Page
FIGURE 1 MEASUREMENTS MADE IN RADIOGRAMMETRY OF THE
METACARPAL...........................................................................11
FIGURE 2 DENSITOMETRIC PATTERN OF A CROSS-SECTIONAL MIDSHAFT BONE..............................................................................12
FIGURE 3 SCHEMATIC REPRESENTATION OF A STEP WEDGE AND
BELOW IT THE RADIOGRAPHIC IMAGE IT WOULD BE
EXPECTED TO PRODUCE (SYMMONS 2004). .....................13
FIGURE 4
MAP OF MAGELANG REGENCY IN CENTRAL JAVA
PROVINCE INDONESIA SHOWING THE STUDY SITES (▼).
.......................................................................................................22
FIGURE 5 GROWTH CHART OF BODY WEIGHT IN GIRLS (LEFT,
SOLID LINES) AND BOYS (CENTER, DASHED-LINES) AGE
4 TO 20 YEARS LIVED IN MAGELANG REGENCY.............27
FIGURE 6 GROWTH CHART OF BODY HEIGHT IN GIRLS (LEFT, SOLID
LINES) AND BOYS (CENTER, DASHED-LINES) AGE 4 TO
20 YEARS LIVED IN MAGELANG REGENCY......................28
FIGURE 7 GROWTH CHART OF BODY MASS INDEX IN GIRLS (LEFT,
SOLID LINES) AND BOYS (CENTER, DASHED-LINES) AGE
4 TO 20 YEARS LIVED IN MAGELANG REGENCY.............29
FIGURE 8 GROWTH CHART OF BODY FAT IN GIRLS (LEFT, SOLID
LINES) AND BOYS (CENTER, DASHED-LINES) AGE 4 TO
20 YEARS LIVED IN MAGELANG REGENCY......................30
FIGURE 9 THE 50TH PERCENTILE VALUES OF SOMATOTYPE
COMPONENTS SCORE IN CHILDREN AGE 4 TO 20 YEARS
LIVED IN MAGELANG REGENCY. ........................................32
FIGURE 10 SOMATOPLOT OF THE 50TH PERCENTILE SOMATOTYPE
SCORE (BOLD NUMBERS) OF GIRLS (LEFT) AND BOYS
(RIGHT) LIVED IN MAGELANG REGENCY BY AGE, 4 TO
20 YEARS. ..................................................................................32
FIGURE 11 CORRELATION OF ENDOMORPHY COMPONENT OF
SOMATOTYPE TO THE BODY MASS INDEX (BMI) AND
PERCENTAGE OF BODY FAT (PBF) IN GIRLS (○) AND
BOYS (×). ..................................................................................33
FIGURE 12 COMPARISON OF BODY HEIGHT (TOP) AND BODY
WEIGHT (BOTTOM) IN JAVANESE CHILDREN FROM THE
PRESENT STUDY WITH DIFFERENT ETHNIC GROUPS. . .35
xxvi
FIGURE 13 A RADIOGRAPH OF CHIMPANZEE LEFT HAND (A) WITH A
TRANSPARENT
RULER
TO
SCALE
LINEAR
MEASUREMENTS EXHIBITS THE POSITION OF SECOND
METACARPAL BONE................................................................42
FIGURE 14 AGE-RELATED CHANGE OF THE SECOND METACARPAL
LENGTH IN FEMALE (LEFT) AND MALE (CENTER)
CHIMPANZEES FROM THE CROSS-SECTIONAL STUDY..45
FIGURE 15 VELOCITY CURVES FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL LENGTH IN FEMALE AND
MALE CHIMPANZEES PREDICTED FROM THE 50TH
PERCENTILE OF THE CROSS-SECTIONAL AGE-CHANGE
CURVE. .......................................................................................46
FIGURE 16 AGE-RELATED CHANGE OF THE SECOND METACARPAL
WIDTH IN FEMALE (LEFT) AND MALE (CENTER)
CHIMPANZEES FROM THE CROSS-SECTIONAL STUDY..47
FIGURE 17 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL WIDTH IN FEMALE AND
MALE CHIMPANZEES PREDICTED FROM THE 50TH
PERCENTILE OF THE CROSS-SECTIONAL AGE-CHANGE
CURVE. .......................................................................................48
FIGURE 18 AGE-RELATED CHANGE OF THE RATIO BONE WIDTH TO
BONE LENGTH IN FEMALE (LEFT) AND MALE (CENTER)
SECOND METACARPAL CHIMPANZEES FROM THE
CROSS-SECTIONAL STUDY. ..................................................49
FIGURE 19 AGE-RELATED CHANGE OF THE CORTICAL THICKNESS
IN FEMALE (LEFT) AND MALE (CENTER) SECOND
METACARPAL CHIMPANZEES FROM THE CROSSSECTIONAL STUDY..................................................................50
FIGURE 20 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE CORTICAL THICKNESS SECOND METACARPAL IN
FEMALE AND MALE CHIMPANZEES PREDICTED FROM
THE 50TH PERCENTILE OF THE CROSS-SECTIONAL AGECHANGE CURVE.......................................................................50
FIGURE 21 CURVES OF AGE-RELATED CHANGE IN THE SECOND
METACARPAL BONE LENGTH FROM LONGITUDINAL
STUDY.........................................................................................52
FIGURE 22 CURVES OF AGE-RELATED CHANGE IN THE SECOND
METACARPAL BONE WIDTH FROM LONGITUDINAL
STUDY.........................................................................................55
FIGURE 23 CURVES OF AGE-RELATED CHANGE IN THE SECOND
METACARPAL
CORTICAL
THICKNESS
FROM
LONGITUDINAL STUDY..........................................................56
xxvii
FIGURE 24 VELOCITY CURVE OF THE SECOND METACARPAL BONE
LENGTH GROWTH OF MALE CHIMPANZEES FROM
LONGITUDINAL STUDY..........................................................59
FIGURE 25
VELOCITY CURVE OF THE SECOND METACARPAL
BONE WIDTH GROWTH OF FEMALE CHIMPANZEES
FROM LONGITUDINAL STUDY..............................................62
FIGURE 26
VELOCITY CURVE OF THE SECOND METACARPAL
CORTICAL
THICKNESS
GROWTH
OF
FEMALE
CHIMPANZEES FROM LONGITUDINAL STUDY.................64
FIGURE 27 PROCEDURE TO MEASURE CORTICAL DENSITY (NOT TO
SCALE). .......................................................................................75
FIGURE 28 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL INDEX (MCI) IN FEMALE (LEFT) AND MALE
(CENTER) CHIMPANZEES FROM THE CROSS-SECTIONAL
STUDY.........................................................................................78
FIGURE 29 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL INDEX (MCI) IN FEMALE AND MALE
CHIMPANZEES AGE 0 TO 18 YEARS DERIVED FROM THE
50TH PERCENTILE. ..................................................................79
FIGURE 30 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL INDEX (MCI) IN
FEMALE AND MALE CHIMPANZEES FROM THE CROSSSECTIONAL STUDY..................................................................80
FIGURE 31 CURVES OF AGE-CHANGE OF THE CORTICAL DENSITY IN
THE SECOND METACARPAL IN FEMALE (LEFT) AND
MALE (CENTER) CHIMPANZEES FROM THE CROSSSECTIONAL STUDY. ................................................................81
FIGURE 32 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL DENSITY IN FEMALE AND MALE
CHIMPANZEES AGE 0 TO 18 YEARS DERIVED FROM THE
50TH PERCENTILE. ..................................................................81
FIGURE 33 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL DENSITY IN
FEMALE AND MALE CHIMPANZEES FROM THE CROSSSECTIONAL STUDY..................................................................82
FIGURE 34 PLOTTING OF AGE AVERAGES OF METACARPAL
CORTICAL INDEX (MCI), CORTICAL DENSITY (CD),
ANTERIOR TRUNK LENGTH (ATL), AND BODY MASS
(BM) IN FEMALE (RED BLOCKED CIRCLES) AND MALE
CHIMPANZEES (BLACK BLOCKED CIRCLES) DURING
AGE 0 TO 12 YEARS (LEFT) AND AFTER AGE 12 YEARS
(RIGHT). ......................................................................................83
xxviii
FIGURE 35 AGE-RELATED CHANGE OF THE SECOND METACARPAL
CORTICAL INDEX OF CHIMPANZEE FROM THE
LONGITUDINAL STUDY WITH INCLUDING THE 25TH
AND 75TH PERCENTILE OF STANDARD CHARTS WHICH
HAD GOTTEN FROM THE CROSS SECTIONAL ANALYSES.
.......................................................................................................85
FIGURE 36 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL INDEX (MCI) IN
FEMALE CHIMPANZEES FROM THE LONGITUDINAL
STUDY.........................................................................................87
FIGURE 37 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
THE SECOND METACARPAL CORTICAL INDEX (MCI) IN
MALE CHIMPANZEES FROM THE LONGITUDINAL
STUDY.........................................................................................88
FIGURE 38 AGE-RELATED CHANGE OF MINERAL DENSITY IN THE
SECOND METACARPAL CORTEX OF CHIMPANZEE FROM
THE LONGITUDINAL STUDY WITH INCLUDING THE
25TH AND 75TH PERCENTILE OF STANDARD CHARTS
(DASHED LINE FOR FEMALE OR DOTTED LINE FOR
MALE) WHICH HAD GOTTEN FROM THE CROSS
SECTIONAL ANALYSES, N=NUMBER OF DATA,
F=FEMALE SUBJECT AND M=MALE SUBJECT..................90
FIGURE 39 VELOCITY CURVE FOR THE AGE-RELATED CHANGE OF
MINERAL DENSITY IN THE SECOND METACARPAL
CORTEX OF THREE REPRESENTATIVES CHIMPANZEE.. 91
FIGURE 40 VELOCITY CURVE FOR THE BODY MASS (A AND C) AND
ANTERIOR TRUNK LENGTH (B AND D) GROWTH FROM
THE CROSS-SECTIONAL STUDY (A AND B) AND
LONGITUDINAL STUDY (C AND D) IN FEMALE (F) AND
MALE (M) CHIMPANZEES.......................................................93
FIGURE 41 COMPARISON OF GROWTH VELOCITY OF BODY HEIGHT
AND BODY WEIGHT IN JAVANESE CHILDREN FROM THE
PRESENT STUDY (RED LINES) WITH JAVANESE
CHILDREN FROM THE LONGITUDINAL STUDY (BLUE
LINES) AND BELGIAN CHILDREN FROM THE
LONGITUDINAL STUDY (BLACK LINES)..........................103
LIST OF ABBREVIATIONS
ANOVA
analysis of variance
ATL
anterior trunk length
BM
body mass
BMC
bone mineral content
BMD
bone mineral density
BMI
body mass index
CT
cortical thickness
FM
fat mass
FFM
fat free mass
HSD
honest significant difference
HWR
height weight ratio
IDR
Indonesian Rupiah
MCI
metacarpal cortical index
NCHS
National Center for Health Statistics
NHES
National Health Examination Surveys
NHANES
National Health and Nutrition Examination
PBF
percentage of body fat
WHO
World Health Organization
GENERAL INTRODUCTION
Background
The pattern of human growth reflects the biocultural evolution of our
species (Bogin 1999). The human pattern of growth and development
(ontogeny) appears to differ markedly from patterns of ontogeny in other
primate species. Humans present complex and sinuous growth curves for both
body mass and stature. Many bodily proportions change dramatically during
ontogeny as we reach sizes that are among the largest of living primates.
Perhaps most obviously, humans grow for a long time, with the interval
between birth and maturation exceeding that of all other primate species (Leigh
2001). In considering the evolution of biological characteristics of primates and
the interrelationships of species-specific life history, ecology, and life-style,
comparison of growth and development of those primates are essential.
Specifically, to understand the evolutionary characteristic of human life history
we need knowledges of growth and development of the closest species to
humans within extant nonhuman primates, the chimpanzee (Pan troglodytes)
(Perelman et al. 2011). At present, the knowledge of growth and development
of chimpanzee is scarce because the population accessible for the study is small,
as chimpanzees are large animals with a long lifespan and growth period.
Growth can be studied in several ways. The two basic approaches are
cross-sectional and longitudinal studies. In a cross-sectional study, individuals
are usually measured or observed only once at their given age and the total
sample may then be categorized arbitrarily into different age cohorts to produce
age-related progress of body properties. Cross-sectional analyses are
economical because the study can be carried on in a short time period. A
longitudinal study, on the other hand, involves repeated observations on the
same individuals at specific intervals over a long period of time (Malina et al.
2004). It is more difficult to conduct longitudinal than cross-sectional study
because it needs patience and takes a long time to be completed. Therefore there
are more cross-sectional studies than longitudinal studies of child growth.
Nevertheless, Hamada and Udono (2002) stated that cross-sectional analysis is
2
not suitable for a fined-tuned and short-duration phenomenon such as the
growth spurt. The adolescent growth spurt in linear dimension was regarded as
unique to humans until it was also found to occur in non-human primates
(Tanner et al. 1990; Hamada et al. 1999). Nevertheless, although growth in
linear dimension is accelerated at chimpanzee puberty, the acceleration is not as
great as that in humans (Hamada and Udono 2002). It is vital to develop a way
of showing whether the chimpanzee has a real spurt or not, and of
discriminating a true spurt from acceleration due to ontogenetic plasticity.
The growth of children is important for the health of the new generation.
It most accurately reflects the health of a population (Onis and Blössner 2003)
and, in all its aspects, is of priority concern to the World Health Organization
(Onis et al. 2007). There are large between-population variation and it is now
clear that a portion of these differences is of genetic origin and a portion (in the
developing countries a large portion) is of environmental origin (Eveleth and
Tanner 1990; Ulijaszek 1993; Bogin 1999). Ulijaszek (2006) summarized
several known environmental factors that influence growth of children
postnatally. They include nutrition, infection, interactions between the two,
psychosocial stress, altitude, and climate. Most of these factors are conditioned
by socioeconomic status.
We evaluated the growth pattern of Javanese population in updating data
for infants, children and adolescence cross-sectionally to overcome the cost and
the long time period required for a longitudinal study in human growth. We
selected children (aged 4 to 20 years) from Magelang Regency, Central Java
Province
Indonesia.
They
were
observed
from
the
viewpoint
of
anthropometrical characteristics. We aim to show growth spurt of body size. A
longitudinal study in chimpanzee was used for a comparison. We analyzed the
growth pattern of body size and of the second metacarpal bone derived from a
longitudinal, repeated measurement of chimpanzee individuals aged 0 to 43.6
years. The longitudinal approach was expected to reveal growth spurt in this
species. The longer period covering older age in chimpanzee allowed us to
observe age-related changing in aging individuals. Human bone is characterized
by a gradual decrease in adulthood and a rapid loss of bone mineral content in
3
postmenopausal women (Schneider et al. 1997; Osei-Hyiaman et al. 1998;
Warming et al. 2002; Ahlborg et al. 2003; Finkelstein et al. 2008; Min et al.
2010). Menopause is not a typical characteristic of chimpanzee life histories
(Thompson et al. 2007; Lacreuse et al. 2008), so it is a point of interest to see
whether or not chimpanzee experience bone loss while aging.
Objectives and Benefits
Comparative studies on growth and aging of several primates are
important to understand the evolutionary characteristic of human life history
and to provide models and insights to efforts in increasing the quality of life.
Therefore the objectives of the study are:
1. a. To evaluate the growth of body size (height and weight) in the Javanese
children aged 4 to 20 years and to compare to that of several reference
populations.
b. To evaluate the growth of body shape (somatotype) in the Javanese
children aged 4 to 20 years.
2. a. To evaluate growth of body size (anterior trunk length and body mass) in
the chimpanzee aged 0 to 43.6 years
b. To evaluate the age-related changes of the mid shaft second metacarpal
dimensions (length, width and cortical thickness) for female and male
chimpanzee aged 0 to 43.6 years using radiographs.
c. To delineate the cross-sectional and longitudinal age-related changes in
the mineral content at the mid-shaft of the second metacarpal of
chimpanzee aged 0 to 43.6 years using radiographs.
3. a. To define whether the chimpanzee has a real growth spurt in its second
metacarpal dimensions and mineral content.
b. To define whether the chimpanzee experiences bone loss in aging.
LITERATURE STUDIES
Growth and Development
Growth of an individual is a dynamic process that is characterized by
physiological changes in infancy, childhood, and adolescence. These growth
periods relate to differences in various underlying genetic, hormonal and
nutritional factors and ultimately lead to differences in skeletal maturation and
development in an individual child. In a child who is physically and emotionally
healthy, and is adequately nourished, growth will proceed at a normal rate.
However, normal growth is not a uniform process and is dependent on the sex
and racial as well as ethnic background of the child. Environmental change is
also a determinant of later physiological and pathological events in growth
process (Gokhale and Kirschner 2003; Dominé et al. 2006).
Growth during infancy phase, up to the age of 2–3 years, is more rapid
than at any other time (Malina et al. 2004). It is a continuation of fetal growth.
In the neonatal phase, growth is dependent upon maternal, placental and fetal
factors (Godfrey et al. 1996). Maternal factors include maternal nutrition,
maternal size, infections and environmental exposure. Placental factors include
vascular abnormalities, placental hormones and hypoxia. Chromosomal
abnormalities or syndromes within the fetus itself also influence the fetal growth
(Resnik 2002).
The childhood phase begins around the preschool years and continues
until puberty. Many hormones, primarily growth hormone, influence skeletal
and somatic growth during this phase. Thyroxine, glucocorticoids, insulin,
oestrogens and androgens along with polypeptide growth factors also contribute
to growth. Therefore nutrition is an important component of this phase.
However, overfeeding during this phase has important implications, since it
may lead to childhood obesity and, subsequently, to obesity in adulthood, with
associated health risks (Cameron and Demerath 2002; Gokhale and Kirschner
2003).
Adolescence is the phase that begins with the onset of pubertal changes
and extends until growth and maturation are completed in adulthood. Puberty is
defined as the transient period between childhood and adulthood during which
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reproductive function is attained. During this period, the secondary sexual
characteristics appear, the adolescent growth spurt occurs, the gonads start to
produce mature gametes (sperm or oocytes) capable of fertilization, and major
psychological changes occur. It is generally considered that human puberty is
the result of two independent physiological processes, namely gonadarche and
adrenarche. Gonadarche refers to the activation of the ovary or testis at the end
of the prepubertal phase of development and leads to the dramatic increase in
gonadal steroid production and the completion of gametogenesis. The unfolding
of gonadarche is manifested by thelarche and menarche in girls, or by testicular
enlargement and virilization in boys. Adrenarche, on the other hand, refers to
the maturation of the adrenal cortex that leads to increased secretion of adrenal
androgens and is manifested by the appearance of sexual hair, a process termed
pubarche. It is interesting to note that adrenarche appears to be peculiar to man
and the Great Apes and the absence of adrenarche in humans do not appear to
prevent fertility or markedly to influence the timing and tempo of gonadarche.
The secretory products of the hypothalamic-pituitary-gonadal axis are the
primary modulators of the somatic changes that appear during puberty in higher
primates including man. Growth hormones are also necessary to realize the full
growth promoting effects of gonadal steroids (Terasawa and Fernandez 2001;
Garnett et al. 2004; Plant and Barker-Gibb 2004; Ebling 2005; Patton and Viner
2007).
Physical development reflects the overall patterns of growth and
morpho-functional maturation of a child. The linear dimensions of the body are
the essential indicators of physical development. The physical changes that
occur include growth acceleration and the changes in fat, muscle, and bone
mass. Anthropometry is used in characterizing growth and well-being not only
for individual assessments but also for reflecting the health status and social and
economic circumstances of populations throughout the life cycle. Actual height,
weight,
and
other
anthropometrics
dimension
including
skinfolds,
circumferences, and breadths serve useful purpose in assessing growth, body fat
distribution, and for provision of reference data. The World Health Organization
(WHO) provides a guidance on the appropriate use and interpretation of
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anthropometric indices. WHO adopts the reference growth charts of the
National Center for Health Statistics (NCHS) of US for international use. The
most commonly used anthropometric indexes for assessing child growth are
weight-for-height,
height-for-age,
weight-for-age,
and
mid-upper-arm
circumference. Whereas for adolescents are height-for-age, body mass index
(BMI)-for-age, and triceps and subscapular skinfold thicknesses-for-age (Onis
and Habitch 1996; Scheplyagina and Moisseyeva 2005; Borghi et al. 2006).
Evaluation of growth potential has been determining by the bone
maturation. Growth processes are characterized with age by the bone size
enlargement, the bone mineral accrual and increase of the bone mineral density
(BMD) (the bone mass). Growth velocity in standing height is the most valid
representation of rate of overall bone growth. Regional segment lengths (such as
sitting height) and limb lengths are used as measures of bone length and growth
in the axial and appendicular skeletons. Bone growth in width has received
much less attention, even though it is of paramount importance for skeletal
development. It is well known that body weight is positively associated with
bone mass. During puberty, completion of skeletal growth is occurred and
accompanied by a marked peak height velocity and increase in skeletal mass.
Approximately half of maximal adult bone mass is accumulated. It is caused by
changes in both modeling and remodeling that occur simultaneously during this
period of life. In addition, there is some suggestion that both enhanced bone
formation and decreased bone resorption contribute to the increment in bone
density. Many cross-sectional studies reported data on bone growth in relation
to age and sex (Libanati et al. 1999; Du et al. 2003; Flores-Mir et al. 2004;
Scheplyagina and Moisseyeva 2005; Nyati et al. 2006; Wells 2007).
Bone growth and maturation
Skeleton is the permanent supportive framework of the body, yet it
grows in length and width while maintaining general shape throughout life.
Skeletal maturity is a good indicator of qualitative age changes in the body
because the process goes through the same stages among different individuals.
These characteristics of the changes in morphology and the fusion of epiphyses
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with respective diaphyse are regarded as "physiological age" or "biological age"
(Tothill 1989; Gilli 1996; Flores-Mir et al. 2004). The skeleton is composed
mostly of bone tissue