Facial Growth in the Rhesus Monkey: A Longitudinal Cephalometric Study

by Emet D. Schneiderman

Overview

For a wide spectrum of scientists from biomedical and dental researchers to primatologists and physical anthropologists, Emet Schneiderman offers the most accurate and up-to-date presentation of the normal growth of the lower facial skeleton in a primate species. His study is based on a sample of thirty-five captive rhesus monkeys, whose facial growth was traced over a ten-year period spanning from infancy to adulthood. The author identifies the relative contribution of various sites of growth, quantifies the relative roles of different types of development—such as appositional and condylar—and sheds light on several long-standing controversies as to how the primate face grows. Unlike many of the traditional cephalometric measurements, the ones included in this work were chosen to reflect the positional, dimensional, and localized remodeling changes that occur during ontogeny. Using a new statistical approach designed for longitudinal data, Schneiderman avoids the misleading information that has often resulted from older, cross-sectional statistical methods. This book serves as a foundation for future experimental and normal studies in the rhesus monkey and, from a methodological standpoint, as a general model for future longitudinal growth studies.

Originally published in 1992.

The Princeton Legacy Library uses the latest print-on-demand technology to again make available previously out-of-print books from the distinguished backlist of Princeton University Press. These editions preserve the original texts of these important books while presenting them in durable paperback and hardcover editions. The goal of the Princeton Legacy Library is to vastly increase access to the rich scholarly heritage found in the thousands of books published by Princeton University Press since its founding in 1905.

Product Details

ISBN-13:	9780691633893
Publisher:	Princeton University Press
Publication date:	04/19/2016
Series:	Princeton Legacy Library , #208
Pages:	232
Product dimensions:	6.10(w) x 9.30(h) x 1.10(d)

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Facial Growth in the Rhesus Monkey

A Longitudinal Cephalometric Study

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By Emet D. Schneiderman

PRINCETON UNIVERSITY PRESS

Copyright © 1992 Princeton University Press
All rights reserved.
ISBN: 978-0-691-08749-8

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CHAPTER 1

INTRODUCTION

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The rhesus monkey (Macaca mulatta) has been widely used for more than three decades as an experimental animal in the study of craniofacial growth. Despite its widespread use, adequate standards of normal craniofacial growth for the full range of chronological ages for this species are not available. This study seeks to alleviate this deficiency by applying statistically rigorous methods to a relatively large collection of longitudinal cephalometric radiographs of rhesus monkeys in order to provide a coherent description of the growth and maturation of the facial skeleton of this long-lived primate.

The specific purpose of this investigation is to describe dimensional and positional changes, as well as osseous remodeling, within the craniofacial complex of the rhesus monkey as they occur over the first ten years of life. To accomplish these ends, three major methodological problems had to be overcome: (1) a biologically sound approach had to be devised to quantify the morphological information contained in the serial radiographs; (2) a practical means of accurate age estimation was needed; (3) an informative and accurate longitudinal statistical model was required for representing the morphological changes as a function of time. Thus the development and application of these methods, in addition to the basic biological finding to which they lead, constitute major portions of this study.

SIGNIFICANCE

A basic quantitative description of normal facial growth in a nonspecialized higher primate species, based on long-term longitudinal records, will be useful to a wide variety of investigators, as no comparable information produced with appropriate methods is available for any primate species (Sirianni and Swindler 1979). Good estimates of dimensional variability in the skull of any primate species as a function of age are currently lacking. Besides the studies by McNamara and Graber (1975) on mandibular growth and by McNamara and coworkers (1976) on maxillary growth—both studies were limited because they provided standards using four gross developmental categories—plus a brief preliminary report on craniofacial growth in pigtailed macaques (Sirianni 1985), there are no good long-term longitudinal studies in which localized sites of growth and remodeling have been considered in nonhuman primates. The current concepts of craniofacial growth of the rhesus monkey are based largely on cross-sectional histological studies of dry skulls (Enlow 1966; Duterloo and Enlow 1970). To be of practical use, these concepts must be reevaluated and quantified by means of a thorough longitudinal investigation.

Standards of normal craniofacial growth consisting of good estimates of central tendency and variability are needed to interpret the numerous experimental studies that use the rhesus monkey as a primate model for human growth. Baseline data are sorely needed, in particular, to help make sense of experiments concerned with the effects of orthodontic and orthognathic surgical intervention in actively growing as well as non-growing monkeys (Smith and Minium 1983). Thus, a thorough understanding of normal growth is a prerequisite to the understanding of abnormal as well as therapeutically altered growth. Furthermore, approaches are needed for evaluating time-dependent phenomena (such as growth, treatment effects, and adaptation to surgery) that can be applied readily to any longitudinal data, whether from humans, monkeys, or from any other laboratory animals.

A comprehensive description should be useful to primatologists and paleontologists as well as to those investigators explicitly doing experimental studies on growth and adaptation in the rhesus monkey. This sort of information based on living primates could also aid in the interpretation of fossil primate material. For instance, it would be advantageous to have a sound quantitative basis for distinguishing the effects of variation due to age or sex differences from those due to taxonomic differences.

APPROACHES

Strategies for gaining biologically meaningful and objective information from lateral head X-ray films (cephalograms) have been elusive over the sixty-year history of radiographic cephalometry. By expanding on the implant techniques first pioneered by Björk (1955a, 1955b), we have been able to develop a satisfactory system for describing the remodeling and repositioning of the elements of the facial skeleton relative to one another and to the cranium. By using a computer-aided system, we can investigate local sites of growth as well as simple dimensional changes in the craniofacial complex. Without this in vivo bone-marking technique, an accurate longitudinal description of bone remodeling is impossible.

Aside from the problems associated with obtaining an appropriate sample with which to analyze normal longitudinal growth in the rhesus monkey, the statistical approaches for such an analysis have also been lacking, at least in application. Therefore, a major focus of this project was the development and application of appropriate statistical methods that account for intercorrelations among serial observations found within longitudinal data sets. Rao's polynomial growth curve-fitting approach (Rao 1959; Schneiderman and Kowalski 1985) and Hills' related approach (Hills 1968; Schneiderman and Kowalski 1989) were developed as suitable alternatives to the widely used but potentially very misleading least-squares methods in the analysis of longitudinal data. The recent accessibility of highspeed computing and powerful matrix algebra programming languages (SAS 1982a, 1982b, and GAUSS [Edlefsen and Jones 1985]) have made it possible to implement the most rigorous statistical methods available that until now, due to the computational complexity, have been applied only to trivial examples of data in textbooks.

In the process of developing biometric and statistical methods for characterizing craniofacial growth, it was necessary to develop procedures for estimating chronological age, since this information was unknown in many of the wild-caught animals used in this study. By devising a means for calculating reliable estimates of chronological age, it was possible to generate age-specific standards for the continuous range of ages from infancy through adulthood. Such an approach was required for documenting subtle short-term developmental changes in morphology. These refinements in technique have also made possible a number of insights into sexual dimorphism.

SCOPE OF PRESENTATION OF THIS STUDY

The digitized data set collected for this investigation consists of an enormous amount of morphological information on the craniofacial complex, including the entire facial skeleton, cranial base and vault, and dentition. The scope of this monograph is limited, however, to morphological change within the maxilla and mandible and their positional relationships to each other and the cranial base.

Since development of the radiographic cephalometric technique using implants was primarily a methodological concern, the presentation of this topic is confined to chapters 1 and 2. The age-estimation problem required resolution to address the other areas considered in this investigation, yet is an issue important in its own right. Also, a separate sample of rhesus monkeys was used for this part of the project. For these reasons, the age estimation problem is presented in a separate chapter (chapter 3), with its own background, results, and discussion sections.

This study has focused on growth in males since adequate long-term cephalometric data were available only for this sex. Thus, the detailed biostatistical descriptions of maxillary and mandibular growth in chapter 4 are based exclusively on the males. The more limited female sample was described in order to examine sexual dimorphism throughout growth. The statistics based on the small female sample must be viewed with caution since they were produced, out of necessity, with less rigorous methods. Therefore, the findings and discussions regarding sexual dimorphism must be viewed as tentative.

BACKGROUND

Numerous cross-sectional investigations have been conducted on ontogenetic variation in the skulls of higher primates since the 1860s (see review in Sirianni and Swindler 1979). Despite the availability of roentgenographic cephalometry since the 1930s, this powerful technique, which permits the longitudinal investigation of morphological change, was not applied to nonhuman primates until the 1950s.

Baume (1951a, 1951b, 1951c) presented radiographic, craniometric, and histologic findings on maxillary and mandibular growth, as well as various aspects of dental eruption in fortyone rhesus monkeys. The extent to which these investigations were truly longitudinal, as well as the precise manner in which these methods were applied to arrive at numerous conclusions, is not clear from these brief abstracts, which were apparently never published as articles. These factors make it impossible to assess the reliability of the various claims.

By using radiographic cephalometry in conjunction with radiopaque implants, Gans and Sarnat (1951) were able to describe short-term longitudinal growth at the zygomaticotemporal and zygomaticomaxillary sutures, as well as appositional growth on the zygomatic arch and zygomatic process of the frontal bone in eight infant/juvenile rhesus monkeys. Moore (1949) and Craven (1956) analyzed histologically the maxillary complexes of young rhesus monkeys stained vitally with alizarin dyes. These studies, in conjunction with that of Baume (1951a), identified the maxillary tuberosity as a major region of growth responsible for the forward displacement of the maxilla.

Erickson (1958) and Pihl (1959) investigated normal mandibular growth in three and two young rhesus monkeys, respectively, using radiographic cephalometry in conjunction with radiopaque implants. Both of these studies were unpublished master's theses and are therefore unavailable. Turpin (1968) reported on mandibular growth in two young rhesus monkeys using histological sections of specimens stained with tetracycline. Two of the animals used in this study also had radiopaque gold wire implants and therefore were also studied radiographically. Sites of mandibular remodeling were analyzed in three unaltered and four partially edentulated infant rhesus monkeys using similar methods by Michejda and Weinstein (1971). Kanouse and coworkers (1969) evaluated mandibular condylar growth (specifically, mitotic activity) in four rhesus monkeys of various ages using autoradiography.

Enlow (1966) described remodeling and displacement of the bones of the facial skeleton of the young rhesus monkey. Findings were based on ground sections prepared from the dry skulls of eleven monkeys. Duterloo and Enlow (1970) described remodeling and displacement of the cranial bones in similar study using fifteen dry monkey skulls. Although these papers present a reasonable picture of the growth and development of the entire skull of the rhesus monkey, it must be recognized that they are qualitative descriptions and are based solely on cross-sectional material. In these studies, the "growth history" of bones was reconstructed by examining the arrangement of layers of the various types of bone tissues (Enlow 1966). Although it is an informative means of investigating bone growth, this sort of analysis alone cannot provide truly normative data, as it has not been subjected to statistical treatment and may defy it. No objective measures of central tendency and variability were reported in these studies. Additionally, there was no serious consideration of how patterns of remodeling may change throughout the long period of active growth in the rhesus monkey.

The use of radiopaque implants in conjunction with radiographic cephalometry in the present study provides a suitable approach for rigorously evaluating Enlow's (1966) and Duterloo and Enlow's (1970) descriptions of craniofacial growth. The implants provide a means of quantifying the behavior of various sites of remodeling in the skull, as well as what these investigators have designated growth movements, that is, translations of the various components relative to one another.

Enlow and coworkers (1971) and Enlow (1982) have popularized the concept of compensatory remodeling and growth, that is, depository and resorptive activity occurs in specific regions of the craniofacial skeleton so as to maintain certain spatial relationships and consistencies of form of the various component bones. On the basis of the pattern of correlations found within a cross-sectional human data set, Solow (1966) has promoted the related concept of the dentoalveolar compensatory mechanism. Although they are intuitively sensible concepts, they require quantitative corroboration that can be provided by cephalometric analysis of serial radiographs using bone implants.

An additional problem with these studies is that they did not consider sexual dimorphism; the sex of the skulls used is not even mentioned. The present study does address differences in growth between the sexes.

Elgoyen and coworkers (1972) reported on changes within the maxilla and mandible of thirteen juvenile monkeys. McNamara (1972) extended observations on normal growth in the rhesus monkey to additional maturational groups including infants, adolescents, and adults. Data were available for animals in two 13-week study periods; twenty-eight of the monkeys were followed during the first of these periods, and sixteen were followed over the second. Both of these studies used cephalometric radiography with implants for recording morphological change.

McNamara and Graber (1975) provide a report specifically on the normal mandibular growth of rhesus monkeys. This study also used cephalometric radiography with implants. McNamara and coworkers (1976) reported on normal maxillary growth in rhesus monkeys in a related study, which also used a mixed-longitudinal design. In both these studies, means and standard deviations for each of four gross dental age categories (infant, juvenile, adolescent, and young adult) were presented. The present study, which reexamines many of the same monkeys, seeks to expand on these earlier reports by providing more rigorous measures of central tendency and variability for the continuous range of ages from infancy to adulthood.

The continuous distribution of observations in the present study provides insights into the sources of sexual dimorphism that could not be detected in earlier studies on craniofacial growth in rhesus monkeys because of the nature of the available samples (McNamara and Graber 1975, and McNamara et al. 1976). In these earlier studies, the female sample was lacking during the period in which sexual dimorphism was greatest. In addition, the method of combining all observations for each of the four developmental categories into four sets of means tended to collapse longitudinal variability.

Carlson and coworkers (1978) provided a detailed qualitative and quantitative histological study of normal mandibular condyle cartilage of rhesus monkeys at various maturational levels. In a radiographic cephalometric study using metallic muscle implants in addition to bone implants, Carlson (1983) described the normal growth and migration of the masseter muscle in relation to the associated craniofacial skeleton. These findings at the condyle and in the masseter are considered as they relate to the present longitudinal cephalometric findings regarding other sites of mandibular remodeling, as well as dimensional and positional changes (particularly rotational) of the mandible that occur during maturation.

(Continues...)

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Excerpted from Facial Growth in the Rhesus Monkey by Emet D. Schneiderman. Copyright © 1992 Princeton University Press. Excerpted by permission of PRINCETON UNIVERSITY PRESS.
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Table of Contents

List of Figures

List of Statistical Tables

Acknowledgments

1 Introduction 3

Significance 4

Approaches 5

Scope of Presentation of This Study 6

Background 7

2 Materials and Methods 19

Primate Samples 19

Radiographic Cephalometry 21

Cephalometric Measurements 40

Statistical Analysis 56

Format of Results 63

3 Age Estimation 65

Background 66

Approach 67

Findings 69

Comparison of Estimated and Actual Ages 71

Discussion and Conclusions 71

4 Results 75

Maxillary Growth and Remodeling in Males 75

Mandibular Growth and Remodeling in Males 91

Changes in the Occlusal Plane in Males 111

Coordination of Maxillomandibular Growth 114

Sexual Dimorphism 116

5 Discussion 121

Morphological Issues 121

Statistical Issues 137

6 Conclusions 143

Summary of Findings 143

Limitations of the Present Study 151

Captive versus Natural Populations 152

Comprehensive Analysis of Longitudinal Data Sets 154

Specific Areas for Future Research 155

App. A. Computer Software and Hardware 159

App. B. Age Prediction Equations 161

App. C. Statistical Tables 165

References 201

Author Index 209

Subject Index 211