comparative anatomy of the anterior cruciate ligament and its associated structures in primates

135 Pages·2017·21.94 MB·English

COMPARATIVE ANATOMY OF THE ANTERIOR CRUCIATE LIGAMENT AND ITS ASSOCIATED
STRUCTURES IN PRIMATES:
A STUDY OF BODY SIZE, BUNDLE NUMBER, AND BIPEDALITY

A dissertation submitted
to Kent State University in partial
fulfillment of the requirements for the
degree of Doctor of Philosophy

by

Aidan A. Ruth
November, 2016
© Copyright
All rights reserved
Except for previously published materials
Dissertation written by

Aidan A. Ruth

B.A., The Ohio State University, 2008

M.A., Kent State University, 2010

Ph.D., Kent State University, 2017

Approved by

___________________________________, Chair, Doctoral Dissertation Committee
Claude O. Lovejoy, Ph.D.

___________________________________, Members, Doctoral Dissertation Committee
Richard S. Meindl, Ph.D.

____________________________________
Mary Ann Raghanti, Ph.D.

____________________________________
Tobin L. Hieronymus, Ph.D.

____________________________________
Ellen L. Glickman, Ph.D.

Accepted by

____________________________________, Director, School of Biomedical Sciences
Ernest J. Freeman, Ph.D.

____________________________________, Dean, College of Arts and Sciences
James L. Blank, Ph.D
TABLE OF CONTENTS
TABLE OF CONTENTS ..................................................................................................................... iii
LIST OF FIGURES ............................................................................................................................ iv
LIST OF TABLES .............................................................................................................................. vi
ACKNOWLEDGEMENTS ................................................................................................................ vii
CHAPTER 1: OVERVIEW .................................................................................................................. 8
CHAPTER 2: COMPARATIVE ANATOMY OF THE ANTERIOR CRUCIATE LIGAMENT ................... 18
Introduction .............................................................................................................................. 18
Research Questions .................................................................................................................. 30
Materials and Methods ............................................................................................................ 32
Results ...................................................................................................................................... 36
Discussion ................................................................................................................................. 46
Conclusion ................................................................................................................................ 49
CHAPTER 3: COMPARATIVE ANATOMY OF THE ACL ENTHESIS .................................................... 52
Introduction .............................................................................................................................. 52
Research Aims .......................................................................................................................... 66
Materials and Methods ............................................................................................................ 67
Results ...................................................................................................................................... 69
Discussion ................................................................................................................................. 76
Conclusion ................................................................................................................................ 79
CHAPTER 4: The Lateral Meniscus ................................................................................................ 80
Introduction .............................................................................................................................. 80
Research Aims ......................................................................................................................... 87
Materials and Methods ............................................................................................................ 88
Results ...................................................................................................................................... 93
Discussion ............................................................................................................................... 100
Conclusion .............................................................................................................................. 101

CHAPTER 5: SUMMARY AND CONCLUSIONS .............................................................................. 103
APPENDIX A ................................................................................................................................ 105
APPENDIX B ................................................................................................................................ 107
APPENDIX C ................................................................................................................................ 109
APPENDIX D ................................................................................................................................ 110
APPENDIX E ................................................................................................................................ 113
REFERENCES ............................................................................................................................... 126

iii
List of Figures

1.1 External rotation of the knee upon extension ................................................................ 9
1.2 Anatomical position of the ACL within the knee joint .................................................... 11
1.3 Origin and insertion of the ACL ...................................................................................... 12

2.1 Origin and insertion of the double-bundle ACL .............................................................. 20
2.2 Origin and insertions of the triple-bundle ACL ............................................................... 21
2.3 Anatomy of the ACL in pigs ............................................................................................. 24
2.4 Postures of the hindlimb in different mammals ............................................................. 29
2.5 Lines representing a simple linear regression equation and a logarithmic regression
equation of Midsubstance circumference and body size. .................................................... 33
2.6 Relationship between body size and ACL circumference. .............................................. 37
2.7. Relationship between ACL quotient and Femoral Condyle Ratio .................................. 38
2.8. Gross anatomy of the ACL in a comparative sample of digitigrade mammals and palmigrade
mammals ............................................................................................................................. 40
2.9. Microscopic anatomy of the ACL .................................................................................. 41
2.10. Mean scores of Mardia’s Spherical Variance ............................................................... 43
2.11. Regression analysis of Mardia’s spherical variance onto Femoral Condyle Ratio. ...... 44
2.12. Overview (summary) images from quantitative polarized light microscopy ............... 45

3.1 Zones of Fibrocartilaginous Ligament attachment ......................................................... 55
3.2. Schematic of Joint formation ........................................................................................ 57
3.3. Schematic of Fibrous enthesis development ................................................................. 59
3.4. Schematic of fibrocartilaginous enthesis development ................................................ 60
3.5 Schematic representing the different pathways taken by fibrous and fibrocartilaginous
entheses ............................................................................................................................... 61
3.6 Illustration of Orthogonal Intercepts stereology ............................................................ 68
3.7. Comparative microanatomy of the femoral ACL insertion ............................................ 70
3.8 Sagittal sections from (a) Loris (b) Tamarin and (c) Diana monkey ................................ 73
3.9 Coronal view of the histological sections of the tibia in Deer, Bonobo, and Human ..... 73
3.10. Standard multiple linear regression analysis of femoral fibrocartilage thickness and tibial
fibrocartilage thickness on body weight .............................................................................. 75
3.11 ACL insertion site on dry bone ...................................................................................... 77

4.1 Diameter of femoral head vs. femoral length in hominoids .......................................... 90
4.2 Diameter of the femoral head vs. Body mass in hominoids ........................................... 91
4.3 Landmarks used in measurements of the femoral condyles .......................................... 92
4.4 Tibial Lateral Condyle/Femoral Head Diameter in Hominoids ....................................... 94
4.5. Comparison of tibial lateral condyle length divided by the cube root of body mass .... 95
4.6. Femoral Lateral Condyle/Femoral Head Diameter in Hominoids ................................. 97
4.7. Femoral Lateral Condyle/Cube root of Body Mass in hominoids .................................. 98
iv
4.8 External rotation of the tibia on the femur in hominoids .............................................. 99

v
List of Tables
Table 2.1 Comparison of linear and logarithmic regression models for ACL circumference and
body size. ............................................................................................................................. 33

Table 3.1 Enthesis types ....................................................................................................... 56

Table 4.1 Typical Lateral meniscus patterns found in primates ........................................... 86
Table 4.2 Atypical meniscus types found in humans ............................................................ 87
Table 4.3 Measurements used in analysis ............................................................................ 92
Table 4.4. Species and sex means for femoral and tibial lateral condyles divided by the cube
root of body mass in kgs ....................................................................................................... 96
Table 4.5 Length of the lateral tibial condyle and lateral femoral condyle divided by the femoral
head, and Femoral Condyle Ratio ........................................................................................ 100

vi
Acknowledgements

This dissertation could not have been completed without the help of many people. First
and foremost, Dr. Lovejoy and Dr. Raghanti have given me many opportunities throughout the
years, from access to lab space and consumables to pep talks and “go get ‘em!” Dr. Meindl’s
always been in my corner, and for that I am very thankful. Dr. Heironymus kindly offered time
on his lab equipment and shared with me his knowledge of ligaments and statistics. Dr.
Glickman graciously agreed to serve as my graduate representative.
Dr. Freddy Fu, Dr. Shiela Ingham, and Monica Linde graciously provided access to
specimens and significant funding for supplies, without which none of this research could have
taken place. Additionally, Dr. Shiela Ingham provided photographs of her beautiful gross
dissections and scientific expertise.
Dr. David Waugh offered guidance, technical support, and the opportunity to hold a
hummingbird and see phosphorescent squirrel bones. Dr. Jenny Marcinkiewicz opened her
laboratory to me so that I could use her tissue processor
Lyman Jellema and Dr. Yohannes Haille-Salaisie granted permission and assistance with
Osteological data collection at the Cleveland Museum of Natural History, while Bruce Patterson,
Anna Goldman, and Rebecca Banasiak granted access to the collections at the Field Museum of
Natural History.
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Chapter I: Overview
Rupture of the anterior cruciate ligament (ACL) is one of the most common knee injuries
in humans. As many as 350,000 ACL tears occur each year, and as many as 175,000 of those
tears result in ACL reconstruction surgery. Orthopedic surgeons have begun to perform
“anatomic” or “double-bundle” reconstructions of the ACL in an effort to restore its native
anatomy with higher fidelity. An assumption that is made in this effort is that the native
anatomy has been selected to perform in an “optimal” fashion and that restoring it will result in
a return to “optimal” kinematics. The present research is an analysis of the anatomy of the ACL
and its proximate structures (the ACL enthesis and the lateral meniscus) in an evolutionary and
comparative context with the goal of identifying differences in the ACL that may be the result of
selection for different types of locomotion.
The Knee Joint
While at first glance the knee joint appears to be a simple hinge, it is in reality a complex
joint that moves in six degrees of freedom: Anterior-posterior, medial-lateral, and cephalad-
caudad translations; and flexion-extension, internal-external, and varus-valgus rotations.
Anterior and posterior translations are coupled by internal and external rotation, and flexion
and extension are coupled by external and internal rotation of the tibia on the femur. The ACL
acts as the primary restraint to anterior translation of the tibia relative to the femur (i.e.,
prevents anterior "drawer" sign), while the posterior cruciate ligament (PCL) acts as the primary
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restraint to posterior translation of the tibia (posterior drawer sign). Additionally, the cruciate
ligaments guide the tibia along a pathway of external rotation during extension (Figure 1.1).
This conjoint axial rotation is often referred to in clinical literature as the “screw home”
mechanism (reviewed in Lovejoy, 2007). Bones, the menisci, and articular capsule structures act
as static stabilizers of the knee, and the hamstrings and quadriceps act as dynamic muscle
stabilizers (Fu et al., 1993; Lovejoy, 2007).

Figure 1.1 Upon extension, the knee rotates externally, guided by the cruciate ligaments.

The cruciate system has been described as a four bar linkage system: A closed-chain
linkage composed of four bars, or rigid links, and four connections among these links. Each
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cruciate ligament represents a bar, and the remaining two bars are an imaginary line
connecting the insertion points of the ACL and PCL on the femur, and one connecting the same
imaginary line on the tibia. The pivoting connections are the femoral and tibial insertions of the
ACL and PCL. The instant center of rotation lies at the overlap between ACL and PCL. During
flexion, the ligaments roll and glide past one another, and this overlapping point moves
posteriorly (Fu et al., 1993).
In humans, the tibial plateau is perpendicular to the long axis of the tibia and is
essentially a flat surface. In quadrupeds, the tibial plateau slopes downward anteriorly. Gravity
pulls the femur down this slope, a motion discussed in veterinary literature as “tibial thrust.”
The ACL (called the “cranial” cruciate ligament in veterinary literature) is reported to prevent
this tibial thrust. In dogs, a steeper tibial plateau is correlated with an increased risk of cranial
cruciate ligament rupture (Morris and Lipowitz, 2001).
The Anterior Cruciate Ligament
The ACL is one of four principal ligaments of the knee, together with the PCL and the
lateral and medial collateral ligaments. The cruciates are arranged in a “spiral” arrangement of
fibers, so that each fiber twists along its path from femur to tibia and is subsequently taut or lax
somewhat independently from the rest of the ligament to which it belongs.
The ACL originates along the medial side of the lateral condyle of the femur and inserts
just anterior to the intercondyloid eminence of the tibia (Figure 1.2 and 1.3). The anterior-most
fibers blend with those of the anterior horn of the medial meniscus and resist anterior
translation and medial rotation of the tibia against the femur (Reviewed in Arnoczky, 1983; MS
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