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© 1996 The Journal of Bone and Joint Surgery, Inc.
CorrespondenceTO THE EDITOR: Recently, The Journal of Bone and Joint Surgery published two interesting articles, "Current Concepts Review. Enhancement of Fracture-Healing" (77-A: 940-956, June 1995), by Einhorn, and "Instructional Course Lecture. Bone Biology. Part II: Formation, Form, Modeling, Remodeling, and Regulation of Cell Function" (77-A: 1276-1289, Aug. 1995), by Buckwalter et al. Surprisingly, both articles propagate the same erroneous idea—that is, that the pelvis is formed by membranous instead of endochondral ossification. In fact, the ossification and, later, the growth pattern of the pelvis is one of the most fascinating examples of endochondral ossification, especially in view of the appearance of multiple ossification centers, the enlargement of the acetabulum by means of the Y-shaped growth plate, the marginal epiphyseal plate along the iliac crest, and the bipolar growth cartilage in the inferior branch of the pubic bone. These features are worth remembering by anybody who works in the field of bone histophysiology and are important for the understanding of the numerous irregularities and malformations of the pelvis. In addition, there is a discussion about the possible difference in the regenerative potential of bone formed through membranous ossification compared with that of bone formed by endochondral ossification and about the suitability of bone grafts transplanted into the respective sites of the skeleton. Dr. Einhorn mentioned this problem on page 941 and referred to a recent article by Phillips and Rahn5. Unfortunately, both the protocol and the results of the study by Phillips and Rahn6 were presented incorrectly by Dr. Einhorn. The grafts were not taken from the iliac crest (as a representative of membranous ossification) and the tibia (as a representative of endochondral ossification) but from the calvaria (membranous ossification) and the fifth rib (endochondral ossification). Moreover, Dr. Einhorn stated that revascularization at two weeks was more advanced in the fixed specimens (compared with the non-fixed ones) from both the grafts formed by membranous ossification and those formed by endochondral ossification. Phillips and Rahn summarized their findings differently: "At 2 weeks, membranous bone demonstrated a greater area of graft revascularization if fixed than if the graft was not fixed. The opposite result was seen for endochondral grafts, where nonfixed grafts showed a greater area of revascularization than fixed grafts." However, Dr. Einhorn as well as Phillips and Rahn stated clearly that the differences found in incorporation of a graft are due more to structural and biomechanical conditions than to membranous or endochondral derivation. Since Dr. Einhorn and Dr. Buckwalter et al. are well recognized experts in the field of bone biology and fracture-healing, it would be interesting to know how they arrived at the statements regarding the development of the pelvis.
Prof. Dr. med. R. Schenk: Pathophysiologisches Institut der Universitat Bern, Murtenstrasse 35, 3010 Bern, Switzerland.
Dr. Eirhorn replies: Professor Schenk raises an important question relevant to the embryological development of the bones of the pelvis. My review of the anatomical and embryological literature, both in preparation for the writing of my Current Concepts Review and in preparation for my response to Professor Schenk, still leaves me unclear as to the development of these bones. I believe that Professor Schenk is correct in that some, if not all, of the pelvic bones develop by endochondral ossification and, in that sense, the information contained in my review stands corrected. However, even after consulting several embryology textbooks, I have found it difficult to find clear statements on the subject. Discussions that I have had with pathologists and anatomists suggest that, since there are centers of cartilage within the developing pelvis, endochondral ossification does take place in these bones. Moreover, orthopaedists who review radiographs of the pelvis in order to make determinations regarding skeletal maturity have described a phenomenon that is generally referred to as capping, a process whereby an epiphysis on the superior aspect of the ilium closes. Phillips and Rahn5 did evaluate the effects of fixation on the ability of grafts obtained from bones developed by membranous or endochondral ossification to stimulate revascularization at the site of implantation. However, they also evaluated the source of the bone graft in terms of its derivation from membranous or endochondral bone and the outcome of the bone-graft procedure. Therefore, my interpretation of this article remains valid. It is correct that the bone grafts in the study by Phillips and Rahn were obtained from the calvaria and the ribs, as opposed to the iliac crest and the proximal aspect of the tibia. I agree that the way that I stated this in my article seemed to be a misquotation. However, what I was attempting to do was to make the information more relevant for orthopaedic applications than for craniofacial applications. That is why I stated it as: "bone grafts that had been taken from portions of the skeleton that are formed by membranous ossification (for example, the iliac crest)." I probably should not have taken the liberty of making the statement in that way without more explanation. I thank Professor Schenk for his comments. I believe that this dialogue helps to clarify the information both for myself and for the readers.
Thomas A. Einhorn, M.D.: Department of Orthopaedics. The Mount Sinai Medical Center, Box 1188, New York. N.Y. 10029-6574.
Dr. Buckwalter, Dr. Glimcher, Dr. Cooper, and Dr. Recker reply: Our review of bone biology (Parts I2 and II) emphasized that, although authors frequently classify bone formation as occurring within cartilage (enchondral bone formation), within a non-cartilaginous organic matrix (intramembranous bone formation), or on the surface of existing bone (appositional bone formation), the available evidence indicates that the basic processes of bone formation and subsequent remodeling are the same in bone formed under the three conditions. (Some authors separate bone formation into enchondral ossification and intramembranous ossification—that is, ossification that occurs in the absence of definitive cartilage—and do not distinguish appositional bone formation from intramembranous ossification.) In the section dealing with formation of bone tissue in the second part of our review, we listed the formation of flat bones (such as the skull and pelvis) during embryonic development as an example of intramembranous bone formation. This statement was based on general discussions in some classic embryology and anatomy texts describing formation of flat bones by intramembranous ossification and formation of tubular bones and short bones primarily by enchondral ossification1,4. We have checked some of the available descriptions of embryonic bone formation cited in older anatomy and embryology texts and none of them documented formation of the flat central portion of the ilium by intramembranous ossification during embryonic development1,4, but they also did not state that the flat portion of the ilium initially forms by enchondral ossification. One source mentioned that the pelvic girdle first appears as a precartilage concentration of mesenchyme and that, later, cartilage miniatures represent all major parts of the limb girdles4. Another text, in describing the formation of the lower limbs, referred to the cartilaginous plate of the hip bone but then stated: "Retention of the membranous condition in the lower half of each primitive cartilagenous coxal plate accounts for the obturator membrane."1 Few detailed studies of the embryonic formation and ossification of specific human bones have been reported in the last four decades; however, a recent study3 supports the findings of older investigations in suggesting that some bones may develop from both intramembranous and enchondral ossification. The results of that study show that the clavicle forms by intramembranous ossification in the central region and by enchondral ossification at both ends3. The portion of the clavicle formed by intramembranous ossification contributes little to the subsequent growth of the bone3. A detailed study of the embryonic formation of the human ilium based on multiple specimens, similar to the work reported concerning the clavicle, could determine if the initial ossification of the central flat portion of the bone occurs in a mesenchymal condensation or in definitive cartilage. Professor Schenk indicated that the growth of the hip bone occurs by enchondral ossification. Our review articles on bone biology2 did not include a discussion of bone growth; however, Ponseti provided one of the best explanations of the growth of the human pelvis6. He clearly showed that the physes provide growth of the ilium in length while the periosteum provides growth in width. Thus, although there is some uncertainty concerning the embryonic formation of the flat portions of the human pelvis, the reported studies show that the human ilium grows by both enchondral (physeal) and periosteal (appositional) bone formation.
J. A. Buckwalter, M.D.; R. R. Cooper, M.D.: Orthopaedics Department, University of Iowa College of Medicine, 200 Hawkins Drive, Iowa City, Iowa 52246.
M. J. Glimcher, M.D.: Laboratory for the Study of Skeletal Disorders and Rehabilitation, Childrens' Hospital, Harvard Medical School, 300 Longwood Avenue, Boston, Massachusetts 02115.
R. Recker, M.D.: Creighton Osteoporosis Center, Creighton University School of Medicine, 600 North 30th Street, Omaha, Nebraska 68131.
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