The Bone-Body Fluid Continuum: Calcium and Phosphorus in the Skeleton and Blood of Extinct and Living Vertebrates

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THE BONE-BODY FLUID CONTINUUM: CALCIUM AND PHOSPHORUS IN THE SKELETON AND BLOOD OF EXTINCT AND LIVING VERTEBRATES MARSHALL R. URIST, M.D.* I. Introduction Bone, extracellular fluid, and blood arise in the embryo from primitive mesoderm and become parts ofan unhomogeneous but nevertheless continuous system. When bone appears in the embryo and calcium salts are deposited, the presence ofmineral in the body in die solid state engages in theregulation ofthe totalionaswellas dieindividualionconcentrations ofthe body fluid. While die composition ofextracellular fluid is regulated chiefly by die integument, gills, kidneys, and other organs (and to some extent by all the tissues ofdie body, hard as well as soft parts) bone tissue contributesspecificallyto thebodymechanismsforhomeostasis ofcalcium, sodium, hydronium, phosphate, carbonate, and odier ions. The observations to follow were made with the use ofclassic techniques ofphysiology in order to correlate structure and function. It will be demonstrated dut all vertebrates, from fish to man, that have bone tissue in the skeleton have a common basic chemical structure. Composition ofthe body fluids in die cartilaginous vertebrates that do not store mineral in the skeleton is characteristically and markedly diffèrent. These différences have been explained on die basis oflower levels offunction ofdie kidneys, gills (or lungs), and integument. Now it can be contended that the metabolic function ofskeleton determines much ofthe character ofbody fluids ofhigher vertebrates. There is aphysical-chemical equilibrium between tie * Department of Surgery, Division of Orthopedics, University of California Medical Center, Los Angeles, Los Angeles 24, California. These investigations were aided in part by grants from the U.S.P.H.S., N.I.H. (No. A-3793), Squibb Institute for Medical Research, Ayerst Laboratories, Inc., Southern California Chapter ofthe Arthritisand Rheumatism Foundation, the Easter Seal Foundation for Crippled Childrenand Adults, and by Contract NR 104-575 betweenthe officeofNaval Research, Department ofthe Navy, and the University ofCalifornia. 75 mineral deposits in die bone and die ions in solution in the fluids ofthe body which contributes to the various mechanisms of homeostasis of sodium, hydronium, carbonate, and odier ions. In addition, diere is a dynamic equilibrium governed by activity ofdie cells ofdie bone tissue; diis controlstheequilibriumbetweencalcium,phosphate, andother ionsinbone salt and body fluid. The physical-chemical equilibrium can be sustained by acellular bone, dentine, and enamel and is accomplished widiout specialized cells, remodeling, or turnover of tissue. The dynamic equilibrium, including the manifold physiologic body functions dependent upon it, is maintained by osteoblasts, osteocytes, and osteoclasts and requires a high level of cellular activity. New comparative biochemical studies will be presentedand a surveywillbe madeofskeletalhistophysiology, embryology , and paleontology to support the theory that the physiologic conditions necessary for a chemical existence independent of the external environment , including the mechanisms of homeostasis, were perfected in two stages as an integral part ofthe evolution ofbone. ?. Materials and Methods Skeletaltissues ofvarious species oflivingvertebratesinlarval, embryonic , and adult forms were sectioned undecalcified, examined by microradiologic methods, stained by Hotchkiss, hematoxylin-eosin-azure II, and die von Kossa stains as employed in previous communications [i]. Sea water was collected from the Pacific Ocean one mile offshore at Santa Monica, California. Fresh specimens of amphioxus (Branchiostoma lanceolatum) were caught onthe beachat high tide. Sixtyhagfish (Eptatretus strouti) trapped at 210 fathoms were exsanguinated by cannulating die ventral aortajust anterior to the ventricle, and die blood was pooled for analysis . Fifty elasmobranch fishes (30 Triakus semifasciata; 11 Platyrhinoidis tristeriata ; and 9 Heterodontus francisa) 35 to 45 cm. long, caught in the surf and brought to the laboratory in tanks of sea water were exsanguinated dirough the caudal artery. Blood was also collected from ten male bass (Paralabrax clathratus), twenty bullfrog tadpoles (Rana catesbiana), and four men and three women. Ultrafiltrates ofsea water and serums were prepared by the mediod ofToribara [2]. The major cations and anions were analyzed by methods listed in previous reports [3]. Urea was measured by the method of Henry and Chiamori [4]. 76 Marshall R. Urist · Bone-Body Fluid Continuum Perspectives in Biology and Medicine · Autumn 1962 Calcium ion concentration was measured by the murexide [5] or the frog heart [6] methods or both. A solution ofmurexide, 0.1 ml. of0.195 X io-3M was used in 2.0 ml. sample ofhuman serum; to allow forthehigher concentrations...

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