J. Anat. (1996) 188, pp. 611-621, with 15 figures Printed in Great Britain 611 Blood supply to the human femoral diaphysis in youth and senescence

GEORGE BRIDGEMAN AND MURRAY BROOKES Division of Anatomy and Cell Biology, United Medical and Dental School, Guy's Hospital, London, UK

(Accepted 9 January 1996)

ABSTRACT The nutrient foramina in the human femoral diaphysis were counted in 109 cleaned and dried , ranging in age from 38 to 98 y. Although statistical analysis for univariate associations found that foramen number was not linked to age, sex (male/female) or side (R/L), multivariate logistic analysis revealed a significant interaction between the effects of sex and side (P < 0.01). Univariate analysis for sex and for side separately revealed a significant difference in foramen number between the results for men and women for R bones 62% (18/29) vs 33°% (8/24) (P < 0.04), but not for L bones 35°% (9/26) vs 48% (13/27) (P < 0.28). One lower limb from 15 cadavers was perfused with a barium sulphate suspension to show the blood supply of the femoral diaphysis. Twelve were in the age group 59-88 y and considered to be senescent material. In addition, 3 more femora were perfused, 1 from a young male aged 21 y, another from a 42-y-old male considered to show early senescent changes, and a third from a man aged 56 y with a hip prosthesis in situ, to provide an example of a cortex deprived entirely of its medulla. All perfused femora were fixed and decalcified, and sections were then radiographed. Cross-sections through the middiaphysis showed that aged cortex is supplied predominantly from the periosteum in contrast to the medullary supply in young human and animal material. The change is attributed to increasingly severe medullary ischaemia with age, brought on by atherosclerosis of the marrow vessels. An examination of the findings reported by investigators of animal bone blood supply in the past 40 y shows a large measure of agreement. Long standing controversy seems to be based on a failure to recognise that marrow ischaemia accompanies natural senescence, affecting transcortical haemodynamics, and entraining an increasing periosteal supply for bone survival in old age. The change over from a medullary to a periosteal blood supply to bone cortex is the consequence of medullary ischaemia and reduced marrow arterial pressure, brought about by medullary atherosclerosis.

Key words: Ageing; bone circulation; atherosclerosis.

innovatory method which reveals the functional INTRODUCTION circulation in vivo. The basic method of investigating the blood cir- Investigations on the vascular anatomy of long culation in a has for long depended on the bones tend to be confined to young rats, rabbits and intravascular perfusion of a marker substance in order dogs. Brookes & Harrison (1957), Gothman (1960), to detect and visualise the bulk layout of blood vessels Brookes (1971) and Rhinelander (1980) found that the in periosteum, cortex and marrow. The literature of bony diaphysis and its marrow are supplied with the past 40 years suggests that the preferred vascular blood in parallel from nutrient , and that markers are a radiopaque barium sulphate suspension cortical blood flow is centrifugal in direction; the (used in conjunction with microfocal radiography), latter is confirmed in small laboratory animals by the and India ink perfusion (used as an adjunct to physiological studies of Gunst (1980), Dillaman Spalteholz histology). The uptake of intravital dyes (1984), Montgomery et al. (1988) and Dillaman et al. and other water soluble markers is a more recent and (1991).

Correspondence to Mr George Bridgeman, Division of Anatomy (UMDS), Guy's Hospital, London Bridge, London SEI 9RT, UK. 612 G. Bridgeman and M. Brookes

De Bruyn et al. (1970) in rats, rabbits and guinea mitted to multivariate and univariate analysis using pigs, Trias & Fery (1979) in young dogs, and De the x2 statistic. Saint-Georges & Miller (1992) in rats, have reported findings contrary to the above. De Bruyn et al. (1970) regarded cortical as venous structures and Perfused bones assumed from the start that cortical blood flow is centripetal and also that the major blood supply to the Intravascular perfusion of one lower limb was is 'transosteal' from the periosteal and performed on 12 elderly cadavers in the age group cortical capillaries. Trias & Fery (1979) found it 59-88 y. In 1 cadaver the femoral, profunda and difficult to draw inferences on the direction of blood circumflex femoral arteries were displayed and painted flow in bone from their studies on bone vasculature. with acrylic paint to demonstrate the source of the De Saint-Georges & Miller (1992) were convinced blood supply to the femoral shaft. Three additional centripetalists. The above 3 groups of investigators, femora were perfused: 1, a young specimen from a however, all confirmed the anatomical continuity of youth aged 21 y who died from a stab wound to the the fine vessels of the periosteum, cortex and bone . In this instance, permission and access for marrow. On the other hand, Lopez-Curto et al. (1980) perfusion and bone sampling were gained from the found in dogs that the ' beds of marrow and police 3 d after death, when medullary necrosis had cortex are totally independent' and 'no arteriolar or begun. Another, from a 42-y-old man, provided an capillary anastomoses were observed linking these example of early senescence. A third additional femur separate beds'. However, these workers also found came from a 56-y-old man with a hip prosthesis that cortical venous drainage is centrifugal, and implanted into the bone 4 y previously, who illustrated periosteal and nutrient arteries supply the cortex. the effect of obliteration of the marrow cavity on the The contrary findings of these principal groups of blood supply to the cortex (Table 2). Four of this investigators are often explained away by an appeal to group of 15 femora were from females. interspecific differences in the small number of animal In practice, 5 1 of a 40 % suspension of barium species investigated. The effect of age on the blood sulphate (Micropaque) in water was prepared for each supply of bone is rarely mentioned. It is therefore the limb and heated to 40 'C. The hot perfusate was aim of this investigation to examine the nutrient pumped through the common iliac at 34 kPa arteries and blood supply to the diaphysis of the (5 psi) until the skin bled Micropaque on incision. ageing human femur. After overnight freezing, the skin was removed and the whole limb was placed on an 80 1 bath of 10% MATERIALS AND METHODS phosphate buffered formalin solution. After fixation (2-4 wk), the limb was put into an 80 1 bath of 5 % Driedfemora nitric acid in 5 % formalin solution in tap water. The nutrient foramina of 109 cleaned and dried Surrounding muscle was removed and the bones were femora in the bone collections of the Department of x-rayed, the specimens being returned to the acid Anatomy, Guy's Hospital, were examined, and rep- bath until all calcium was dissolved. When decalci- resentative specimens were photographed. There were fication was complete (4-6 wk), the femora were x- 14 pairs of female femora and 15 male pairs in the rayed whole, and then sectioned either transversely or collection (Table 1). The entire collection was sub- sagittally in 4 mm slices. These specimens were

Table 1. Summary data for 109 driedfemora (54 L, 55 R) with distribution ofpresence of 0, 1 or 2 nutrient foramina

Left femoral foramina Right femoral foramina Mean age Sex (y) None (0) Single (1) Double (2) None (0) Single (1) Double (2)

Female 82 0 13 14 1 8 16 Male 73 1 9 17 1 18 11 Subset of paired femora Female 81 0 8 6 0 4 10 Male 75.5 0 5 10 1 8 6 Female 14 pairs Male 15 pairs Blood supply to femoral diaphysis 613

Table 2. Age, sex and cause of death for 15 single femora siders men and women with unequal numbers of perfused with barium sulphate suspension foramina in their left (L) and right (R) femora. If there Case Age is no association between side and foramen number, no. (y) Sex Cause of death i.e. for every individual the probability for there being 2 foramina is the same on the L and R sides, then 1 21 M Stab wound to heart there is an expectation that half of the femora would 2 42 M Myocardial infarction 3 56 M Cardiac failure have 1 foramen on the L, and 2 on the R; and the 4 59 M Carcinoma of the bronchus other half would have 2 foramina on the L and 1 on 5 65 M Ventricular failure the R. The results for the separate female and male 6 72 F Myocardial infarction 7 72 M Cardiac failure groups were not statistically significant. It is noted 8 74 M Ischaemic heart disease that the available paired data numbers were small. 9 76 M Bronchopneumonia and Unequal foramen numbers in L and R femora were cerebrovascular accident present in only 9 men and 8 women, of the 29 original 10 77 M Chronic obstructive airways disease 11 81 F Myocardial infarction bone pairs. 12 82 M Bronchopneumonia The foramen numbers of all 109 dried bones, with 13 86 F Pneumonia sex and side, were therefore submitted to multivariate 14 86 M Myocardial infarction 15 88 F Congestive cardiac failure logistic analysis. This revealed a significant interaction (P < 0.01) between sex and side. The sex effect depended on side (R/L); the side effect depended on the sex of the bone. R and L sides only were then microradiographed using a Hilger and Watts micro- analysed to ensure uniqueness of data, thereby focal x-ray unit. avoiding double entries from same source individuals. Univariate analysis of 53 R male and female femora showed that in females, 8 had 1 nutrient foramen and RESULTS 16 had 2, while in males 18 had 1 foramen against 11 The dissected femoral and profunda femoris arteries with 2 (P < 0.04, Table 3). In 53 L male and female femora, there was no significant effect of sex on side are demonstrated in anterior and posterior view in with respect to foramen number (P < 0.32, Table 4). Figures 1 and 2. The lateral and medial circumflex The effect of side on foramen number was analysed femoral arteries (Fig. 1) arose from the profunda separately in the 2 sexes. Of 55 male bones, 18 had 1 femoris in this specimen, and were the major sources of blood supply to the femoral head and neck. The foramen on the R against 9 on the L, and 11 had 2 profunda femoris supplied the periosteum and the foramina on the R against 17 on the L (P < 0.04, muscles attached to the femur (Fig. 2). Table 5). These significant findings contrasted with similar data in 51 female femora where the results were not significant (P < 0.28, Table 6). Dried femora In summary, separate univariate analysis revealed a significant sex difference in foramen number between Of the entire collection of dried femora examined men and women for R bones (18/29 vs 8/24) but not without regard to sex or side, 2 diaphyseal nutrient for L bones (9/26 vs 13/27). Likewise, there was a foramina were present in 58 cases; in 48 cases only 1 significant side effect for men (18/29 on the R, vs 9/26 was found; in 3 cases nutrient foramina were absent. on the L), but not for women (8/24 on the R, vs 13/27 Femoral nutrient foramina point obliquely upwards on the L). to the femoral head. When 2 were present, they were not necessarily equal in size (Figs 3, 4). Either the upper (Fig. 4) or the lower foramen (Fig. 6) could be the smaller. Figure 5 is an example of a lone femoral Perfusedfemora nutrient foramen in the linea aspera. In the group of 15 aged and perfused cadaveric femora, x-rays show that 2 diaphyseal nutrient arteries may form an anastomotic loop in the medulla, Statistical analysis which then gives off ascending and descending Initially, the paired female and male dried bones were branches (Fig. 6). The anastomosis is not always there submitted to the McNemar test for independence of in which case the 2 nutrients go their separate ways side and foramen number. The McNemar test con- (Fig. 7). If one nutrient artery is predominant, it may 614 G. Bridgeman and M. Brookes Blood supply to femoral diaphysis 615 pass upwards into the marrow and divide into the and women had to be considered separately for major ascending and descending branches (Fig. 8). A statistical purposes. Likewise, when considering the single femoral nutrient artery and its division into association of foramen number and sex, the results for medullary branches is shown in Figure 9. R and L bones had to be analysed separately. It is Transverse sections of the perfused aged femoral surprising that univariate logistic analysis showed diaphysis, in men and women, show blood vessels on that, in males only, there is roughly a 2: 1 chance in the periosteal surface, supplying the underlying cortex favour of there being a single nutrient foramen in a R (Figs 10, 11). The marrow is ischaemic. It is apparent femur, and a 2: 1 chance in favour of 2 foramina in a that the periosteal blood supply to the femoral shaft is L femur. In R and L female bones, the chances of the dominant supply in the aged femur. there being 1 or 2 foramina are even. For control purposes, Figure 12 shows a transverse section of a femur taken from a 42-y-old man who may be classed as in early senescence. The marrow Diaphyseal nutrient arteries generally appears normal and a dominant medullary The femoral diaphyseal nutrients always point proxi- supply to the cortex is clearly present. Nevertheless, mally, because osteogenesis at the lower growth slight barium sulphate (arterial) traces penetrate the cartilage is faster than at the upper one in the femoral cortex and linea aspera centripetally from the peri- head (Lacroix, 1951). With 2 foramina, the arteries osteum. The femoral diaphysis of a 21-y-old male, 3 d may be equal in size, or one larger than the other. In postmortem, has a medullary arterial supply to the the latter case, the reduced nutrient artery may not cortex generally, except at the linea aspera, which have a companion . Angiography of our 15 shows periosteal arterial penetration (Fig. 13). perfused femora showed that a lone nutrient artery To demonstrate the importance of the periosteal branches up and down in the marrow. If there are 2 supply to ageing femoral cortex, Figure 14 shows a nutrient arteries, they may or may not anastomose in femur with a prosthetic steel stem impacted in acrylic the marrow as an arterial loop (Figs 6, 7). bone cement, obliterating the com- The extent to which the nutrient arteries contribute pletely. Angiography shows that the cortex is of to the total femoral flow is uncertain. Trueta (1968) normal thickness, and is supplied solely by periosteal surmised that 70 % of the total bone blood flow was arteries. Figure 15, a transverse section taken below carried by the nutrient arteries to the diaphyseal the stem, shows the marrow cavity filled solely with cortex and marrow. The cross-sectional area of acrylic cement. The marrow and its vessels have been arteries to the cancellous epiphyses is probably greater destroyed, but the cortex is healthy, sustained by a than that of a diaphyseal nutrient artery (Skawina et periosteal, arterial blood supply. al. 1994), in which case the nutrient vessels seemingly contribute a third or less of the total flow to the bone. DISCUSSION Kelly (1973), using hydrogen washout flow measure- ment in the canine , found that 71 % of the Statistical analysis nutrient flow went to the cortex and 30% to the First results suggested that there was roughly an even marrow. His dogs were of unstated age. Brookes chance of there being 1 (48 cases) or 2 (58 cases) (1971) supplied volumetric data in rat femora, from nutrient foramina in the linea aspera of the dried which it can be calculated that the marrow accounts human femur. Multivariate analysis, however, indi- for 90 % of the diaphyseal blood volume in 24-month- cated a significant interaction between sex and side, old rats, and the cortex 10%. Similarly, M. Okubo meaning that the number of diaphyseal foramina (personal communication, 1977), using microspheres varies between men and women, and the effect of an for blood flow measurement in mature dogs, found individual's sex on the foramen number varies with that 88 % of the femoral diaphyseal flow went to the side. Hence the observed foramen numbers for men marrow and 12 % to the cortex. These results conform

Fig. 1. The femoral (f), profunda femoris (p), lateral (1) and medial (m) circumflex femoral arteries dissected and painted in a cadaver aged 72 y. Anterior view. Natural size. Fig. 2. Posterior view of specimen in Figure 1, showing dissected and painted femoral (f) and profunda femoris (p) arteries. One fourth natural size. Fig. 3. Two femoral nutrient foramina of similar size on the linea aspera. Natural size. Fig. 4. Two femoral nutrient foramina; the upper is smaller. Natural size. Fig. 5. A lone femoral nutrient foramen on the linea aspera. Natural size. 616 G. Bridgeman and M. Brookes

Fig. 6. Angiogram ofa perfused femur from an elderly cadaver, showing 2 diaphyseal nutrient arteries linked by a prominent loop. The lower artery is very much reduced in calibre. Natural size. Blood supply to femoral diaphysis 617

Table 3. Effect of sex on foramen number in right femora* arterial supply to the canine tibia was negligible. Johnson (1927), often misquoted, failed to stain dog Sex 1 foramen 2 foramina Totals diaphyseal cortex with India ink, injected solely Female 8 (33%) 16 (67 %) 24 through the periosteal system, and therefore chose to Male 18 (62%) 11 (38%) 29 neglect it. Using barium sulphate perfusion and Both sexes 26 27 53 microangiography, Brookes & Harrison (1957, rab- bit), and Brookes (1958a, rat; 1958b, 1963, human * = P Statistically significant difference: x2 4.339, < 0.04. fetus; 1986, dog) showed that diaphyseal nutrient arteries give off which join the cortical Table 4. Effect of sex on foramen number in left femora* capillaries and also the marrow sinusoids, i.e. the 2 arterial supplies to bone marrow and to cortex are in Sex 1 foramen 2 foramina Totals parallel. In addition, there are 2 types of Female 13 (48%) 14 (52%) 27 in young bone cortex, arterioles from the marrow and Male 9 (35%) 17 (65%) 26 cortical capillaries. Furthermore, periosteal capillaries Both sexes 22 31 53 freely communicate with cortical capillaries, and they in turn with the sinusoids of bone marrow, in young * P Nonsignificant: X2 = 0.999, = 0.32. material. The above results have recently been confirmed by Skawina et al. (1994) by means of Table 5. Effect of side in male femora* microvascular corrosion casts, who found that 'the medullary arteries supplied both bone cortex and Side 1 foramen 2 foramina Totals marrow', and 'there was no arterial supply to the Right 18 (62%) 11 (38%) 29 [fetal] shaft cortex from the periosteal side'. Left 9 (35%) 17 (65%) 26 De Bruyn et al. (1970) in a study wholly employing Both sexes 27 28 55 India ink believed that nutrient artery blood normally feeds into the cortical capillaries, but then exits into * = Statistically significant difference: XI 4.134, P < 0.04. the marrow sinusoids. Trias & Fery (1979) concluded in their adult mongrel dogs that 'The direction of Table 6. Effect of side in female femora* arterial blood flow ... is predominantly centrifugal while the venous drainage is centripetal'. Their finding Side 1 foramen 2 foramina Totals that 'in an Haversian canal there is usually only one Right 8 (33%) 16 (67%) 24 vessel, and this has the structure of a capillary', Left 13 (48%) 14 (52%) 27 suggests their dogs were young (Brookes & Harrison, Both sides 21 30 51 1957). De Saint-Georges & Miller (1992) injected India ink into 3-month-old rats. They reported that * x2 = = Nonsignificant: 1.15 1, P 0.28. 'most of the vascular flow appears to be centripetally through the diaphyseal cortex, and this appears to be with the mathematical concept F = kV, where the primary blood supply for the adjacent bone F = blood flow rate, V = unit volume, and k = a marrow'. The authors stated that most of their results constant. are based on inadequately filled preparations. One fully filled specimen (their fig. 2), shows the cortical vessels, sparse relative to the marrow sinusoids, Blood supply to young bone passing obliquely to the external surface, and mani- The in vivo injected India ink studies of Drinker et al. festly bifurcating towards the periosteal surface, (1922) found that ink did not penetrate from the becoming thinner as they go. In any other tissue, such periosteum into the underlying cortex, and thereby a vascular layout would coincide with a blood current justified their isolated canine tibia model for venous from stem vessel to branches, from thicker to thinner, collection flow studies. In their view a periosteal and here in bone cortex, from within outwards.

Fig. 7. Angiogram as in Figure 6, showing absence of medullary loop to link 2 diaphyseal nutrient arteries of equal calibre. Natural size. Fig. 8. Angiogram showing a dominant inferior nutrient artery providing the ascending and descending medullary arteries. The latter branches partly supply the cortex in this aged cadaveric femur. x 3. Fig. 9. Angiogram as in Figure 6, showing a single nutrient artery dividing in the into ascending and descending medullary arteries. x 2. 618 G. Bridgeman and M. Brookes

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1 0 1 1 Fig. 10. Angiogram of transverse section of a femur from individual aged 65 y (linea aspera, below), showing a dominant periosteal arterial supply to the cortex. The barium traces represent arterioles. The marrow is ischaemic. x 4. Fig. 11. Angiogram as in Figure 10, femur from individual aged 72 y. The marrow is ischaemic. The cortex is supplied almost wholly from the periosteum. x 2.5.

However, centrifugal blood flow in the cortex of supplied.the canine marrow and cortex in parallel, in young long bones has also been demonstrated after the 6 adult dogs of unstated age that they examined; the injection of intravital dyes in the living human but for them, cortical and medullary vascular beds femoral cortex during amputation (Lamas et al. 1946; were largely independent. Transcortical periosteo- Evans Blue), and in the rabbit (Gunst, 1980; medullary anastomoses were also noted in their Disulphine Blue). In young rats, Dillaman (1984) has material. It is possible that their use of Microfil, a shown a transcortical passage of ferritin from marrow silicone elastomer, capable of filling the total vascu- to periosteum. The passage of horseradish peroxidase lature of a tissue, failed for technical reasons to has been similarly tracked suggesting that not only is demonstrate the continuity between sinusoid and the blood flow centrifugal in young material, but also capillary at the osteomyeloid junction. The possibility the movement of bone water across the entire cortex must also be considered that the bone marrow was (Montgomery et al. 1988; Dillaman et al. 1989). ischaemic on account of the age of the dogs. Arterial periosteomedullary anastomoses, demon- strated the use of the more Bloodflow in old bone by viscous Micropaque, were illustrated as a feature of 25 aged human tibiae Both Crock (1967) and Trueta (1968) illustrated a aged 59-80 y, average 70 y, amputated for senile periosteal supply to human bone cortex, significantly atherosclerosis (Brookes, 1960a). A periosteal arterial in aged specimens of the 7th decade. Nelson et al. supply to bone cortex was also prominent in this (1960) examined 14 human tibiae amputated for material, and contrasted with its absence in a perfused femoral cancers. Regrettably the age range of this tibia of a 15-y-old youth (leg amputated for femoral material, presumably old, was not supplied, but they sarcoma), which acted as a control. Vascular canals in did describe a periosteal arterial supply to the tibia, the bone cortex of these aged specimens were irregular with multiple blood vessels in cortical canals, and in size and contained a variable number of blood periosteomedullary anastomoses. An osteoporotic vessels. The above features and medullary ischaemia cortex and ischaemic bone marrow also illustrate their were taken to reflect the ageing process in long bones. text without comment. Lopez-Curto et al. (1980) This view was strengthened (Brookes, 1960b) by the pointed out that the diaphyseal nutrient arteries demonstration in rabbits that unilateral ligation of the Blood supply to femoral diaphysis 619

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1 4 _ Fig. 12. Angiogram as in Figure 10, femur from individual aged 42 y. The medullary arteries are robust, and supply the cortex entirely, except in the R posterior quadrant where periosteal arterial traces are detectable. x 3. Fig. 13. Angiogram as in Figure 10, femur from individual aged 21 y (see text). Central necrosis of the marrow is present, but the peripheral arteries are numerous and robust. They supply the entire cortex, except in the region of the linea aspera. x 3. 620 G. Bridgeman and M. Brookes nutrient artery of the femur provokes an abnormal women than in men, and is usually accounted for by centripetal blood flow into the compact bone from the hormonal and mineral imbalances. It is possible that vessels in the periosteum and attached vastus inter- bone vascular change in senescence supplies an medius. This contrasts with the normal medullary aetiological background of reduced bone blood pH blood supply and centrifugal vascular penetration of and disturbed P02 and PCO2 (Brookes, 1971; Arnett the cortex in the contralateral controls. Histologically, & Dempster, 1990; Arnett et al. 1994) against which enlarged Haversian spaces in the ischaemic cortex hormonal, nutritional and cellular factors operate in contained multiple blood vessels. this disorder. Brookes (1973) showed that the circulating blood Bone marrow biopsy and its histomorphology volume in rat bone declines semilogarithmically with might be added to aortic radiography and retino- age from 1 month to 24 months, when the blood scopy, to make a quantitative overall assessment of volume reaches the value of one tenth of what it was the degree of atherosclerosis in the vascular system. in youth. More recently, Kita et al. (1987) in rabbits, Marrow biopsy might also provide a predictive using hydrogen washout for blood flow measurement, element with respect to other arterial territories demonstrated a falling blood flow in bone marrow of (Ramseier, 1962). 50, 23, 15 and 12 ml/min/100 g in immature, mature, Our results are also relevant to fracture treatment. middle aged and advanced aged rabbits, respectively. Our findings of a combined periosteal and medullary blood supply to bone cortex in senescent bones, in contrast to a purely medullary supply in youth, help Clinical considerations to explain the success of intramedullary reaming and Medullary ischaemia in human long bones is not rare. nailing of long bone fractures, particularly in the Ramseier (1962) in more than 200 consecutive weight-bearing femur and tibia (Gahr et al. 1995). In postmortem examinations assessed histologically the old and young fractured bones the periosteum is grades of atherosclerosis in intraosseous, muscular, conserved, thus keeping the cortex alive while the coronary and cerebral arteries. He found that human marrow regenerates. At the same time, the intra- bone marrow is generally subject to arterial disease, medullary nail maintains the bone fragments in and that grade for grade, atherosclerotic disease mechanical reduction in a maximally advantageous appears at least 10 years earlier in femoral marrow site, the medullary axis. Medullary reaming in sheep is than in the arteries of the brain, heart or thigh known to provoke a 6-fold increase in the blood muscles. Ramseier's findings and those of Brookes supply to the periosteum (Reichert et al. 1994). In (1960a, b; 1990), Nelson et al. (1960), Crock (1967), rabbits, reaming of the marrow cavity followed by Trueta (1968), Lopez-Curto et al. (1980) and Kita et intramedullary nailing has been shown to promote an al. (1987), suggest that ageing in long bones is abundant callus deposition from the periosteum, accompanied by marrow ischaemia. essential for the rapid establishment of firm bony With the known increasing severity of athero- union (Brueton & Brookes, 1995). sclerosis in bone marrow, it is also likely that the normal high diaphyseal pressures in youthful bone marrow fall below those at the arterial end of the CONCLUSION periosteal capillaries. This haemodynamic pressure The results of this investigation suggest that a change accounts for a centripetal blood flow from the periosteal arterial supply to bone cortex is a clamant periosteum into the senescent cortex. With the feature of the senescent human femur. In contrast, a development of a combined, yet directionally con- periosteal supply to youthful bone cortex is absent in trary, dual blood supply to the cortex, the evidence young laboratory animals, the human fetus and rare also suggests that the amount of circulating blood, youthful human femora. The femoral diaphysis of a and its speed, in the cortex also fall (Brookes, 1973; 21-y-old male showed medullary arteries supplying Kita et al. 1987). This may be related to the the cortex, except for the linea aspera which has a osteoporosis of age. The prevalence of this, the periosteal supply, a normal feature of apophyses in commonest metabolic bone disease, is much greater in general (Rhinelander, 1980). In the 42-y-old male

Fig. 14. Angiogram in longitudinal section showing the stem of a hip prosthesis held in a femoral diaphysis by acrylic cement; cadaver aged 56 y. The cortex is entirely vascularised from the periosteal vascular network. x 2. Fig. 15. Angiogram of transverse section of the femur below the prosthetic stem shown in Figure 14. The marrow cavity is blocked with acrylic cement. The entire cortex is vascularised from the periosteum. x 4. Blood supply to femoral diaphysis 621

(Fig. 12), a periosteal supply to the cortex is just in DE SAINT-GEORGES L, MILLER SC (1992) The of evidence, adjuvant to a medullary supply. The aged bone and marrow in the diaphysis of the rat hemopoietic long bones. Anatomical Record 233, 169-177. specimens all show a prominent periosteal supply and DILLAMAN RM (1984) Movement of ferritin in the 2-day-old chick a reduced medullary supply. The 56-y-old male femur femur. Anatomical Record 209, 445-543. with a hip prosthesis (Fig. 14) demonstrated that the DILLAMAN RM, ROER RD, GAY DM (1991) Fluid movement in bone: theoretical and empirical. Journal of Biomechanics 24, periosteal circulation is adequate to supply the full Suppl. 1, 163-177. thickness of the cortex with arterial blood, in spite of DRINKER CK, DRINKER KR, LUND CC (1992) Circulation in the the marrow cavity being obliterated by acrylic cement mammalian bone marrow. American Journal of Physiology 62, 1-92. and stainless steel. 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