Bone demineralization induced by cementless alumina-coated femoral stems

The Journal

Bone Demineralization Alumina-coated

of Arthroplasty

Vol. 9 No. 4 1994

Induced by Cementless Femoral Stems

A. Toni, MD,* C. G. Lewis, MD,t A. Sudanese, MD,* S. Stea, BSc,+ F. Calista, BSc,* L. Savarino, BSc,+ A. Pizzoferrato, MD, PhD,+ and A. Giunti, MD*

Abstract: The biologic compatibility of ceramic materials hasbeen widely demonstrated, and alumina (A1203) has been used extensively in clinical applications for nearly 20 years. The authors examined the behavior of bone tissueadjacent to the alumina coating in eight cementlesship prosthetic stemsthat appearedradiologically stableand were explanted becauseof pain. Histologic evaluation demonstratedthe presenceof a consistentlayer of decalcifiedbone tissuein continuity with and parallel to the prosthetic interface. Basedon laboratory findings, the authors attribute this demineralization phenomenon to a high local concentration of aluminum ions with metabolicbone disease,which is histologically comparableto the osteomalacicosteodystrophy describedin dialysis patients. Thesefindings must be carefully considered given the potential long-term implicationsfor alumina-coatedimplants.Key words: hip prosthesis,alumina, aluminum, bone, mineralization, revision surgery.

much lower rates of wear’8-2’ than conventional ultra-high molecular weight polyethylene components. Recently, we identified several patients with pain following total hip arthroplasty (THA) performed with a cementless alumina-coated stem. As no radiographic signsof loosening or evidence of sepsiscould be detected, clinical evaluation of these patients was difficult. All casesdemonstrated dramatic remodeling of the proximal femur with respect to preoperative geometry. Nevertheless, the implant was radiographically in contact with cancellous (metaphyseal) and endosteal bone without true radiolucency or other suggestion of mechanical instability. The discrepancy between clinical presentation and diagnostic work-up required caution regarding surgical indication; nevertheless, eight patients with functionally limiting hip pain underwent femoral stem revision, permitting further investigation of the bone-prosthesis interface. The aim of this study is to analyze by microradiographic, x-ray diffractometry, and histochemical means the structure of the bone at the implant interface. In particular, our research is directed toward

The ceramic coating of cementless prosthetic hip implants has been advocated to achieve a more rapid and extensive secondary stabilization by bone ingrowth.le5 Among various ceramic coatings, the plasma-spray application of aluminum oxide (A1203) has been widely used6,’ in clinical applications. Such a ceramic coating has been described as being inert and entirely compatible with bone both in vitro by means of cell culture techniques’,’ and in viva with experimental implants.‘“-14 The ionic diffusion from AllO has been considered negligible, and consequently, the material has been regarded as extremely safe15-” from a biologic perspective. In addition to application in implant coatings, the mechanical properties of alumina have made it a reasonable load-bearing material in prostheses due to From the *Orthopaedic Clinic of the University of Bologna, Bologna, Italy, -fDepartment of Orthopaedic Surgery, University of Connecticut Health Center, Farmington, Connecticut, and +Laboratorv for Biocompatibi/it.v Research on Implant Materials, Istifuti Ortopedici Rizzoli, Bologna, Itab. Supported by grants from Istituto Ortopedico Rizzoli, Ricerca Corrente Area 6, 1992. Reprint requests: Dr. Aldo Toni, Orthopaedic Clinic of the University of Bologna, Via di Barbiano l/IO, 40136 Bologna, Italy.

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Table 1. Patient Case No.

Sex/Age (years) at Primary Surgery Ml62 F/68 F/54 Ml47 F/53 M/58 M/55 F/63

1994

Characteristics

Time to Revision (months)

6 16 18 28 33 42 Y 32

42 51 67 33 44 48 25 39

Between November 1985 and December 1989, we implanted 238 cementless anatomic ceramic arthroplasties (ANCA, Cremascoli, Milan, Italy) in 2 16 patients.7 Since December 1989, we used the same stem, but coated with hydroxylapatite. The femoral implant is automatically designed and fabricated of cobalt-chrome alloy (ASTM F75), and the body of the implant is entirely coated with air plasma-sprayed alumina. The stem has a madreporic surface on the anterior, posterior, and medial aspects of the proximal one third, with the remaining area being smooth. The head and socket articulating surfaces are fabricated of dense alumina. The ceramic acetabular component is chemically bonded at the periphery to a titanium-(TiA1,Va4) alloy threaded ring. The dome of the ceramic cup is coated with three-dimensional porous alumina (PORAL, Cremascoli)” to permit bone ingrowth of the component.

Ratings

Revised Implant Cemented Cemented Cemented Cemented Cemented Cemented Cementless Resection arthroplasty

Eight patients, at an average of 23 months following the index surgery (Table 1 ), presented with thigh pain (absent at rest and progressively worsening with walking) that was functionally limiting on a daily basis. In most cases (Table 2). the patients realized significant clinical improvement after their index surgery followed by recrudescent pain. Radiographs did not show loosening of the stem. There was evidence of stress shielding of the proximal femur. Thinning of the diaphyseal cortical bone (intracortical remodeling) and cancellous transformation (endosteal bone loss) were consistently noted. Radiographic aspects were quite different and classified as two types: 1, intracortical remodeling with endosteal bone loss (Fig. 1, 6 cases) and 2, proximal bone loss with marked distal hypertrophy (Fig. 2, 2 cases). To eliminate the possibility of occult sepsis, scintigraphy with technetium-labeled leukocytesl” was performed with negative results in all cases. Erythrocyte sedimentation rate, white blood cell count, and C-reactive protein titers were noncontributory. Arthrocentesis for culture was performed in five cases and was negative in all. None of the patients showed signs of allergic reaction, and no anamnestic data on allergic pathology were reported.

and Methods

Table 2. Postel-D’Aubigne

Surgery

Onset of Pain (months)

elucidating the etiology of these atypical radiographic presentations in a subgroup of patients with uncemented, alumina-coated femoral components.

Materials

at Index

for Pain, Ambulation,

and Joint Mobility

Score Case No.

*Girdlestone

Preindex Surgery

Maximum After Index Surgery

Prerevision Surgery

Final Follow-up Evaluation

2.2.5 4.5.3 2.3.3 4.5.5 3.5.4 3.3.6 2.3.2 3.3.4

2.4.5 4.5.5 4.6.5 5.6.5 6.6.6 6.5.5 5.3.5 6.5.5

3.2.6 3.3.5 2.3.3 4.5.5 3.4.4 4.4.2 3.2.5 3.3.4

4.4.6 6.4.6 4.4.6 6.5.6 6.6.6 6.6.6 6.6.6 2.3.3*

procedure.

First number

is pain rating,

second

is ambulation

rating,

and third

is joint

mobility.

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Fig. 1. Type I : intracortical remodeling with endostealbone loss.(A) Postoperativeradiograph. (B) Thirty-nine-month follow-up radiograph.

Due to persistent symptoms unrelieved by nonsteroidal therapy, these patients underwent surgical revision of the stem. Since the stem was not loose, caution was required for its removal to avoid damaging the surrounding demineralized bone. Macroscopically, the femoral bone was directly contacting the stem proximal surface. Using thin osteotomes and curved gouges, the metaphyseal bone was interrupted at the proximal porous stem surface. The bone presented a wet cardboard consistency, due to severe demineralization. With some strong hammering, the stem moved upward and could then be removed easily. The smooth surface (placed in the distal two thirds of the stem) was always extracted without any bone attached, while some spongeous bone was in the porous surface. After stem removal, in the diaphyseal canal, a continuous bone lamina reproduced the stem shape; this bone was sampled accurately

for histologic evaluation. Needle biopsies were also taken from the femoral cortex. In one patient (no. 8), biopsy specimenswere obtained at revision with a different presentation from that delineated above. In 1987, this patient had an uncemented revision of a cemented THA with subsequent failure of the acetabular component. Due to an unreconstructable acetabulum, she underwent resection arthroplasty (Girdlestone procedure) with removal of the ANCA stem that, despite the absence of unequivocal loosening, demonstrated dramatic loss of bone density with associated cortical remodeling. Histologic

Evaluation

For each case, sections of bone obtained adjacent to both the smooth surface and madreporic regions

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Fig. 2. Type 2: proximal bone losswith marked distal hypertrophy. (A) Postoperativeradiograph. (B) Forty-eight-month follow-up radiograph.

of the prosthesis were prepared. Only in the latter region was bone recovered still attached to the stem surface. Sections of bone tissue 5 pm thick were derived from samples fixed in buffered formalin at ph 7.2, dehydrated in methanol, then embedded in methyl methacrylate and deplasticized before staining. Transverse slices of the stem 5 mm thick, at the level of the macroporous zone, were obtained with the Exakt Cutting system (Kulzer 6 Co., Wehrheim, Germany) with boron nitride saws, taking particular care not to damage the bone spiculae that had grown within the macroporosites. After fixation in methyl methacrylate, slices were ground to a thickness of 50 pm for light microscopic evaluation of bone ingrowth. Both the deplasticized sections of the bone samples and those of the stem at the macroporous level were stained with traditional histologic methods, including Paragon (toluidine blue-basic fuchsin), modified

Goldner, and von Kossa stains. A method for detecting aluminum utilizing the ammonium salt of aurine tricarboxylic acid,‘” which aluminum hydroxide stains as a red band, was employed. The details of these techniques have been presented previously.23 Microradiography

Microradiographs per contact were obtained on sections 100 km thick using Kodak High Resolution Type 1A radiosensitive slides (Rochester, NY). X-ray Diffraction

Studies

Conventional powder diffraction analysis was carried out on the alumina coating of the retrieved stems and on the sockets and ceramic heads using a powder Bragg-Brentano goniometer (Philips, Almelo, The Netherlands). As a control measure of the structural analysis of the implanted prostheses, x-ray

Demineralization

diffraction was performed on the alumina coating of the stem of an unimplanted prosthesis. X-ray diffraction was obtained under the following conditions: 40 KV, 40 mA, l&hour exposition, and 5-70” 28 with 0.01 20 angular step. The crystalline composition of the coatings was identified using the crystallographic identification files of gamma (JCPD S # lo0425) and alpha (JCPDS # 10-0173) alumina. Wear debris was identified by means of microbeam x-ray diffraction, using the Chesley microcamera (Italstructures, Riva de1 Garda, Italy) in such a way as to focus the beam on a 50 km* area. Radiographic Evaluation Excluding cases with loosening or radiolucency in more than two areas, the femoral bone was classified, according to Gruen et a1.,24 as follows: type 1 remodeling: either thinning or cancellous transformation of the cortical bone or both that is present in the four proximal areas, according to the Gruen evaluation protocol, and type 2 remodeling: hypertrophy of the cortical bone in areas around the distal third of the stem, either medially, laterally, or both. Among the 238 hips, 22 were lost during the follow-up period and one stem was cemented. To evaluate the incidence of pain and the revision rate relating to the different remodeling types, 60 implants presenting with either loosening or radiolucencies at the socket or bone-stem interface were rejected, leaving 155 hips eligible for radiographic evaluation. Results Histochemical

tests carried out on bone tissue adja-

cent to the interface, both at the smooth and madreporic surfaces of the prostheses, demonstrated the

Fig. 3. Bone tissueat the alu-

mina interface. Demineralized bone tissue is stained lighter (Goldnerstain, original magni(A) Cobaltfication x25). chromealloy, (B) alumina, (C) demineralizedlayer, (D) mineralized trabecula.

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presence of a nonmineralized layer, parallel to the profile of the implant. The nonmineralized layer lining the madreporic surface was measured in sections with both alloy and bone, measuring 106 + 24 pm

thick (range, 68-140

pm). The bone contacting

the

smooth surface of the stem presented a laminar ar-

chitecture, which usually remained attached to the femoral bone. The retrieved sample of this lamina was histologically evaluated without the metallic counterpart. The nonmineralized layer thickness was 109.2 ? 41.3 pm (range, 74-164 pm). The morphology of the noncalcified zone was lamellar at the light microscopic level with osteon systems typical of mature bone over most of the surface. In several cases, individual osteons appeared clearly subdivided into both a nonmineralized part immediately adjacent to the prosthesis and a normally mineralized region in continuity (Fig. 3). The osteoclastdominated osteolysis of the failed cemented implant was not encountered in this series, and the histologic findings were remarkable for the absence of osteolysis per se; likewise, the bone interface could be described as hypocellular with no clearly increased populations of histiocytes or inflammatory cells. The histologic evaluation performed on some bone samples retrieved after stem removal and on the small amount of bone still attached to the ceramic surface could not permit any quantitative evaluation of bone ingrowth. Nevertheless, qualitative analysis of the bone-stem interface showed that no fibrous tissue was ever interposed between the porous surface and bone, while at the interface between the smooth surface and bone, either a thin fibrous or chondroid tissue layer was found in about 20% of the samples. By means of the specific histochemical technique described above, aluminum was found in all of the

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4. Same sample as Figure 3. The tricarboxilic acid stains the dark band and the aluminum hydroxide deposition front (arrows) which divides the mineralized (bottom) and demineralized bone tissue (top) (aluminum stain, original magnification X 40). Fig.

examined specimens, both at the level of the smooth stem and at the rough portion of the implant. It was found in the highest concentration and identified as a continuous line along the (de) mineralization front (Fig. 4). Only rarely was the linear deposit of aluminum at the level of the cement lines or throughout the calcified region of the bone. Microradiographs confirmed the absence of calcifi-

5. Top: bone trabeculae interrupted by a microfracture, evidenced by the reparative tissue. Bottom: bone trabeculae crack due to artifact (solochromocyanine, original magnification X 40).

Fig.

cation in the regions in close contact with the prosthesis. Microfractures were detected in the trabecular bone tissue surrounding the implant (Fig. 5). For six patients, the presence of microfracture was evaluated on tissue sample areas ranging from 6 to 22 mm’, and was expressed as number of microfractures per mm’. Microfracture incidence ranged from 0.05 to 0.6 per mm2 (average, 0.2 t 0.2 per mm”). Alumina

Demineralization Table

3. Femoral Remodeling vs Pain and Revision Rate Pain

Total No.

Type 1 Type 2 Absent*

17 28 110

% 10.9 18.0 70.9

No. 8 5 9

% 47.1 18.5 8.2

Revision Rate No. % 6 2 0

35.3 7.1 -

*Minor signs of remodeling could be present, but as far as they were not type 1 or 2 remodeling, they were not taken into account.

debris was detected at the bone-stem interface and evaluated quantitatively as the number of debris particles per mm’. Wear debris was seen in five of the six cases evaluated; particles ranged from 8 to 246 per mm2 (average, 87.4 * 103.1 per mm’). Alumina debris at the bone-stem interface was analyzed by means of microbeam x-ray diffraction, and was found to have the same composition as the stem coating, for example, gamma alumina. In fact, in all of the cases, we found crystallographic transformation of the coating of the stem from the stable a phase to the y phase, a form that is relatively less stable and permits a partial solubilization of the alumina coating. On the contrary, ceramic heads and sockets were consistently the stable CYphase. Alumina wear debris was also encountered in the capsular soft tissues in all but two cases. In these cases, the microbeam x-ray diffraction of the particles was not performed. Radiographs of the 155 stable arthroplasties, both socket and stem, were evaluated to define the incidence of type 1 and 2 femoral remodeling and their relation to pain and the revision rate (Table 3).

Discussion The application of ceramics in the fabrication of total joint arthroplasty implants continues to receive considerable attention; reports on negative phenomena related to their use are very scarce.25-27 The histopathologic findings of altered mineralization immediately adjacent to the prosthesis induced us to consider a possible toxic local effect of A120S, particularly given the absence of clinical or radiographic stigmata, suggesting metabolic bone disease in these patients. These findings appear somewhat analogous to those of osteomalacic bone, where the newly formed bone matrix fails to mineralize in a normal or timely manner. The presence of mature lamellar bone rather than osteoid bone alone, however, indicates that the phenomenon is more likely

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related to demineralization of otherwise normal bone. Alterations in mineralization, induced by the toxic effects of diphosphonates, fluorides, and aluminum, have been widely documented.“8-32 This study was directed toward the latter substance, which as aluminum oxide, constitutes the coating of the prostheses under study. The systemic toxicities of aluminum due to excessive oral or parenteral intake are well known.33 Aluminum intake in the diet is about lo- 100 mg a day and is influenced by the cooking modality and containers used. Absorption in the gastrointestinal tract is negligible in healthy subjects, but becomes significant in patients suffering from renal failure, where aluminum excretion is impaired. In viva, aluminum ions are largely protein-bound via transferrin. It is conceivable that this favors aluminum storage in cells with numerous transferrin receptors. The first reports on the possible toxicity of aluminum appeared in the early 1970’s when Berlyne et a1.34 observed that patients suffering from chronic renal failure and treated with aluminum ion-exchange resins to correct hyperkalemia showed significant increases in the plasma concentrations of the element. A similar increase was found in patients who took A1(OH)3 antacids to control hyperphosphatemia or peptic ulcer disease. In 1971, Parsons et a1.3s found significant amounts of aluminum, which could be related to both uremia and the duration of dialysis, in the bone tissue of nephropathic patients. Dent and Winter36 subsequently reported a case of osteomalacia due to hypophosphatemia induced by excessive intake of aluminum hydroxide. During the following years, these initial and occasional observations of aluminum toxicity were confirmed and became recognized as the etiologic agent in several dialysis-related complications. Many dialysed patients, in the long term, suffered from damage of the central nervous system, osteomalacia, and anemia. In support of these observations, Ward et a1.37 and Parkinson et a1.3” found a correlation between osteomalacia and the aluminum content of water used as a dialysate. As a corollary, patients receiving long-term total parenteral nutrition in the presence of a variety of intestinal disorders were found to develop metabolic bone disease. In such individuals with normal kidney function, bone pathology similar to that described for dialysed patients was noted. In this clinical scenario, the etiologic agent was found to be aluminum, which contaminated the casein hydrolysate source of protein in the parenteral nutrition formulation. 3,5 The biochemical mechanisms underlying alumi-

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num toxicity have not been identified with certainty. Numerous in vitro experiments have demonstrated interactions of aluminum with essential biochemical processes, but extrapolation to clinical aluminum toxicity is difficult. The documented interaction of aluminum with biologically important substances3’ can be summarized as ( 1) interactions with proteins (enzymes, calcium-binding proteins, structural proteins, storage proteins), (2) interactions with nucleotides, (3) interactions with phospholipides (cellular membranes), and (4) interactions with minerals (mainly hydroxylapatite) . At the bone-cellular level, Cournot Witmer et al.‘” and Robertson et al. 32 advanced the hypothesis that aluminum action on bone cells and matrix mineralization could be modulated by the parathyroid hormone. Other authors have suggested a direct action on osteoblasts, possibly mediated by the parathyroid hormone.4’ Bachra and Van Harskamp42 hypothesized that aluminum salts could interfere with the deposition of the bone-mineral matrix, forming insoluble phosphates, thus, creating a local depletion of phosphates able to inhibit regular calcium deposition. Ott et a1.43confirmed that aluminum deposition at the calcified bone boundary inhibits mineralization of the osteoid directly. Maloney et al.j4 further hypothesized that aluminum may bind at the mineralization front and consequently inhibit normal calcification, or that it may bind to existing hydroxylapatite crystals, thus blocking further deposition of calcium phosphate. In other studies, however, it has been demonstrated, by means of double tetracycline labels, that active mineralization may continue, despite the presence of substantial aluminum deposits.4’ Talwar et a1.45 highlighted the chemical-physical role of aluminum on the deposition of calcium phosphates in bone. Goodman et a1.46,“7 confirmed the toxic effect of aluminum on osteoblasts in their short-term toxicity tests on rats, although they were not able to define the role of the altered metabolism of vitamin D in mediating the phenomenon in their studies on dogs. In summary, the specific mechanism(s) for aluminum toxicity in bone remains enigmatic.” Although studies of aluminum toxicity are numerous, reports on analogous phenomena related to the implantation of alumina, either as bulk or coating, are extremely rare. Lewandowska-Szumiel and IQmende? carried out traditional histologic tests and assays of aluminum in the bone tissue of experimental models in which alumina rods were implanted for a period of 6-8 months. With normal histologic results, they found significant concentrations of aluminum in periprosthetic tissues. The microfractures that WC have quantitatively

1994

evaluated are the result of intravital phenomena and not artifacts incurred during histologic processing, as fracture repair is evidenced around them. Microfractures could be advocated as the cause or consequence of micromotion. We have not observed evidence of such motion at the bone-stem interface, since fibrous tissue was not found in the methaphyseal level where the microfracture was detected. Alumina wear debris was found adjacent to the implant in considerable concentration. The crystallographic evidence of the y phase detected for this debris proved to originate from the coating, since debris due to wear of the head-socket ceramic-bearing surfaces always presented in the (Y phase crystallographically. Type 1 remodeling presented a significantly (P < .0003) higher incidence of cases with pain, and consequently, a higher revision rate (P < .OOOl). Six of the eight cases revised were classified as type 1 remodeling. Conclusion We were not able to conclusively elucidate the mechanism(s) by which aluminum inhibits or reverses mineralization. Moreover, given the documented chemical stability of alumina, it is difficult to understand how aluminum ions appear to be leached from the coating. We can only suggest that crystallographic transformation occurs from the stable (Y phase to the relatively less stable y phase, and that the presence of impurities in the form of Al( OH) 3 are such that partial solubilization of the alumina coating follows in viva. Given the extensive world-wide use of alumina in clinical applications, the phenomenon we describe deserves careful evaluation, as one might hypothesize that periprosthetic decalcification leads to implant loosening. We have described a histologic phenomenon that appears to be related to the presence of aluminum at the bone-prosthesis interface. As noted above, we did not find loosening per se, but rather demineralization with residual bone apposition at the interface in the specimens retrieved at revision surgery. In our opinion, it is clearly premature to propose, in order to correct localized osteomalacia, the LW of therapies based on chelating substances (eg, desferrioxamine) as currently employed in the treatment of systemic dialysis-related metabolic bone disease. The phenomenon described was related to the relatively early onset of pain following the index surgery. We converted to the use of hydroxylapatitc coating in 1989, and in our study, only 8 of 238 hips (3.3%) have demonstrated progressive, functionally limiting

Demineralization

pain related to the changes described that required revision surgery. Therefore, an unproven prophylactic regimen directed toward preventing further clinical problems seems unwarranted at this time. Our observations, if further confirmed, could play an important role in the understanding of biocompatibility with prosthetic devices, and identify further areas of research in the application of ceramics to total joint arthroplasty. Our results also underline the need for at least 24 months of clinical validation to elucidate the long-term effects of the new coating.

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31. Rich C, Ensinck J: Effect of sodium fluoride on calcium metabolism of human beings. Nature 19 I : 184, 196 I 32. Robertson JA, Fenselfeld AJ, Haygood CC et al: Animal model of aluminium-induced osteomalacia: role of chronic renal failure. Kidney Int 23:327, I983 33. Slatopolsky E, Delmez J: Bone disease in chronic renal failure and after renak transplantation. p. 92 1. In Coe FL, Favus MJ (eds): Disorders of bone and mineral metabolism. Raven Press, New York, 1992 34. Berlyne GM, Ben Ari J, Pest D et al: Hyperaluminaemia from aluminum resins in renal failure. Lancet 5: 494, 1970 35. Parsons V, Davies C, Goode C et al: Aluminum in bone from patients with renal failure. BMJ 4:273, 1971 36. Dent E, Winter C: Osteomalacia due to phosphate depletion from excessive aluminium hydroxyde ingestion. BMJ 1:551, 1974 37. Ward MK, Feest TG, Ellis HA et al: Osteomalacic dialysis osteodistrophy: evidence for a water-borne aetiological agent, probably aluminium. Lancet 22:841, 1978 38. Klein GL, Alfrey AC, Miller NL et al: Aluminum as a factor in the bone disease of long term parenteral nutrition. Am J Clin Nutr 35:1425, 1982 39. Van de Vyver F, Visser WJ: Aluminum accumulation in bone, in trace metals and fluorides in bones and teeth. CRC Press, Boca Raton, 1990 40. Cournot Witmer G, Zingraff J, Plachot JJ et al: Aluminium localization in bone from hemodialyzed pa-

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tients: relationship to matrix mineralization. Kidney Int 20:375, 1981 Dunstan CR, Evans RA, Hills E et al: Effect of aluminum and parathyroid hormone on osteoblasts and bone mineralization in chronic renal failure. Calcif Tissue Int 36:133, 1984 Bachra BN, Van Harskamp GA: The effect of polyvalent metal ions on the stability of a buffer system for calcification in vitro. Calcif Tissue Res 4:359, 1970 Ott SM. Maloney SA, Coburn JW et al: The prevalence of bone aluminum deposition in renal osteodystrophy and its relation to the response to calcitrol therapy. N Engl J Mcd 307:709, 1982 Maloney NA, Ott SM. Alfrey AC et al: Histological quantitation of aluminium in iliac bone from patients with renal failure. J Lab Clin Med 99:206, 1982 Talwar HS, Reddi AH, Menczel .I et al: Influence of aluminium on mineralization during matrix-induced bone development. Kidney Int 29: 1038, 1986 Goodman W: Short-term aluminum administration in the rat: reductions in bone formation without osteomalacia. J Lab Clin Med 103:749, I984 Goodman W, Henry DA, Horst R et al: Parenteral aluminium administration in the dog: Induction of osteomalacia and effect on vitamin D metabolism. Kidney Int 25:370, 1984 Mare1 GM, MC Kenna MJ, Frame B: Osteomalacia. p. 335. In Peck W (ed): Bone and mineral research. Elsevier Science Publishers, Amsterdam, 1986