Histopathology and quantitative bone changes
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1 Archives of Disese in Childhood, 198, 55, Neontl rickets Histopthology nd quntittive bone chnges S J OPPENHEMER AND G J A SNODGRASS Deprtment of Morbid Antomy, London Hospitl Medicl College, nd Deprtment of Peditrics, London Hospitl SUMMARY Ribs from 3 preterm infnts, who hd died fter prolonged intrvenous feeding nd rtificil ventiltion, were exmined histologiclly nd ssessed for the degree of osteomlci nd osteoporosis in cncellous bone of the shft. A grid counting technique ws used. Osteomlci ws noted in ll 3 cses but to lesser degree thn in clssicl vitmin D-deficient controls. Osteoporosis ws pronounced in the cses of neontl rickets, but this ws not feture of the vitmin D-deficient controls. Histologicl fetures were similr to those reported in experimentl phosphtedeficient rickets nd vitmin D-resistnt rickets. A combintion of rchitic chnges nd multiple rib frctures occurring in preterm infnts hs been described by severl uthors.1 This report describes the histology nd quntifies the chnges in cncellous bone occurring in 3 neontes dying with rickets; ech hd received prolonged intrvenous limenttion including intrvenous vitmin D. Mteril nd methods Three groups were studied. Norml controls, 9 term fresh stillbirths nd firstweek neontl deths. Vitmin D-deficient rickets, 6 cses occurring in infncy were obtined from the London Hospitl pthologicl collection. Neontl rickets, 3 infnts who hd died of bronchopulmonry fibroplsi nd hert filure fter prolonged mechnicl ventiltion. Ech of them hd received prolonged intrvenous feeding including intrvenous vitmin D supplements of 2 U dily (5,ug). n ech cse there hd been x-ry nd biochemicl evidence of rickets before deth. Suitbly-stined, undeclcified sections of rib were ssessed quntittively for osteoid nd minerlised bone content. A grid re point counting method ws used.2 This enbles n ccurte estimte to be mde of the res occupied within cncellous bone by osteoid nd minerlised bone. A Zeiss integrting disc No 4 ws used, which incorportes grid of 9 points. Only cncellous bone in the shft of the rib ws studied nd n verge of 7 different re counts ws tken for ech cse (tht is 63 points). To seprte elements of osteomlci nd osteoporosis, the results were expressed in the following form: % osteoid = men osteoid grid count x 1/(men osteoid grid count + men minerlised grid count). This expression indictes the proportion of the totl osseous tissue tht is unclcified (norml <5%).2 To produce vlue for the proportion of totl osseous in cncellous bone (tht is, bone density), the osteoid nd minerlised bone counts were combined nd expressed s percentge of the totl tissue re. Thus: % totl osseous tissue = (men osteoid grid count + men minerlised grid count) x 1/9 The sttisticl method used for comprison ws the Mnn-Whitney U test. Results The reltive vlues of % osteoid nd % totl osseous tissue re shown in Fig. 1. The men % totl osseous tissue in the norml controls ws 33-6% ± 1- (n = 9), while tht in the vitmin D-deficient rickets cses ws 37 5% SE (n = 6), nonsignificnt difference (P> 5). n contrst, the % totl osseous tissue in the 3 intrvenously-fed infnts ws less thn 2%. This ws significntly less thn in both the other groups (P< 5). The men % osteoid in the norml 945
2 946 Oppenheimer nd Snodgrss Fig. ' 45., osseous tissue. ts; S X ~ F & - 55e Reltive proportions of % osteoid nd % totl controls ws 3 5% SE ± 7 (n = 9), much less thn tht in vitmin D-deficient rickets (P<-1). As cn be seen from Fig. 1, the % osteoid in the intrvenously-fed infnts occupied n intermedite position between the norml infnts nd the clssicl vitmin D-deficient cses, nd tken s group were different from either of the other groups (P <.5). Histopthology A norml costochondrl junction from term stillbirth is shown in Fig. 2. Vitmin D-deficient rickets. Ribs All 6 cses showed clssic florid chnges of vitmin D-deficient rickets. The histologicl chnges hve been fully described,3 but the following re relevnt to the discussion. There is gross enlrgement of the costochondrl junction (Fig. 2b). This is due to the expnsion in thickness nd lterl width of the crtilge plte nd to the production of thick bnd of osteoid. With osteoblstic ctivity norml or incresed, there is deposition of bundnt osteoid e e \S: directly on to crtilge. Filure of osteoclstic resorption occurs since osteoclsts cn only remove clcified mteril. As result the crtilge is indequtely removed nd there is irregulr invsion of blood vessels. Subperiostel bone formtion is less ffected; it overtkes endochondrl ossifiction t the sides nd produces the chrcteristic cup deformity (Fig 2b). n the shft, trbecule re orientted in bizrre fshion, tend to be thickened, nd re covered over most of their surfces by thick osteoid sems. Clcified bone is of the lmellr type. Osteoblstic ctivity is norml or incresed. Osteoclstic ctivity is reduced or bsent. The cortex tends to be thickened nd covered with thick osteoid sem; it is often reduplicted. With the virtul bsence of osteoclsts norml resorption remodelling does not occur. Neontl cses. Cse Cse 1 ws fed intrvenously throughout life (3 months) nd by the time deth occurred t the gesttionl ge of 44 weeks, rchitic chnges were florid. These re described in detil. The ribs on the left from 7 to 1 nd on the right from 6 to 1 were frctured t the ngle. Around ech frcture ws hrd fusiform swelling 5-7 mm in dimeter. The ribs were soft nd esily deformed (s were ll bones exmined). The costochondrl junctions were enlrged up to 6 mm nteroposterior. The lower femorl ossifictions centre ws present. Specimens of lower end of femur, rib, nd rib frcture were tken nd embedded undeclcified in methcrylte. Histologiclly (Figs 2c nd d), there ws n enlrgement of the costochondrl junction to 5*5 mm (norml 3 mm). The hypertrophic zone of crtilge ws incresed to 3 mm nd the columns of hypertrophic cells showed disorderly lignment nd pronounced vrition in size, with mny lrge ellipsoid lcune especilly t the periphery. The normlly cler junction between the hypertrophic zone nd the zone of provisionl clcifiction ws replced by disorgnised re 3 mm deep, where there ws irregulr penetrtion of the crtilge by blood vessels leving residul lrge tongues nd islnds of clcified crtilge (TCC) deep in the primry spongios (Figs 2c nd d). These tongues of clcified crtilge were prtly covered with thin osteoid. Also in this disorgnised re were scttered smll islnds of osteoid. A few osteoclsts were seen in the primry spongios minly ssocited with islnds of prtly clcified crtilge. The cncellous bone of the shft ws chrcterised by (1) thin, sprse, irregulr, poorly-clcified
3 trbecule consisting of woven bone. (2) Modertely thickened osteoid sems covering pproximtely hlf the surfce of the trbecule. (3) Very little osteoclstic ctivity. (4) Very few nd flttened osteoblsts. Neontl rickets 947 The cortex of the shft ws very thin nd in one plce buckled. There ws thick lyer of subperiostel osteoid on the outer cortex but poor osteoblstic ctivity. The rib shft ws very porotic. There ws n Arch Dis Child: first published s /dc on 1 December 198. Downloded from Fig. 2 Undeclcified sections of rib from () norml stillbirth, (b) clssicl vitmin D-deficient rickets, (c) nd (d) Cse (neontl rickets), (e) rib frcture from Cse 1. Fig. 2 (, c, e,) Von Koss stin for clcifiction. Fig. 2 (b, d) hemtoxylin nd eosin. x 12. CP=crtilge plte, ZPC=zone of provisionl clcifction, BV=invdingbloodvessels,ost=osteoid,TCC=tonguesofclcified crtilge, CD=clcified deposit, Crt=crtilge. on 22 Februry 219 by guest. Protected by
4 948 Oppenheimer nd Snodgrss irregulr frcture but no displcement (Fig. 2e). The trbecule djoining the frcture site showed only slight signs of remodelling. The cllus ws composed of bundnt osteoid nd metplstic crtilge but showed little clcifiction. Lungs showed mrked prenchyml fibrosis: the cuse of deth ws bronchopulmonry fibroplsi. Histology of other orgns ws norml. Cses 2 nd 3 showed bony chnges similr to those of Cse 1, with the sme chrcteristic disorgnistion of the costochondrl junctions nd generlised osteoporosis, but these infnts, who hd received intrvenous phosphte supplements in the lst weeks of their lives, showed evidence of heling: (1) lthough the osteoid sems in the shft were thicker thn norml they were thinner thn in Cse 1; (2) the trbecule in the shft were chrcterised by core of woven bone (s in Cse 1) but this ws surrounded by lyer of fresh lmellr bone lined with ctive osteoblsts. Discussion The three infnts described in this pper hd been fed intrvenously for long periods nd received vitmin D throughout. Bone chnges were similr microscopiclly nd by quntittive ssessment of the reltive mounts of bone nd osteoid. The evidence for their being considered s rickets is: (1) widened costochondrl junctions; (2) deepened disordered crtilge plte; (3) irregulr invsion of the crtilge plte by blood vessels; (4) poor removl of crtilge; (5) widened osteoid sems; nd (6) disordered remodelling of the cortex nd of the cncellous bone of the shft. Despite these similrities to clssicl rickets, there re importnt differences between our cses nd vitmin D-deficient rickets (Tble). A common mechnism for these differences could be decresed osteoblstic ctivity in the neontl cses, which does not occur in the vitmin D-deficient cses. We suggest tht these neontl cses re in fct Tble Bone histology compred in vitmin D-deficient rickets nd neontl rickets hypophosphtemic rickets nd tht this rickets is chrcterised by: (1) indequte minerlistion of osteoid (s in vitmin D-deficient rickets), nd (2) reduced osteoblstic ctivity. The histology of Cse 1 shows the osteoblsts to be fewer in number nd forming considerbly less mtrix thn in vitmin D-deficient rickets where there is norml or incresed ctivity. This reduced osteoblstic ctivity would ccount for the pronounced osteoporosis. Osteoblsts ppered to be norml in Cses 2 nd 3, but these infnts hd lredy been prtly treted with phosphte; in other respects they resembled Cse 1 nd showed mrked osteoporosis nd disorgnistion of the costochondrl junction. n this connection osteoporosis is n estblished ccompniment of fmilil vitmin D-resistnt rickets.4-5 Moreover Villnuev et l.f obtined direct evidence of mrked reduction of osteoblstic ctivity in vitmin D-resistnt rickets using double tetrcycline lbelling technique. Another difference between the neontl rickets cses nd vitmin D-deficient rickets is the persistence of tongues of clcified crtilge in the primry spongios in the former. Similr findings were described in untreted vitmin D-resistnt rickets,7 nd in phosphte-deficient rts.8 Confirmtion tht the bone chnges in Cse 1 were due to hypophosphtemi is shown by the effects of tretment. Cses 2 nd 3 who received dequte phosphte for some time before deth showed norml osteoblstic ctivity, ccompnied by the development of norml orderly lmellr bone on the previously formed disorderly woven bone. n this connection Engfeldt et l.9 described the formtion of bnorml woven bone in vitmin D- resistnt rickets. The minerlistion of osteoid showed return to norml; this ws prticulrly pronounced in Cse 3 who hd received prolonged tretment with phosphte. Furthermore, there ws reorgnistion of the re of the primry spongios, nd in Cse 3 the beginnings of orderly norml endochondrl ossifiction. Norml Vitmin D-deficient Neontl rickets controls rickets (n=9) (n=6) Cse Cse 2 Cse 3 Costochondrl junction Accumultion of osteoid ginst crtilge plte Absent + + Verylittle Verylittle Very little Clcified crtilge tongues in primry spongios Absent Absent Rib shft Thickness of trbecule Norml t Thickness of osteoid sems Norml tt t t t Proportion of trbecule covered by osteoid (Y%) Osteoblstic ctivity Norml t or norml 14 Norml Norml Corticl thickness Norml t 14
5 n conclusion, histologicl evidence is presented tht rickets occurring in preterm infnts intrvenously fed is qulittively nd quntittively different from vitmin D-deficient rickets. Phosphte deficiency my be n etiologicl fctor. Clinicl supporting evidence for this will be presented in subsequent pper. We thnk Professor Donich nd Professor B Vernon-Roberts both formerly of the Deprtment of Morbid Antomy, London Hospitl Medicl College, for dvice, Mr V Trenwith, Senior Technicin, for prepring the undeclcified sections, nd Dr E M E Poskitt, nstitute of Child Helth, Alder Hey Hospitl, Liverpool, for reding the mnuscript. References Anonymous. Rickets, jundice, nd lte onset respirtory distress in premture bbies. Br Med J 1977; ii: Woods C G, Morgn D B, Pterson C R, Gossmn H H. Mesurement of osteoid in bone biopsy. JPthol Bcteriol 1968; 95: Pommer G. Untersuchungen uber Osteomlcie und. Rchitis. Leipzig: Vogel, Neontl rickets Cooke W T, Brcly J A, Gorn A D T, Ngley L. Osteoporosis ssocited with low serum phosphorus nd renl glycosuri. Arch ntern Med 1947; 8: Huge B N. Vitmin D resistnt osteomlci. Act Med Scnd 1956; 153: Villnuev A R, lnicki L, Frost H M, Arnstein R. Mesurement of the bone formtion rte in cse of fmilil hypophosphtemic vitmin D resistnt rickets. JLb Clin Med 1966; 67: Kuhlmn R E, Stmp W G. Biochemicl biopsy evlution of the epiphysel mechnism in ptient with vitmin D resistnt rickets. J Lb Clin Med 1964; 64: Colemn R C, Becks H, Kohl F V N, Copp D H. Skeletl chnges in severe phosphorous deficiency of the rt: tibi, metcrpl bone, costochondrl junction, cudl vertebr. Arch Pthol 195; 5: Engfeldt B, Zetterstrom R, Winberg J. Primry vitmin- D resistnt rickets.. Biophysicl studies of skeletl tissue. J Bone Joint Surg (Am) 1956; 38: Correspondence to Dr G J A Snodgrss, Deprtment of Peditrics, London Hospitl, Turner Street, London El 1BB. Received 2 October 1979 Arch Dis Child: first published s /dc on 1 December 198. Downloded from on 22 Februry 219 by guest. Protected by
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