Differentiation of malignant from normal and reactive mesothelial cells by the argyrophil technique for

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1 Thorx 1988;43: Differentition of mlignnt from norml nd rective mesothelil cells by the rgyrophil technique for nucleolr orgniser region ssocited proteins JON G AYRES, JOHN G CROCKER, NCHOLAS Q SKLBECK From the Deprtments of Respirtory Medicine nd Histopthology, Est Birminghm Hospitl, Birminghm ABSTRACT Nucleolr orgniser regions represent nucleolr ctivity in both norml nd mlignnt cells. More numerous nucleolr orgniser regions hve been found in cells from mny forms of mlignncy thn in norml cells. An rgyrophilic method of stining these regions (the AgNOR technique) hs been pplied to specimens ofpleur obtined by biopsy or t necropsy in n ttempt to differentite between norml, "rective," nd mlignnt pleurl disese. The number of nucleolr orgniser regions in smples tken from 10 ptients with norml pleur (men 1 04 (95 % confidence intervl )) ws less thn the number seen in smples from 10 ptients with "rective" (inflmmtory) pleurl disese (1-75 ( ); p < 0-001). This is the first demonstrtion of incresed numbers of nucleolr orgniser regions in n inflmmtory condition. n specimens from 25 ptients with mesotheliom the corresponding numbers of nucleolr orgniser regions were: tubuloppillry (n = 10) 5.43 (4 42-6A44); undifferentited (n = 5) 5-00 ( ); srcomtous (n = 5) 7 52 ( ); nd mixed histologicl types (n = 5) 4-94 ( ). All these vlues differ significntly from those for both norml nd "rective" tissue (p < 0-001). t is concluded tht the AgNOR technique seprtes "rective" pleurl disese from mesotheliom with high degree of confidence nd is n importnt dvnce in the dignosis of mlignnt mesotheliom. Nucleolr orgniser regions represent res of ribosoml DNA on certin chromosomes from which ribosoml RNA is formed' nd their numbers per nucleus re thought to reflect nucleolr ctivity.2 Studies of vrious forms of mlignncy3 (prosttic crcinom,2 melnocrcinom,4 smll cell bronchogenic crcinom,5 nd crcinom of the brest6) hve confirmed tht enumertion of nucleolr orgniser regions s identified by n rgyrophilic method (the AgNOR technique) permits cler differentition of mlignnt from benign tissue. This technique stins proteins ssocited with nucleolr orgniser regions.7 n non-hodgkin's lymphom' the numbers of nucleolr orgniser regions re relted to the degree of mlignncy of the tumours. Mlignnt mesotheliom is n uncommon tumour with vrible histologicl ppernces.9 The two mjor res of difficulty in the pthologicl dignosis of this tumour re in its differentition from denocr- cinom nd, in pleurl biopsy specimens, in defining whether the mesothelil cells re "rective" or mlignnt. n n ttempt to throw light on the ltter problem we hve pplied the AgNOR technique to norml pleur nd to pleur obtined from ptients with "rective" nd mlignnt pleurl disese to determine whether this simple stining method cn help to seprte benign from mlignnt disese of the pleur. Methods Blocks of pleurl tissue obtined t thorcotomy or necropsy were studied. Specimens were obtined from 10 subjects with norml pleur, from 10 subjects with pleur hving "rective" histologicl chnges, nd from 25 ptients with mesotheliom. n the cses of "rective" chnges the tissue ws obtined t necropsy in five nd t open lung biopsy in five (tble). n the open lung biopsy specimens the underlying cuse ws Address for reprint requests: Dr J G Ayres, Deprtment of Respirtory Medicine, ssessed s Est Birminghm Hospitl, Birminghm B9 5ST. inflmmtory (tht is, resolving pleurisy with or without pneumoni) in ll cses becuse of the Accepted 26 Jnury 1988 findings t thorcotomy nd the subsequent recovery 366

2 Differentition ofmlignntfrom norml nd rective mesothelil cells by the rgyrophil technique 367 Men number ofsilver stined nucleolr orgniser regions (AgNORs) per cellfor ech tissue section ccording to histologicl type Mesotheliom Norml Rective Tubuloppillry Undifferentited Srcomtous Mixed (n = 10) (n = 10) (n = 10) (n = 5) (n = S) (n =5) 09 09* * * * * 7-5 Men SD % C *Necropsy specimens. Cl-confidence intervl. of the ptient. n the cse of the postmortem specimens ll the ptients hd hd pneumoni with pleurisy. n three cses the pneumoni ws distl to n obstructing tumour, but there ws no histologicl evidence of tumour in the re from which the biopsy specimen for this study ws tken. Norml pleur ws obtined from resected lobes or lungs for loclised crcinoms with no peripherl extension of tumour. Mesotheliom tissue ws obtined by open lung biopsy in ech cse; the tumour ws clssified ccording to the nomenclture used by Whitwell nd Rwcliffe.' Of the 25 specimens, 10 were tubuloppillry, five undifferentited polygonl cell, five srcomtous, nd Men No AgNORs Per cell mll -14- i No rml Rective Tubuloppillry T-r five mixed type tumours. The nture of the tumours ws confirmed by positive lcin blue-hyluronidse stining nd lck of immunohistochemicl rection for crcinoembryonic ntigen. The method for stining nucleolr orgniser regions is fully described elsewhere.8 Briefly, sections were dewxed, tken to wter, nd wshed in deionised, distilled wter. The rection mixture consisted of geltin in 1 g/dl formic cid to mke 2 g/dl solution, which ws then mixed with 50 g/dl silver nitrte in proportion of 1:2. After 30 minutes' incubtion t room temperture in the drk the specimens were wshed, tken to xylene, nd mounted in synthetic - Undiff. Srcomtous Mixed pol ygonl Mesothel iom Fig 1 Men number (wsith 95% confidence intervls) of stined nucleolr orgniser regions (AgNOR dots) per cellfor norml pleur, rective pleur, nd thefour histologicl grdes ofmesotheliom.

3 368 Fig 2 Normlpleur showing on verge one stined nucleolr orgniser region (AgNOR dot) per cell (focusing confirmed this number). medium. For ech smple the number of silver stined nucleolr orgniser regions (AgNORs) in 100 cells were counted with the id of grticule, with creful focusing on ech cell to enble cler identifiction of ech AgNOR dot. t is impossible to enumerte AgNOR dots without knowledge of the histologicl type; interobserver vrition in our hnds is of the order of 10%. Cells nd fields were selected t rndom. n the mixed type of tumour, cinr nd spindle cells were counted in proportion to their presence in the biopsy specimen. nflmmtory nd stroml cells (such s endothelil cells nd fibroblsts) were excluded. For sttisticl nlysis we used Student's t test for unpired dt nd clcultion of 95% confidence intervls (C). Results The men number of AgNOR dots per nucleus ws 1-04 (95% C ) for norml mesothelil cells nd 1-75 ( ) for "rective" cells (tble nd figs 1-3). These vlues were significntly different (p < 0001). The pooled vlue for norml nd rective specimens ws 1 4 ( ). The men number of AgNOR dots for the mesothelioms rnged from 4 94 (95% C ) in the mixed type to 7-52 ( ) for the srcomtous type (tble nd figs 1, 4, nd 5). The pooled dt for ll Ayres, Crocker, Skilbeck 25 mesothelioms, regrdless of cell type, ws 5-66 ( ), which ws highly significntly different from the pooled dt for norml nd rective dt combined (p < 0-001). Discussion After the originl identifiction of nucleolr orgniser regions by cytogeneticists nd their subsequent use of the regions in the investigtion of certin trisomies,11 interest hs recently turned to the number nd distribution of nucleolr orgniser regions in mlignnt cells.38 After the initil observtion tht more nucleolr orgniser regions were present in prosttic crcinom cells thn in cells from hyperplstic prostte,2 similr observtions hve been mde in lymphom,8 smll cell crcinom of the bronchus,5 nd melnocrcinom.4 The consistency of the finding tht mlignnt cells from different orgn sites hve more nucleolr orgniser regions thn the cells of their tissue oforigin suggests tht this simple technique is n indictor of mlignncy. t my consequently replce or be complementry to flow cytometry in this regrd. Recent modifictions (discussed elsewhere8) hve simplified nd improved the sensitivity of the AgNOR technique, mking it esy to use in ny lbortory. The interobserver nd introbserver vrition in counting AgNORs is 10-12%...**X.*~P.A.: 7 Fig 3 Pleurl tissue showing rective mesothelil cells showing bout two stined nucleolr orgniser regions (AgNOR dots) per cell nucleus.

4 Differentition ofmlignnt from norml nd rective mesothelil cells by the rgyrophil technique Wo. 0.1 #. #, % S. * ;,. *0 :, --o* Fig 4 Tubuloppillry type mesotheliom showing incresed numbers ofstined nucleolr orgniser regions (AgNOR dots) per cell. Our findings show tht, in n re which hs cused much dignostic difficulty in the pst, the AgNOR technique is ble to seprte clerly mlignnt from benign pleur. Previous ttempts to do this by the use of ntibodies to epithelil membrne ntigen hve been unsuccessful.'2 Other immunohistochemicl methods hve been pplied to the problem of seprting denocrcinom from mesotheliom, the most useful being stining for crcinoembryonic ntigen nd,b pregnncy specific glycoprotein.'3 These re both negtive in ll but few mesothelioms, wheres in denocrcinom one or both re invribly positive.'3 These techniques do not, however, differentite between rective nd mlignnt mesothelil cells / U - S s. E. 6.. t* -., * 1 A _-P,* '.)-..3,6 3 ' S 33*.3 ' \.,.e * '' *'6 U *.53 i 4.Q,-, A- * 'o,,*"j:, rf 0" 4s 11 t. Fig 5 Srcomtous mesotheliom verging eight stined nucleolr orgniser regions (AgNOR dots) per cell. ilf.^ AN0, t,4e v. R ) 369 in consistent mnner. Our findings confirm tht the cells from ll four types of mesotheliom hve more AgNORs thn cells from either norml or "rective" pleur, the lrgest number being in the srcomtous form. We must emphsise tht the sections used in this study were cut t 3 gm thickness, nd the quoted numbers of AgNOR dots thus re not bsolute numbers of nucleolr orgniser regions per nucleus, which cn be obtined only from cell imprint preprtions.8 The configurtion nd distribution of the AgNORs (found only on chromosomes 13, 14, 15, 21, nd 22 in norml humn cells'4) hve yet to be investigted fully in mlignnt cells, lthough "ectopic" AgNORs hve been reported in metphse spreds of testiculr cncer nd myeloid leukemi cells.' 16 The finding tht "rective" cells cn be seprted from norml cells by this technique shows for the first time tht this method my be extended to the investigtion of inflmmtory diseses. Further investigtion here should look t possible differences between the nucleolr orgniser regions of inflmmtory lesions nd those of low grde mlignncy. The prognosis of mesotheliom is very poor, most ptients dying within two yers of presenttion. t is importnt when ptient with pleurl effusion hs been exposed to sbestos to obtin firm dignosis. The benign pleurl effusion ssocited with sbestos exposure crries fr better prognosis,'7 lthough there is some suggestion tht the condition might be premlignnt. Assessment of mesothelil cells from such ptients with the AgNOR technique would be of interest, dignosticlly in the first instnce, nd over long period with seril mesurements tht might help to detect the development of mlignnt chnge. References 1 Alberts B, Bry J, Lewis J, Rff M, Roberts K, Wtson JD. Moleculr biology of the cell. New York: Grlnd, 1983: Ploton D, Menger M, Jennesson P, Himber G, Pigeon F, Adnett JJ. mprovement in the stining nd in the visulistion of the rgyrophilic proteins of the nucleolr orgnizer region t the opticl level. Histochem J 1986;18: Editoril. NORs- new method for the pthologist. Lncet 1987;i: Crocker J, Skilbeck NQ. Nucleolr orgniser regionssocited proteins in cutneous melnotic lesions: quntittive study. J Clin Pthol 1987;40: Crocker J, Ayres J, McGovern J. Nucleolr orgniser regions in smll cell crcinom of the bronchus. Thorx 1987;42: Smith R, Crocker J. Evlution of nucleolr orgnizer region-ssocited proteins in brest mlignncy. Histopthology 1988;12: Ochs RL, Buswch H. Further evidence tht phospho-

5 370 protein C23(1 1OKD/pH 5 1) is nucleolr silver stining protein. Exp Cell Res 1984;152: Crocker J, Nr P. Nucleolr orgnizer regions in lymphoms. J Pthol 1987;151: Spencer H. Pthology of the lung. 4th ed. Oxford: Pergmon Press, 1984: Whitwell F, Rwcliffe RM. Diffuse mlignnt pleurl mesotheliom nd sbestos exposure. Thorx 1971;26: de l Cruz FF, Gerld PS. Trisomy 21. Bltimore: University Prk Press, 1981: Kerr KM, Cossr D, Krjewski AS, Lmb D. Histochemistry in the dignosis of pleurl biopsies [bstrct]. Thorx 1987;42: Gibbs AR. ndustril lung disese. n: Anthony PP, Ayres, Crocker, Skilbeck Mcsween RNM, eds. Recent dvnces in histopthology. No 13. Edinburgh: Churchill Livingstone, 1987: Lewin B. Gene expression: 2. Eukryotic chromosomes. 2nd ed. New York: Wiley, 1980: De Lzier-Blnchet CD, Wlt H, Engel E. Ectopic nucleolus orgnizer regions (NORs) in humn testiculr regions. Cytogenet Cell Genet 1986;41: Kohno S, Abe S, Mtsui S, Sndberg AA. Chromosomes nd custion of humn cncer nd leukemi. XXXV. Nucleolus orgnizers on the Ph chromsome in chronic myelocytic leukemi. Cncer Genet Cytogenet 1979;1: Hillerdl G. Non-mlignnt sbestos pleurl disese. Thorx 1981;36: Thorx: first published s /thx on 1 My Downloded from on 31 October 2018 by guest. Protected by copyright.

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