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Mesotheliomas of Peritoneum, Epicardium, and Pericardium Induced by Strain MC29 Avian Leukosis Virus1

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Mesotheliomas of Peritoneum, Epicardium, and Pericardium Induced by Strain MC29 Avian Leukosis Virus1 [CANCER RESEARCH 30, 1287 1308, May 1970] Mesotheliomas of Peritoneum, Epicardium, and Pericardium Induced by Strain MC29 Avian Leukosis Virus1 J. F. Chabot, Dorothy Beard, A. J. Langlois, and J. W. Beard Department of Surgery, Duke University Medical Center, Durham, North Carolina 27706 SUMMARY myeloid hematopoietic tissue neoplasms distributed in bone, liver, and other sites, primary renal tumors occur Injection of strain MC29 avian leukosis virus into the in high incidence, erythroblastosis is occasionally seen, peritoneal, pericardia!, and air sac cavities of the chicken and, in small proportion, growths arise from hepatic pa- resulted in high incidence of tumors of the mesothelium renchymal cells (9). A singular influence of the MC29 of the respective structures. As determined by light and strain is the infection and rapid morphological alteration of CEC" in tissue culture not observed with other leuko electron microscopy, the growths arose as papillomas or expanding tumors by alteration of the squamous mesothe sis agents (4, 8, 16). Recent studies initiated with the in lium to spheroidal or cuboidal cells characterized by u/7ro-altered CEC revealed still another unusual host re rounded nuclei with clear nucleoplasm and very large sponse to this leukosis strain. Cells inoculated into the nucleoli and cytoplasm deeply stained with hematoxylin. chicken by different routes gave rise to tumors simulating With continued rapid growth, the nuclear features les transplants at various sites in the peritoneum. However, sened somewhat, cytoplasmic staining diminished greatly, introduction in the same way of cell-free fluid from CEC and the cell limits became indistinct. A second stage of cultures altered by MC29 virus resulted in the appear metaplasia was marked by frequent alteration of the ance of growths at similar sites and, also in the pericar epithelioid cells to cartilage which increased both by con dium and epicardium. Further investigation showed that tinued alteration of peripheral mesothelioma cells and certain of the tumors were the result of neoplastic re proliferation of chondrocytes. The tumors, sometimes sponse of peritoneal and pericardial mesothelium to in isolated but usually coalesced in masses, were poorly en fection with the MC29 virus. Studies have been made of capsulated, contained little fibrous stroma, and showed the occurrence, pathomorphology, and ultrastructure of no necrosis. They readily invaded contiguous visceral tis some of these tumors, and the results are described in sues but did not metastasize to distant sites. Numerous this report. For comparison there are considered, also, 2 tumors in subcutaneous tissue and myelocytic1 growths virus particles were observed in the tumors together with occasional budding of the particles from the cell mem in visceral organs. Growths induced by response to prep branes. The mesotheliomas were an addition to the al arations of morphologically altered cells will be consid ready broad spectrum of responses to strain MC29 virus ered in another report. consisting of myelocytic growths, high incidence of renal tumors, primary tumors of the liver parenchyma, and singular aspects of morphological alteration of chick em MATERIALS AND METHODS bryo cells in vitro. These virus-induced tumors in the chicken closely resembled mesotheliomas of unknown Virus. Isolation of strain MC29 leukosis agent and etiology in man and bovines in both morphology and be chicken response to virus obtained from blood plasma havior. from birds diseased with the strain were described (12, 18). The virus for the present studies was in 3 pools from CEC cultures infected with strain MC29 of previous pas INTRODUCTION sage in vitro. Passage was in primary cultures (14) of embryos from eggs of RIF-free White Leghorn hens4 Strain MC29 avian leukosis virus infection in the (22). Fluids in contact with cells of altered morphology chicken results in the induction, principally, of myelocy- for 4.5 to 6 hr in cultures 6 to 15 days following exposure toma and myelocytomatosis (12, 18). In addition to these "The abbreviations used are: CEC, chick embryo cells: RIF, re 1This work was aided by USPHS Grant C-4572, by the Annie Ma sistance-inducing factor; WW, subcutaneous wing web tissue; i.e.. intra- bel Sherris Memorial Grant for Cancer Research from the American cardiac: dpi, days postinoculation. Cancer Society, Inc., by National Defense and Education Act Title IV ' The term myelocyte is used in descriptions of strain MC29 virus Fellowship 67-08530.0, by IN-611 American Cancer Society International disease to designate nonmyeloblast myeloid elements at any level of Research Grant, and by the Dorothy Beard Research Fund. The paper differentiation—with or without granules (15, 18)—lessthan that of the is part of the studies submitted by J. F. C. in partial fulfillment of the mature granulocytes. requirements for the degree of Doctor of Philosophy in Zoology in the 4The chick embryos were from White Leghorn eggs provided by Graduate School of Arts and Sciences of Duke University. Dr. Roy Luginbuhl, University of Connecticut, through the Research Received September 12, 1969; accepted November 19, 1969. Resource Program of the National Cancer Institute Bethesda, Md. MAY 1970 1287 Downloaded from cancerres.aacrjournals.org on September 30, 2021. © 1970 American Association for Cancer Research. Chabot, Beard, Langlois, and Beard to virus (14) were harvested and passed through 0.45-^ nitely related to dose as measured by numbers of virus Millipore filters. Virus particle content and infectivity of particles. Introduction of virus into the heart through the the fluids were measured by electron microscopy (24) chest wall gave neoplasms of the epicardium or pericar and focus assay (13), respectively. dium or both in 4 of 19 birds. Injections into the wing Chickens and Examinations. White Leghorn chicks of webs of 19 chicks resulted in l (Y148) apparently virus- line 15 (28) were inoculated 1 day after hatching with induced subcutaneous growth. Another tumor in subcu virus amounts and by WW, i.e., or i.p. routes as indicated taneous tissue (Y623) arose in the abdominal wall near in Table 1. Blood smears made routinely as in earlier the site of i.p. inoculation. Generalized response of the studies (5) were stained with May-Grunwald-Giemsa. myeloid hematopoietic cells consisted principally of At the onset of illness or after appropriate periods of diffuse infiltration of the liver by nongranulated myelo- study, birds were killed by bleeding from the heart. Tis cytes—myelocytomatosis—with few circumscribed cell sues for light microscopy were taken in Zenker-formol aggregates—myelocytomas; few of the cells contained solution, and the sections were stained with hematoxylin eosinophilic granules. Except in birds receiving inocu and eosin. Some sections were stained with Alcian blue lations i.e. (into the circulating blood), myeloid cell re and by Masson's technique. Cells from peritoneal fluid sponse was relatively small. Line 15 chickens were less were stained with May-Grunwald-Giemsa or hematoxy- responsive to strain MC29 in this respect than the Shaver lin-eosin. birds previously used (18). Moreover, as with BAI strain Specimens for electron microscopy were fixed for 2 to A (myeloblastosis) virus (6), the i.p. inoculation route was 4 hr in 5% glutaraldehyde (Fisher G-151, Fisher Scien much less effective in the induction of generalized mye tific Co., Silver Spring, Md.) buffered at pH 7.2 with loid response than the i.v. or i.e. routes. sodium cacodylate (20, 23); transferred to 0.1 M sodium Peritoneal Tumors. Birds with tumors in the peritoneal cacodylate buffer, pH 7.4, containing 0.3 M sucrose (23); cavity exhibited general signs of lassitude, droopiness, and held for 2 to 5 days at 4°.The tissues were postfixed disinterest, and ruffled feathers. The skin and mucous for 1 hr with 1% osmic acid buffered at pH 7.2 with Vero membranes were pale, and the blood smears of many of nal (19), embedded in Maraglas (7), sectioned with glass the birds showed large mononuclear primitive cells (15, knives on a Porter-Blum ultramicrotome, stained with 18) of the myeloid series. Peritoneal fluid in volumes of uranyl acetate (29) and lead citrate (21), and examined about 8 to 80 ml was found in a large proportion of the with a Siemens Elmiskop I at 80 kV equipped with a birds, and some animals showed pronounced abdominal double condenser and a 50-/¿objectiveaperture. distension. The murky, greenish fluid contained large numbers of mesothelial cells and other mononuclear ele ments. RESULTS Figs. 1 to 4 illustrate the gross appearance of minute beginning MC29 virus-induced growths (Fig. 1) and that Table 1 summarizes 3 experiments yielding the results of large (Fig. 2) and smaller (Figs. 3 and 4) developing described here (Bird Y879, Figs. 18 to 21, from a differ neoplasms. An impressive feature of the process was the ent study was given an injection i.p. of 8.5 X 10' virus high growth response of the mesothelial cells in the loose particles). Of 148 birds receiving inoculations into the folds of mesentery. This was indicated by the numerous peritoneal cavity in the 3 studies, 52 had tumors of de tiny individual growths (Fig. 1) and emphasized by the monstrable mesothelial cell origin. Incidence was defi multitude of nodules coalescing into the extensive nodu- Table I Chicken response to tissue culture-grown MC29 virus inoculated into the wing web. into the peritoneal cavity (i.p.), and into the heart (i.e.) Cor. no., number of chicks surviving early nonspecific deaths; MYE. myeloid growth: PCS, pericardial or epicardial neoplasms; PTS, tumors of peritoneal mesothelium: ERY, erythroblastosis; SUBC, tumor in subcutaneous tissue; and ASC, ascites. Exper-Virus . r particles no.19191716181619172223MYE15563141530PCS4000000000PTS1012105121714ERY1000000000SUBC0100000010ASC221141021710 iment v6(X (ml)0.10.050.50.50.50.50.50.50.250.5Routei.e.WWi.p.i.p.i.p.i.p.i.p.i.p.i.p.i.p.ChicksinoculatedY100-I19Y139-157Y158-176Y347-364Y365-383Y384-401Y402-421Y422-440Y602-624Y625-648(20)(19)(19)(18)(19)(18)(20)(19)(22)(23)Cor )961 10 2513127971 115234.60.90.18985 280560Volume 1288 CANCER RESEARCH VOL.
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