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On the Proliferative Changes Taking Place in The ON THE PROLIFERATIVE CHANGES TAKING PLACE IN THE EPITHELIUM OF VAGINA AND CERVIX OF MICE WITH ADVANCING AGE AND UNDER THE INFLUENCE OF EXPERIMENTALLY ADMINISTERED ESTROGENIC HORMONES 1 V. SUNTZEFF, E. L. BURNS, MARIAN MOSKOP AND LEO LOEB (From the Laboratory of Research Pathology, Washington University School 01 Medicine, St. Louis) In the course of our studies of the effects of estrogen injections on the epithelium of the mammary gland in various strains of mice we observed the development of epithelial processes in vagina and cervix reaching downward into the underlying connective tissue and becoming carcinoma-like under the influence of this substance. Comparing these experimental animals with nor­ mal, non-injected mice, we found that long processes, and even processes re­ sembling early stages of cancer, may also develop spontaneously, without in­ jections of estrogen, though apparently less frequently. There exists, then, a noteworthy analogy between the behavior of the non-stimulated and that of the estrogen-stimulated mammary gland on the one hand, and the non-stim­ ulated and estrogen-stimulated epithelium of vagina and cervix on the other (1,2,3). In the study of these processes in vagina and cervix it is not primarily our aim to describe the precancerous or early cancerous lesions of the epi­ thelium, but to consider the gradual changes which take place in this epi­ thelium from early to advanced age, with and without the stimulation of estrogen and other hormones, in mice belonging to various strains, and the eventual transition from normal growth processes to precancerous and early cancerous proliferations. Before proceeding to the description of these changes it will be necessary to discuss briefly some facts concerning the struc­ ture of the vagina and especially of the cervix in the mouse. In our investigations into the alterations which take place during the sexual cycle in the vagina, cervix, and uterus of the guinea-pig (4), we found that the cervix may be divided into three parts, namely, the vaginal, inter­ mediate, and uterine cervix. The structure and mode of reaction of the vaginal cervix are similar to those of the vagina, while the uterine cervix re­ sembles the uterus in these respects, although both these parts differ to some extent from the adjoining areas in vagina and uterus. There exists thus a graded transition from vagina to uterus as far as structure and response to estrogen and lutein hormones are concerned. In the mouse the differentiation of the various parts of the cervix is less marked than in the guinea-pig, but here also there are indications that it exists. 1 These investigations were carried out with the aid of a grant from the International Cancer Research Foundation. We are indebted to the Schering Corporation for part of the estrogenic substance used in the experiments. 256 PROLIFERATIVE CHANGES IN VAGINA AND CERVIX OF MICE 257 Thus there is a gradual decrease from vagina to uterus in the height of the squamous epithelium which develops under the influence of estrogen. This may be taken as a suggestion of graded changes in the constitution of the epithelium of the cervix in the direction of the uterus; but the distinction between vaginal and medium cervix is less sharply defined than in the guinea­ pig. Likewise, an area of transition seems to exist between the uterus and cervix. Where the mucosa begins to be covered by a single layer of epi­ thelium, this cell-layer still possesses to a certain extent a tendency to become changed into a low squamous epithelium; while such a change may take place in the uterus proper, this tendency is greater in the lower uterine tissues than in those higher up. In order to simplify the description of alterations which take place in the vagina, cervix and the beginning of the uterus, we have divided this tract into four parts: The vagina up to the level at which the cervix begins is designated FIG.!. SCHEMATIC REPRESENTATION Ol!' VAGINA AND CERVIX Ol!' MOUSE as area 1; that part of the vagina which consists of folds running parallel to the cervix as area 2, including the portio, which connects the vaginal folds and the beginning of the uterus; the cervix proper as area 3, and the beginning of the uterus, corresponding to the cervix in the guinea-pig, as area 4. These subdivisions are shown in Fig. 1. The changes which are analyzed in this paper affect not only the vagina proper, but also the portio and the cervix, and they may extend to the beginning of the uterus. The whole tract extending from the beginning of the vagina to the beginning of the uterus is designated as VC in the tables, and occasionally also in our discussion. In order to describe the downgrowth of the' epithelium into the underlying connective tissue and the formation of epithelial processes in vagina, cervix, and the beginning of the uterus, in an approximately quantitative manner in different individuals and strains, we have adopted the following terminology: 258 V. SUNTZEFF, E. L. BURNS, MARIAN MOSKOP AND LEO LOEB Grade 0 signifies either the absence of downgrowth or the presence of only very short epithelial processes. Grade 1 represents epithelial processes ex­ tending for a moderate distance into the underlying tissue. Grade 2 signifies epithelial processes which reach to a considerable depth and which may, in addition, have begun to branch out. Grade 3 indicates a precancerous down­ growth, extending deeply and invading the connective tissue irregularly, with branching processes, frequently showing hyaline pearls. Grade 4 designates a marked cancer-like invasion of the underlying connective tissue and adjoin­ ing parts. One of the points which we wished to determine was whether a relation exists between the degree of proliferation in the vagina and cervix (VC) in different individuals and strains and that in the mammary gland. For this purpose we have recognized the following grades of proliferation in the mam­ mary gland. Grade 0 signifies that mammary gland ducts are seen very rarely. Grade 1 designates a mammary gland tissue consisting of frequent branching ducts, which mayor may not be surrounded by a very small number of acini. Grade 2 indicates a precancerous proliferation of the mammary gland, and Grade 3 complete carcinomatous transformation. Altogether we studied the condition of vagina and cervix in 375 mice; 128 of these served as controls, while 235 were injected with estrogenic hor­ mones, 52 of the latter group receiving, in addition to estrogen, preparations of anterior pituitary or lutein hormone, or of both. These 52 mice we have designated as combination-treated mice. In addition 12 mice were injected with lutein or anterior pituitary preparations without estrogen. Included in the total series of 375 mice is an injected" New Buffalo" mouse to which no VC grade could be assigned. It was found that the depth to which the epithelial processes penetrated into the underlying connective tissue varied greatly in different mice. In some almost no processes were present, while in others they were so strongly developed in places that a precancerous state or one of early cancer presented itself. Intermediate conditions of all kinds existed. Even in the same mouse the character of the epithelial processes often differed in different areas of the vaginal-cervical tract; these differences were recorded by assigning dif­ ferent grades to different areas. In this way it was possible to compare the average degree of the development of the vaginal-cervical epithelial processes in different individuals. Notwithstanding the presence of variations within the same animal, it was possible to correlate the degree of development of the processes with (1) the age of the mice and (2) the nature and quantity of the hormones injected. Vagina, cervix, uterus and mammary gland, and often also other organs, after the death of the animals, were studied in sections and the ovaries were cut into serial sections. The large number of mice used in our experiments made the analysis of our findings by statistical methods possible. Two difficulties, however. had to be overcome. In the first place the assigning of grades to VC in different mice depends upon the judgment of the individual observer and is therefore not entirely objective. In order to eliminate this personal factor as much as possible two persons graded the microscopic specimens independently of each other, after a third investigator had described the histologic changes. PROLIFERATIVE CHANGES IN VAGINA AND CERVIX OF MICE 259 TABLE I: Epithelial Processes and Age at Death in Controls of Various Strains (Total Controls: 128) VC-o VC-l VC-2 VC-3 and VC-4 Strain Age at Age at Age at Age at Number death Number deathNumber death Number death of mice (months) of mice (months) of mice (months) of mice (months} A 21 10.0 26 9.5 3 15.5 C57 12 8.5 12 8.3 3 17.7 D 8 12.3 1 22.0 3 16.0 1 20 C3H 5 8.4 3 16.7 CBA 4 9.6 6 10.2 New Buffalo 1 18.0 3 20.0 4 18.0 Old Buffalo 8 17.1 4 21.8 Number and av- 59 (46% . 10.9 55 (42.9% 11.4 13 (10.2% 16.9 1 (0.8% 20 erage age at of total) of total) of total) of total) death While there were some differences between the grades given by these observers, these were, on the whole, slight. A second difficulty consisted in the fact that the age at which the mice died or were killed with chloroform depended upon certain accidental factors and differed in different groups of mice.
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