DECILIATION IN THE PUERPERAL FALLOPIAN TUBE*

Transcription

1 FERTILITY AND STERILITY Copyright < 1978 The American Fertility Society Vol. 29, No.1, January 1978 Printed in U.SA. DECILIATION IN THE PUERPERAL FALLOPIAN TUBE* KENICHI SEKI, M.D.t J. RAWSON, PH.D.t CARLTON A. EDDY, PH.D. NANCY K. SMITH, PH.D. CARL J. PAUERSTEIN, M.D.:!: Center for Research and Training in Reproductive Biology, Department of Obstetrics and Gynecology, and Department of Anatomy (Morphology Core Laboratory), The University of Texas Health Science Center at San Antonio, San Antonio, Texas Tubal segments obtained from patients at cesarean section and at intervals during the first 5 postpartum days were examined to evaluate puerperal changes in the tubal epithelium. The specimens of tubal epithelium were examined under the scanning and transmission electron microscopes. Ciliated cells were most densely distributed on the fimbria and in the ampulla, and were relatively sparsely distributed in the isthmus. Progressive diminution of numbers of ciliated cells and deciliation of individual cells were noted in specimens obtained during the puerperium; Nonciliated cells were in the resting stage at term pregnancy. Secretory activity returned during the puerperium. Although it is widely accepted that tubal epithelium undergoes morphologic changes during the ovarian cycle, pregnancy and the puerperium, and under the influence of exogenous hormones,1-5 there is disagreement concerning specific changes in the structure and distribution of the ciliated cells during the cycle. There is also some argument as to whether or not human tubal epithelium undergoes cyclic ciliation-deciliatioll- 6 Changes in ciliated cells during the human puerperium have been the subject of controversial reports. Andrews 7 reported deciliation and inactive tubal epithelium following delivery. Two weeks after delivery, the epithelium was said to resemble that oflate postmenopause_ On the contrary, Patek et al. 8 and Horbelt9 observed pro- Received July 5, 1977; revised August 19, 1977; accepted August 22, *Supported in part by Grant P30 HD A1 from the National Institute for Child Health and Human Development. trockefeller Foundation Postdoctoral Fellow in Reproductive Biology. :j:reprint requests: Carl J. Pauerstein, M.D., University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, Tex liferative activity or evidence of active cytoplasmic organelles in puerperal ciliated cells. The present study was designed to document puerperal changes in the ciliated cells of the human oviduct. MATERIALS AND METHODS Entire oviducts or segments of oviduct were obtained from 14 patients, ages 19 to 36, undergoing surgical sterilization at selected intervals related to delivery (4 at cesarean section, 3 at 26 to 27 hours after delivery, 5 at 62 to 72 hours after delivery, and 2 at 108 to 112 hours after delivery). For transmission electron microscopy (TEM), samples were fixed immediately in 2.5% glutaraldehyde-2% paraformaldehyde mixture in 0.1 M cacodylate buffer for 4 hours and postfixed in buffered 1% osmium tetroxide for 2 hours. They were dehydrated in graded series of ethanol followed by propyreroxide and embedded in Spurr's plastic. 10 Thin sections were cut on an LKB 8800A Ultra tome III, stained with uranyl acetate and lead citrate, and examined with a Siemens 101 electron microscope_

2 76 SEKI ET AL. January 1978 FIG.!' Distribution of ciliated cells in fallopian tubes obtained at cesarean section. The ciliated cells are most populous in the fimbria (a). The distribution in the ampulla (b) was slightly less than that in the fimbria, but only scattered ciliated cells are noted in the isthmus (c). (a, x890; b, x890; c, x 1,390). For scanning electron microscopy (SEM), small segments were longitudinally incised and rinsed several times with buffer solution. Fixation and dehydration were performed utilizing the same method as for TEM. After placement in acetone the segments were subjected to critical-point drying and were then coated with gold and palladium by sputtering and observed with a JSM-35 scanning electron microscope. RESULTS Term Pregnancy. Although some differences were observed among segments and even in the same segments, in general the ciliated cells made up about 20% to 30% of the epithelium in fimbriae obtained at cesarean section. The proportion of ciliated cells was slightly lower in the ampulla than in the fimbria. In contrast, ciliated cells were sparsely distributed in the isthmus (Fig. 1). Several atypical cell forms were observed. Smaller, nonciliated cells about onefourth the size of the normal cells and covered with microvilli were prominent. Cells containing only a single cilium, about the same length as the normal cilia, were also observed. Some cells demonstrated short cilia that were clumped together (Fig. 2). Examination by TEM revealed decreased height of both ciliated and secretory cells. The latter protruded into the lumen beyond the ciliated and secretory cells. The cytoplasm of the ciliated cells was less electron-dense. The nuclei were round or oval. In contrast, the cytoplasm of the nonciliated cells was darker, and the nuclei were elongated and less regular. The mitochondria appeared smaller than those seen in the ciliated cells, and fewer polyribosomes were noted, as compared with the ciliated cells.

3 Vol. 29, No.1 DEC ILlATION IN THE PUERPERAL FALLOPIAN TUBE 77 FIG. 2. a, Ampulla of fallopian tube at cesarean section. Note that the surfaces of the nonciliated cells are covered with microvilli the lengths of which are different in each cell. The tiny nonciliated cells (arrows) are covered with similar microvilli. b, A single cilium is seen on several cells in the fimbria (arrows). These cilia are almost the same length as the normal cilia. c, Several short cilia are gathered together on the surface of a cell in the ampulla (arrows) (a, x7, 810; b, x7,400; c, x 13, 150).

4 78 SEKIET AL. January 1978 FIG. 3. Term pregnancy. The ciliated cells demonstrate light cytoplasm, many cilia are seen in cross-section. Mitochondria (M) are well-developed. Nonciliated cells demonstrate darker cytoplasm. Golgi apparatus (G) and endoplasmic reticulum are seen in both cell types. Polyribosomes are scattered in the cytoplasm. Desmosomes (D) are prominent (x7,625). FIG. 4. Term pregnancy. Well-formed cilia with well-developed basal rootlets (R) are seen. The microvilli (arrows) and mitochondria (M) are also well-developed. Polyribosomes are scattered in the cytoplasm (x19,240).

5 Vol. 29, No.1 DECILIATION IN THE PUERPERAL FALLOPIAN TUBE 79 FIG. 5. This figure contrasts the ciliary distribution in the fallopian tube at 62 hours (a) and 112 hours (b) postpartum (a, xl,030; b, xl,150). No secretory granules were observed in the cytoplasm (Fig. 3). No evidence of degeneration was seen in the ciliated cells (Fig. 4). The cilia were well-formed, as were the striated rootlets. Well-developed mitochondria were present, and polyribosomes were scattered throughout the cytoplasm. Puerperium. In the puerperium the numbers of ciliated cells decreased with time. This decrease was most obvious in the fimbria and in the ampulla. The individual ciliated cells were widely separated (Fig. 5). By 62 hours the cilia on many cells had decreased in number and length. Some cells displayed only a simple cilium (Fig. 6). The FIG. 6. a, Ampulla of oviduct at 62 hours postpartum. Ciliated cells are isolated from each other. One cell has shorter and clumped cilia (arrow). Single cilia are shorter than those seen at cesarean section. Some secretory granules are observed. b, Isthmus at 62 hours postpartum. An isolated ciliated cell with diminished number of cilia is seen. A short, single cilium and microvilli of variable length are observed on nonciliated cells (a, x5,150; b, x8,480).

6 80 SEKI ET AL. January 1978 t FIG. 7. Single cilium from 55-hour oviduct. A well-developed basal striated rootlet (R) is associated with the cilium. b, fimbria at 108 hours postpartum. The cell contains basal body (BB) and basal rootlet (R), but deciliation has occurred (a, x22,6l0; b, x52,800).

7 Vol. 29, No.1 DECILIATION IN THE PUERPERAL FALLOPIAN TUBE 81 FIG. S. Nonciliated cell demonstrating dense microvilli. Some of the microvilli have fused with each other. This specimen was taken from the isthmus at 26 hours postpartum (x20,soo). FIG. 9. Nonciliated cell in the isthmus at los hours postpartum. The nucleus is more regular in shape. The Golgi apparatus (G) is slightly distended. The mitochondria (M) are well-developed. Electron-dense secretory granules are observed in the cytoplasm (x 14,400).

8 B2 SEKI ET AL. January 1978 ultrastructure was similar to that seen in term pregnancy. The cells with a single cilium displayed an otherwise normal structure, including the striated rootlet. The basal body and rootlet persisted even in cells showing only stumps of cilia or no cilia, observed at lob hours. Condensation forms, the precursor of basal body formation in ciliogenesis, were not observed (Fig. 7). N onciliated cells did not protrude into the lumen as much as in the cesarean section specimens, but the microvilli were well-developed and regularly distributed. In the nonciliated cells at 26 hours postpartum the majority of organelles were located in the region of the nucleus. The mitochondria were spherical or oblong with prominent cristae. Rough-surfaced endoplasmic reticulum was distributed sparsely. The Golgi apparatuses were few in number and appeared slightly distended. A large number of polyribosomes were scattered irregularly in the cytoplasm. Some cells contained several lipid droplets. The surfaces of the nonciliated cells were covered with microvilli. Some were longer than the others and fused together (Fig. B). Later in the puerperium the nuclei of the nonciliated cells were more regular in shape. The mitochondria were better developed. The Golgi apparatus and endoplasmic reticulum were increased in number and size and more distended. Secretory activity was also observed (Fig. 9). DISCUSSION Ciliated cells at term pregnancy and early in the puerperium were most densely distributed in the fimbria and ampulla and decreased in the isthmic portion. This finding is in agreement with studies of the normal menstrual cycles and of midpregnancy12 but contradicts the results of Hashimoto et al,13 and Ferenczy et al.,14 who reported even distribution of ciliated cells along the entire oviduct. At term pregnancy, the cilia were of normal length and the cytoplasmic organelles, including the basal rootlets, were well-developed. We found no evidence of degeneration such as drooping cilia or a granulated surface appearance as reported by Patek et al. 12 and Hashimoto et al. 13 in midpregnancy. We observed a decrease in the number of ciliated cells in the puerperium, thus confirming the report by Andrews. 7 In addition, the numbers of cilia on many cells were decreased, and the cilia were shorter. We observed many cells with a single cilium. Although it is difficult to distinguish deciliation from regeneration, we saw no clear evidence of ciliogenesis. Oberti and Gomez Rogers1S demonstrated the formation of centrioles and subsequently of basal bodies in the initial stages of ciliogenesis. We saw no such structures in our material. In addition, our observation of many cells demonstrating well-developed striated rootlets but no cilia presents evidence of deciliation, but not of ciliogenesis. Thus, we believe that deciliation occurs in the early puerperium as a result of estrogen withdrawal. The conclusion is strengthened by the observations of other authors of cells containing decreased numbers of cilia in postmenopausal women.16 The nonciliated cells of term pregnancy were in the resting stage, as reported by previous authors.b.9 In these reports many flat cells with sparse microvilli, scant endoplasmic reticulum, and absence of secretory granules were noted. In the puerperi um, these cells increased in volume. Microvilli were well-developed and the expansion of the Golgi apparatus and endoplasmic reticulum as well as the presence of secretory granules suggested resumption of secretory activity. These observations agree with those of Horbelt9 and Patek et al. B In summary, our observations suggest resumption of secretory activity and prolonged regression of the ciliated cells during the early puerperium. Acknowledgments. We gratefully acknowledge the cooperation of Dr. R. Huff and Dr. R. Hayashi in obtaining the clinical material. REFERENCES 1. Fredericsson B: Proliferation of rabbit oviduct epithelium after estrogenic stimulation, with reference to the relationship between ciliated and secretory cells. Acta Morphol Neerl Scand 2:193, Bjorkman N, Fredricsson B: Ultrastructural features of the human oviduct epithelium. Int J Fertil 7:259, Fredricsson B, Bjorkman N: Studies on the ultrastructure of the human oviduct epithelium in different functional states. Z Zellforsch Mikrosk Anat 58:387, Hashimoto M, Komori A, Hirasawa T, Yokoyama Y, Akashi K: Electron microscopic studies on the perithelial cells of the human fallopian tube. Report I. J Jap Obstet Gynecol Soc 9:200, Clyman M: Electron microscopy of the human fallopian tube. Fertil Steril17:281, Woodruff JD, Pauerstein CJ: The Fallopian Tube: Structure, Function, Pathology and Management. Baltimore, Williams & Wilkins Co, Andrews Me: Epithelial changes in the puerperal fallopian tube. Am J Obstet Gynecol 62:28, 1951

9 Vol. 29, No.1 DECILIATION IN THE PUERPERAL FALLOPIAN TUBE Patek E, Nilsson L, Hillema M: Scanning electron microscopic study of the human fallopian tube. Report IV. At term gestation and in the puerperium: the effect of a synthetic progestin on the postmenopausal tube. Fertil Steril 24:832, Horbelt DV: Ultrastuctural changes in fallopian tube epithelium at term gestation and during postpartum period. Texas Med J 66:76, Spurr AR: A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31, Patek E, Nilsson L, Johannisson E: Scanning electron microscopic study of the human fallopian tube. Report I. The proliferative and secretory stages. Fertil Steril 23: 459, Patek E, Nilsson L, Johannisson E, Hellema M, Bout J: Scanning electron microscopic study on the human fallopian tube. Report III. The effect of midpregnancy and of various steroids. Fertil Steril 24:31, Hashimoto M, Shimoyama Y, Kosaka M, Komori A, Hirasawa T, Yokoyama Y, Kawase N, Nakamura T: Electron microscopic studies on the epithelial cells of the human fallopian tube. Report II. J Jap Obstet Gynecol Soc 11:92, Ferenczy A, Richart RM, Agate FJ, Purkerson ML, Dempsey EW: Scanning electron microscopy of the human fallopian tube. Science 175:783, Oberti C, Gomez-Rogers C: "De novo"ciliogenesis in the human oviduct during the menstrual cycle. In Biological Reports: Basic and Clinical Studies, Pan American Congress of Anatomy III, Edited by JT Velardo, BA Kasprow. New Orleans, 1972, p Gaddum-Rosse P, Rumery RE, Blandau RJ, Theirsch JB: Studies on the mucosa of postmenopausal oviducts: surface appearance, ciliary activity and the effect of estrogen treatment. Fertil Steril 26:951, 1975