Effect of environmental pollutants, polychlorinated biphenyls (PCBs), on the reproductive function of adult male rhesus monkey (Macaca mulatta)

Abstract

Three groups (n=4 each) of adult male rhesus monkeys (Maeaea mulalta) were Jen oral treatment of Aroclor 1242 or Aroclor 1254 at a dose of 200 fIg/kg ./day/animal or vehicle (corn oil and glycerol) for SIX months to exanllne the effect of :Bs on plasma testosterone, testicular and accessory gland morphology During the ~atrne nt period, observations were made on body mass and testicular size. Blood 1m pies (3 ml X 2) were collected on weekly basis for determination of testosterone Jels. At the end of the treatment period, the animals were sacrificed humanely. Testis Id accessory glands (epididymides, seminal vesicles and prostrates) were removed, .ed and processed for light and electron microscopy. Serum testosterone .ncentratian was determined by radioimmunoassay. PCB treatment caused pathological symptoms (loss of appetite, diarrhea, thargy, fever and vomiting), clinical signs of toxicity (swelling of eyelids, edema under e eyes, hair loss and appearance of lesIons in nail beds) and neurobehavioral langes including depression, aggression and lethargy. Mean body weights of Aroclor !54-treated animals decreased significantly while the Aroclor 1242-treatment only ghtly reduced body weights of the treated animals. Teshcular diametel of both the :B-treated groups also decreased significantly during the treatment period The langes In body weight and testicular diameter were highly correlated in Aroclar 1254- ,ated group but not in Aroclar 1242-treated animals. While Aroclor 1254-treatment did )t affect the mean plasma testosterone levels, there was a general decline in the Jels of hormone in Aroclor 1242-treated monkeys. PCB-treatment resulted in disruption of normal epithelial organization due to lich spermatogenetic activity in the seminiferous tubules was adversely affected. The ckness of the tunica propria increased in both the PCB-treated groups and it ,veloped wavy margins accompanied by separation of the basement membrane from ~ necrotic peritubular Myeoid cell layer, The number of spermatogonia was reduced ,d differentiation between sub-types was not possible in the Aroclor 1254-treated vi DUp. The spermatogonia of Aroclor 1254~treated animals were abnormally large In <e showing much vanability In shape and disorganization of cyloplasm They had und or oval completely euchromatic and hypertrophied nuclei. On the other hand. the lermatogoma of Aroclor 1242~treated testes did not show such abnormalities In sIze \d shape. yet exhiblled slight hypertrophy and vesiculation. The Sertoll cells of Aroclor !54-treated testes appeared highly shrunken with cluslering at some places. Nuclear foldings were reduced to a great extent. In Aroclor 1242-treated testes, the 'toplasmlc extensions of Sertoli cells in many sections occupied lumInal areas besides lot of fat droplets gathered peripherally. The Leydig cells of the Aroclor 1254- and ,hicle-treated monkeys were more or less similar. Leydig cells of Aroclor 1242-treated stes were higilly damaged and contained pyknotic nuclei. Cytoplasm was scanty. At ,me places, the Leydig cells also contained fat droplets and vacuolation. The ultrastructural observations of testes revealed that the basement membrane both the PCB-treated groups was far apart from the Myeoid cells and the gap was ;cupied by disassembled collagenous fibers. In Aroclor 1254-lreated lestes, lermatogonia lacked most of the cytoplasmic componenls and developed empty laces. Delamination of the cell membrane. distortion of mitochondrial cristae. ustering of mitochondna, decreased endoplasmic reticulum, shrinkage of the 'toplasm and pyknosis of nuclei were the main features of spermatogonia of Aroclor !42-treated testes. In Aroclor 1254-lreated lestes, the spermatocytes were very rare ld highly necrotic. However, in Aroclor 1242-treated testes, though the spermatocytes ld condensed chromatin, yet the cytoplasm at most of places was sh runken. The ocess of spermeogenesis which was not evident in the sections of Aroclor 1254- ,ated testes, was also adversely affected in Aroclor 1242-treated testes exhibiting Image in the form of shrinkage of the cytoplasm and thickening of cell membrane of e round and elongated sperm at ids, absence of stages of acrosomal formation and :istence of some abnormal spermatozoa. In the Aroclor 1254 ~trea ted testes, the size the Serloli cells was much reduced , cytoplasm was disorganized and lacked ganelles except mitochondria, ectoplasmic specializations were damaged and nuclear foldings were reduced. Though the cytoplasm of the Sertoli cells of Aroclar 1242- rated testes contained mitochondria, endoplasmic reticulum , Goigi apparatus and fat oplets, empty spaces of vanable sIzes and reduction of nuclear infoldings were .mmon observations In these cells In the Leydig cells of the Aroclor 1242-treated lImals, the cytoplasm developed zones of electron dense and electron opaque 9,ons, empty patches, thread-like extensions of the cell membrane, distort.on and 'knosis of nLlc!ei and variations in the quantity of heterochromatin. All accessory glands were also affected by the PCB treatment The proportion of mnective tissue increased considerably in all the PCB-treated accessory glands. The lithelium in the Aroclar 1254-treated epididymides was increased in thickness and ratification. The cells were necrotic and lacked stereocilia. It was not possible to scriminate between cell types owing to the effect of the pollutant. Some of the cells ere abnormally large. In the epididymides of the Aroclor 1242-treated animals, the minal spaces lacked spermatozoa. The epithelium contained Irregular-shaped necrotic ,lis that possessed stereocilia. In the prostate glands of the Aroclar 1254-treated lima Is, the lumina of the gland were either collapsed or much reduced in size and led with a single layer of necrotic cells with pyknotic nuclei that frequently showed , t.chment and accumulated in the luminal matrix. In the prostate glands of the Aroclor ?42-treated animals, the epithelium was thickened With cells that had lost their normal Iboldal/columnar shape. The nuclei of these cells too were pyknotic. Often the lithelial cells were hypertrophied and thus appeared conspicuous. In the seminal !Sicles of both the PCB-treated groups, the mucosal fold attained abnormal 'ganization with an increase in the thickness of the epithelium due to increased ratification. Cellular features of PCB-treated seminal vesicles were also adversely fected. It is concluded that exposure of male adult rhesus monkeys to Aroclor 1254 and 'oclor 1242 causes severe morphological alterations. Aroclor 1254 has far mare 'totoxic influence than Aroclar 1242. Of the two PCBs tested on monkeys, only Aroclar ~42 exerted estrogenic effect.