Experimental intoxication of pregnant goats with Tetrapterys multiglandulosa A. Juss. (Malpighiaceae)

Intoxicação experimental por Tetrapterys multiglandulosa A. Juss. (Malpighiaceae) em cabras gestantes

Experimental intoxication of pregnant goats with Tetrapterys multiglandulosa A. Juss. (Malpighiaceae)

(Intoxicação experimental por Tetrapterys multiglandulosa A. Juss. (Malpighiaceae) em cabras gestantes)

M.M. Melo¹, A.C.Vasconcelos², G.C. Dantas², R. Serakides¹, F. Alzamora Filho¹

¹Escola de Veterinária da UFMG

Caixa Postal 567

30123-970 - Belo Horizonte, MG

²Instituto de Ciências Biológicas da UFMG

Recebido para publicação, após modificações, em 26 de outubro de 2000.

E-mail: [e-mail]

ABSTRACT

Green leaves of Tetrapterys multiglandulosa A. Juss were fed to pregnant goats from day 35 of pregnancy. Five goats received 10g/kgBW (group I), five received 20g/kgBW (group II) and five were used as control (group III), and received only hay, fresh grass and commercial ration. All animals were clinically examined daily and submitted to ultrasonography every three days. Fetal death and vulvar catarrhal discharge with subsequent abortion were observed at the end of the second month of pregnancy in group II and at the third month of pregnancy in group I. Animals from groups I and II were slaughtered after abortion and necropsied. Goats from the control group were necropsied at the same time. The main lesions in the aborted goats were focal placentitis with early involution (apoptosis) and placentary coagulation necrosis, acute focal endometritis and vulvo-vaginal petechiae. All aborted fetuses were underdeveloped when compared to control fetuses, probably due to fetal malnutrition, since no congenital malformations could be noted. The majority of aborted fetuses showed some degree of autolysis, as fetal death occurred five and three days before abortion, in groups I and II, respectively. The most remarkable fetal lesions were focal or diffuse hemorrhages in the skin, meninges and visceral serosae.

Keywords: Goat, abortion, Tetrapterys multiglandulosa, intoxication

RESUMO

Com o objetivo de investigar a toxicidade da Tetrapterys multiglandulosa A. Juss. foram utilizadas 15 cabras gestantes, divididas aleatoriamente em três grupos (GI, GII e GIII) com cinco animais cada. Após estabelecer o diagnóstico de gestação no tempo médio de 35 dias, eram oferecidas diariamente doses de 10 e 20g/kg PV das folhas (jovens e maduras) de Tetrapterys multiglandulosa para os grupos I e II, respectivamente, junto ao capim picado, feno e concentrado. Para o grupo III, usado como controle, foram fornecidos somente capim picado, feno e concentrado. Todos os animais foram submetidos a exames clínicos diários e a ultra-sonografia a cada três dias. Foi detectada por ultra-sonografia morte fetal e, ao exame clínico, presença de secreção vaginal com subseqüente aborto. Os animais dos grupos I e II (tradados) abortaram no terceiro e no final do segundo mês de gestação, respectivamente, e juntos com os do grupo III (controle) foram sacrificados e submetidos a exames anátomo-histopatológicos. Pela histopatologia observou-se placentite focal com grande quantidade de células trofoblásticas binucleadas em apoptose, além de endometrite focal aguda e petéquias vulvo-vaginais. Todos os fetos abortados estavam subdesenvolvidos quando comparados com os fetos do grupo III (controle) devido à malnutrição, pois nenhum defeito congênito pôde ser notado. Vários fetos abortados mostravam alguma autólise, pois sua morte precedia em cinco e três dias o aborto, nos tratamentos I e II, respectivamente. As lesões fetais observadas foram hemorragias difusas ou focais na pele, meninges e serosa visceral.

Palavras chave: Cabra, aborto, Tetrapterys multiglandulosa, intoxicação

INTRODUCTION

Considering the great extensions of natural pastures in Brazil and the way they are used, it is expected that feeding intoxication may be common in animal husbandry. It is difficult to determine the real impact caused by toxic plants and it is almost impossible to establish the economical losses they cause. The losses may be not only direct, represented by deaths, reproductive disturbs (such as abortion and teratogenic alterations) and tissue lesions, but also indirect, such as decrease in production and the high costs due to control and prophylactic measures (Melo, 1998).

Ateleia glazioviana is responsible for a high number of abortions in cattle and probably in sheep, goats and horses (Gava, 1993). Gutierrezia spp. cause abortion in sheep and cattle and premature birth of calves (Dollahite & Allen, 1959; Dollahite et al., 1962; Roitman et al., 1996). Panter et al. (1987) observed alterations in placenta and fetal death, followed by abortion, in pregnant sheep fed with Astragalus spp. Pinus ponderosa, P. radiata and P. cubensis cause abortion in cattle when ingested particularly during the final three months of pregnancy. Other problems have also been reported such as retention of fetal annexa, pyometra, septicemic metritis, toxemia and death (Stevenson et al., 1972; Stuart et al., 1989).

The Malpighiaceae family is found especially in the tropical Americas. Amongst the 850 known species, approximately 350 are found in the Brazilian territory. Among them, Tetrapterys multiglandulosa is found in the States of Minas Gerais (Mamede, 1987), Rio de Janeiro, São Paulo and Espírito Santo (Tokarnia et al., 1989). In those states T. multiglandulosa and T. acutifolia had been reported as a cause of abortion and degeneration, necrosis and fibrosis of the heart in cattle (Tokarnia et al., 1989).

Due to the lack of scientific studies regarding abortions caused by Tetrapterys multiglandulosa in ruminants, the present paper had the objective to study experimentally the effect of fresh green leaves of this plant fed to pregnant goats.

MATERIALS AND METHODS

Green leaves of T. multiglandulosa were collected from an experimental field of toxic plants (Escola de Veterinária da Universidade Federal de Minas Gerais-UFMG). Fifteen female domestic goats (Capra hircus), Saanen breed, from two to three-year-old and mean body weight of 38kg were used. Prior to the experiment the animals were weighted, treated with levamisol (Vermitrat G5% - Minas Agrovet) (7.5 ml/kg live weight), coccidiostatic (Baycox - Bayer S. A.) (0.8 ml/kg live weight), and dipped with amitraz (Amitracid – Químio Divisão Veterinária) (20ml/10 liters of water). They also received a vitaminic supplement (ADE – Pfizer) (5ml, intramuscularly).

Serological tests for CAE (caprine arthitisncephalitis brucelosis and leptospirosis were carried out in order to eliminate any reagent animal. All animals were vaccinated against foot and mouth disease (Campivac – Ministério da Agricultura) (these vaccines were kindly donated by the Instituto Mineiro de Agropecuária - IMA) and against black leg (Polivacina Valleé – Valleé).

Initially the goats were maintained on a star grass pasture (Cynodon plectostachium), where they received elephant grass (Penisetum purpureum), balanced ration, hay, and mineral salt.

Estrus was induced by an intramuscular injection of 4mg of sodic cloprostenol (Ciosin – Pitman-Moore Brasil Ltda) in order to synchronize the pregnancies. After a period of 24 to 72 hours, all females were exposed to a teasing buck for detection of heat. Females that did not come into heat received a second dose of sodic cloprostenol, 10 days after the first dose. They were mated two times, with an interval of 12 hours. Goats were then weekly submitted to ultrasonography for pregnancy diagnosis, confirmed by fetal heartbeat (at or after 35 days of pregnancy).

After confirm the pregnancy, the animals were individually numbered, housed in individual pens and randomly distributed in three groups as follows: group I - five goats received daily 10g/kg BW of fresh green leaves of T. multiglandulosa; group II - five goats received daily 20g/kg BW of fresh green leaves of T. multiglandulosa; group III - five goats used as controls did not receive the plant.

All animals were daily inspected for general condition, behavior, walking and any body alteration, such as edema and vaginal secretions. Clinical examination included rectal temperature, inspection of conjuctival, gingival and vaginal mucosae, heart beat, auscultation of trachea and lungs, number of respiratory movements, odor and simmetry of exhaled air, rib palpation, ruminal and abdominal movements, and examination of the buccal cavity, lymphonodes and reproductive system (mammary gland and vulva).

Immediately after abortion, fetuses were measured based on Jainudeen & Hafez (1982) method, and submitted to necropsy. Samples were collected from heart, liver, lungs, kidneys, brain and bones. On the same day, the females were sacrificed with electric shock and submitted to necropsy for macroscopic examination. Samples from heart, lungs, spleen, kidneys, liver, rumen, omasum, abomasum, intestine, brain, ovaries, uterus and placentoma were collected for histologic examination.

Animals from group III (control) were submitted to necropsy at different gestational periods, corresponding to the abortions occurred in groups I and II.

Tissue fragments were fixed with a 10% formalin buffered solution. After two hours they were standard sliced to allow fixation. After 24 hours in the formalin solution the fragments were transferred to flasks containing ethyl alcohol (70%), where they were left until being embedded in paraffin, sectioned at 6mm, and stained by hematoxilin/eosin (Luna, 1968).

RESULTS

All animals in all groups showed normal body temperature, breathing and ruminal movements; however heart beats were significantly lower in animals in groups I (10g/kg) and II (20g/kg) after ingestion of T. multiglandulosa. No alterations, regarding skin, mucosae, lymphonodes, and digestive, urinary and circulatory systems were observed during the experimental period.

Fetal deaths, detected by ultrasonography, and vulvar catarrhal discharge were observed in all treated goats. They occurred at the third month of pregnancy in group I, and at the end of the second month of pregnancy in group II (Table 1). Four goats from group I aborted five days after fetal deaths. The other goat aborted a mummified fetus 14 days after fetal death. The five goats from group II aborted three days after fetal deaths (Table 1). No clinical signs were observed in group III. In animals from groups I and II, the abortion was also characterized by weak uterine contractions, except in goat2 from group I, that presented intense uterine contractions for two days before the abortion.

At necropsies, no alterations were observed in animals from group III. Minor macroscopic lesions, such as petechial hemorrhages in the mitral valve of one animal and a small cyst in the tricuspid valve in another, were observed in the heart of goats from group I. Three goats from group I showed lesions in the lungs. Goat 1 had adherences (8 and 5cm in diameter) between the diaphragmatic lobe of the right lung and the diaphragm (8cm in diameter), and between the parietal coastal pleura and the diaphragm (5cm in diameter). Goat 2 had an adherence (3cm in diameter) between the final portion of the apical right lobe and the parietal pleura. A cyst and grey areas, with approximately 2cm in diameter and firm consistency, were observed in the right diaphragmatic lobus in goat 3. Adherence between the lateral right and the parietal lobe and the mediastinum were observed in the liver of animals 1 and 2 from group I. Goat 8, from group II (20g/kg) showed an area of hemorrhage (4cm by 1cm) in the surface of the kidney cortex.

The alterations observed in the reproductive system and fetal annexa are summarized in Table 2.

Microscopic examination showed that all animals in groups I (10g/kg) and II (20g/kg) had corpus luteum at an initial stage of involution in ovaries, with vasoconstriction.

All animals from groups I and II had placentitis with inflammatory infiltration, predominantly polymorphonuclear (neutrophils), few macrophages and high quantity of binuclear cells with acidophilus cytoplasm and dense chromatin in the nucleus. Additionally, areas of coagulation necrosis were observed in several segments of the caruncula. Adenomyosis was observed in the uterus of two animals (numbers 2 and 5) from group I. Other two animals (numbers 1 and 5) from the same group had areas of mineralization, and acute focal endometritis characterized by periglandular inflammatory polymorphonuclear cells and edema in the endometrium. Areas of coagulation necrosis with discrete infiltration of polymorphonuclear and mononuclear cells were observed in the uterus of goats from group II (20g/kg). Only one goat (number 6) had discrete adenomyosis and mucous hypersecrection in the luminal surface.

Goats from group III (control) had the ovary and the uterus morphologically normal. It is important to note that rare trophoblastic binuclear cells were observed in apoptosis, apparently in less extension than in animals from groups I and II.

Regarding the liver, only goat number 1 (group I) showed little proliferation of the biliary ducts, with discrete mononuclear (lymphocytes and macrophages) infiltration. The central cells were pale and many epithelial cells of large ducts showed eosinophilic hyalin inclusions, located at the basis of the epithelium. On the other hand, goat number 2 (group I) had a discrete infiltration of lymphocytes and macrophages in the portal triads. It is important to stress that goat number 1 ingested T. multiglandulosa during a longer period (10 weeks). No significant lesions were observed in the other tissues examined microscopically.

Autolysis was observed in the fetuses from goats in groups I and II. Liver congestion was observed in the fetus from goat 4 (group I), and petechial hemorrhages were seem in lungs in the fetus from goat 6 (group II). Other macroscopic observations in fetuses from the three groups are presented in Table 3. All fetuses from groups I and II were smaller than the size proposed by Sivachelvan et al. (1996). In contrast, the fetuses from group III (control) had sizes within the standard measures suggested by Mialot et al. (1991) and Sivachelvan et al. (1996).

DISCUSSION

The observed results allowed the conclusion that T. multiglandulosa is abortive for goats, causing up to 100% of abortion. A large number of plants including Gutierrezia spp. (Dollahite & Allen, 1959; Dollahite et al., 1962), Pinus ponderosa (James et al., 1967; Stevenson et al., 1972) and Astragalus spp. (Panter et al., 1992) have been reported as cause of abortion in sheep and cattle. Other plants, such as Juniperus utahensis and Chrysothammus nauseosus, also cause abortion, but are ingested only in situations of extreme starvation (James et al., 1992). In Brazil T. multiglandulosa and T. acutifolia had been reported as a cause of abortion in cattle in the states of São Paulo, Rio de Janeiro, Espírito Santo and Minas Gerais (Tokarnia et al., 1989). Ateleia glazioviana causes abortion in ruminants and probably in horses in Santa Catarina and Rio Grande do Sul. The intoxication occurs when the animals ingest green leaves or leaves felt in the ground during autumn and winter (Gava, 1993). Outbreaks of abortion had been reported in cattle after the ingestion of the fruits of Enterolobium spp .and Stryphnodendrom spp. (Tokarnia et al., 2000).

T. multiglandulosa, when mature, does not have good palatability due to the presence of condensed tannins. However, the young leaves present good palatability and are well ingested. Normally the animals ingest the T. multiglandulosa during the dry season, when pasture is poor but the plant is preserved green (Tokarnia et al., 1989).

T. multiglandulosa has probably a toxic component, which results in fetal death with subsequent abortion. James et al. (1967) studying the intoxication with Astragalus spp. and Binns et al. (1963) studying the intoxication with Veratrum californicum also reported fetal death and subsequent abortion. James et al. (1967, 1969) observed macerated fetuses after intoxication with Astragalus pubentissimus. According to Panter et al. (1987), the fetal death induces the synthesis of cotyledonary prostaglandin, resulting in abortion. Ellis et al. (1985) reported significant higher concentrations of prostaglandin (alpha PGF1, alpha PGF2 and PGE) in sheep with dead fetuses than in those with live fetus.

According to Stuart et al. (1989), pregnant cows ingesting Pinus ponderosa present initially vulvar edema and uterine discharge with mucus and bloody aspect. Similar findings were observed in all animals in groups I and II, and goat 1 (group I) had hyperemia of the vulvar mucosa. According to Panter et al. (1992), the abortion caused by Pinus is characterized by weak uterine contractions, incomplete cervical dilatation and excessive uterine hemorrhage with mucus, occurring one day to one week or more after the plant ingestion. Weak uterine contractions were also observed in goats from groups I and II, except in goat2 from group I, that presented intense uterine contractions for two days before the abortion.

Regarding the period of exposition to T. multiglandulosa, animals in group I aborted 42-45 days after the beginning of the ingestion; one exception was goat 1 that aborted a mummified fetus after a exposition period of 73 days. On the other hand, animals in group II aborted 17-24 days after the beginning of ingestion of T. multiglandulosa. These variations of time are probably related to the doses offered. Fetal deaths resulting in abortions during the medium and final gestation are also reported in sheep ingesting Veratrum californicum (Binns et al., 1963).

All goats from groups I and II presented alterations in the genital system and fetal annexa, which were characterized mainly by edema and petechial hemorrhages in the vulvar, vaginal and endometrial mucosae, as well as mucous bloody exudation. These facts indicate that T. multiglandulosa, given at the doses of 10 and 20 g/kg to goats, results in a deleterious effect in placenta and fetal annexa. Similar lesions were reported by Stuart et al. (1989).

All animals from groups I and II presented focus of coagulation necrosis in the maternal placenta (caruncula), and/or apoptosis of binuclear cells in the trophoblast (cotyledon), with variable extension from moderate to intense. It is known that the placenta is responsible for exchanging components between mother and fetus during pregnancy, with several functions, such as nutrition and respiration (King et al., 1982). In addition, accumulation of binuclear cells is needed for the formation of sincicium (Wimsatt, 1951; Wooding, 1980; Wathes & Wooding, 1981; Wooding & Staples, 1981). The maternal epithelium suffers alterations during pregnancy, particularly at late gestation (Marques Júnior, 1988; Barreto Filho, 1992), although without necrosis or cellular apoptosis, as observed in groups I and II, at mid gestation. Possibly, these alterations compromise the normal functions of the placenta. The trophoblastic epithelium, which is surrounded by binuclear cells (Lawn et al., 1969; Wooding, 1980), also suffers modifications (Hamilton et al., 1960), occurring its decrease during pregnancy (Williams et al., 1987). These results are in agreement with the findings described by Wooding et al. (1986), who observed a decrease of binuclear cells in dead fetuses, and the results from Jensen et al. (1989), who also observed decrease of these cells during intoxication with Pinus ponderosa.

The binuclear cells have the goat placentary lactogen (gPL) inside their granules, which diminishes after fetal death, indicating that the live fetus is essential for the secretion of gPL (Taylor et al., 1983). Hurtley et al. (1977) apud Taylor et al. (1983) reaffirm that the placentary lactogen is important for fetal growth. This could possible explain the relationship between the decrease of binuclear cells and the concomitant decrease in fetal size, observed in fetuses from groups I and II. In contrast, Thorburn et al. (1977) suggest that the placentary lactogen is responsible for the regulation of delivery, partially controlling the liberation of prostaglandin by the uterus. During the last weeks of pregnancy sheep have a decrease of placentary lactogen associated to a decrease in the number of binuclear cells (Wooding et al., 1986). These observations support the hyphotesis that decrease of binuclear cells in groups I and II, with possible decrease of the placentary lactogen, indicate the beginning of uterus contractions, initiating the mechanism of abortion.

The placentary lesions do not allow the fetus to receive all nutrients needed for its development, due to a vascular regression and coagulation necrosis of the supportive conjunctive tissue (Van Remsburg et al., 1971). The findings of placentary necrosis with polymorphonuclear and mononuclear infiltration in groups I and II were similar to the ones observed by Stuart et al. (1989) in Pinus ponderosa intoxication.

Although it is known that apoptosis is due to a physiological or pathological stimulus, and that necrosis is a pathological phenomenon (Vasconcelos & Vasconcelos, 1995), it is believed that the apoptosis observed in groups I and II could be due to toxins, according to reports by Gerschenson & Rotello (1992).

Despite the fact that animals in groups I and II presented a significant decrease of heart beat at clinical examination, no macroscopic lesions were observed in the circulatory system, that could justify this decrease. Thus, ingestion of T. multiglandulosa by pregnant goats at the doses of 10 and 20g/kg, during six and two weeks respectively, does not cause macroscopic and microscopic heart alterations, differently from what has been observed in cattle (Tokarnia et al., 1989).

The presence of eosinophilic hyalin inclusions in epithelial cells of large ducts observed in the liver from goat 2 is probably related to toxic metabolic residues from the plant as reported by King (1997, personal communication) (King, J. Personal communication. 1997. New York State College of Veterinary Medicine, Departament of Pathology, Ithaca, New York, USA.). This goat ingested T. multiglandulosa for 10 weeks, in contrast with the other goats from the same group that ingested the plant for six weeks.

All aborted fetuses were underdeveloped when compared to control fetuses, probably due to fetal malnutrition, since no congenital malformations could be noted. Congenital malformation and abortion are seen in the intoxications by Veratrum californicum (Binns et al., 1963; Van Kampen et al., 1969; Keeler & Stuart, 1987; Keeler et al., 1985), Astragalus pubentissimus (James et al., 1969), Conium maculatum, Nicotiana glauca and Lupinus formosus (Keeler & Balls, 1978, Panter et al., 1990a,b; James et al., 1992).

CONCLUSIONS

The experimental intoxication of pregnant goats with Tetrapterys multiglandulosa at doses of 10 and 20g/kg BW causes decrease of heart beats detectable at clinical examination, fetal dead and abortion, and placentary coagulation necrosis and apoptosis of binuclear cells in the trophoblastic epithelium.

• BARRETO FILHO, J.B. Aspectos morfofisiológicos da placentaçăo do zebu (Bos taurus indicus). Belo Horizonte: Escola de Veterinária da UFMG, 1992. 106p. (Dissertaçăo, Mestrado.)
• BINNS, W., JAMES, L.F., SHUPE, J.L. A congenital cyclopian-type malformation in lambs induced by maternal ingestion a range plant Veratrum californicum Am. J. Vet. Res, v.24, p.1164-1175, 1963.
• DOLLAHITE, J.W., ALLEN, T.J. Feeding perennial broomweed to cattle, swine, sheep, goats, rabbits, guinea pigs and chickens. Tex. Agric. Exper. Stat. Prog. Rep., p.2105, 1959.
• DOLLAHITE, J.W., SHAVER, T., CAMP, B.J. Injected saponins as abortifacients. Am. J. Vet. Res., v.23, p.1261-1263, 1962.
• ELLIS, L.C., JAMES, L.F., MCMIILLEN, R.W. et al. Reduced progesterone and altered cotyledonary prostaglandin values induced by locoweed (Astragalus lentiginosus) in sheep. Am. J. Vet. Res., v.46, p.1903-1907, 1985.
• GAVA, A. Intoxicaçăo por Ateleia glazioviana. IN: RIET-CORREA, F., MÉNDEZ, M.C., SCHILD, A.L. Intoxicaçăo por plantas e micotoxinas em animais domésticos Pelotas: Hemisfério Sul do Brasil, 1993. v.1, p.222-225.
• GERSCHENSON, L.E., ROTELLO, R.J. Apoptosis: A different type of cell death. Faseb. J., v.3, p.2450-2455, 1992.
• HAMILTON, W.J., HARRISON, R.J., YOUNG, B.A. Aspects of placentation in certain cervidae. J. Anat., v.94, p. 1-33, 1960.
• JAINUDEEN, M.R., HAFEZ, E.S.E. Gestaçăo fisiologia pré-natal e parto. IN: HAFEZ, E.S.E. Reproduçăo Animal, 4.ed, Săo Paulo: Manole, p.280-321, 1982.
• JAMES, L.F., KEELER, R.F., BINNS, W. Sequence in the abortive and teratogenic effects of locoweed fed sheep. Am. J. Vet. Res., v.30, p.377-380, 1969.
• JAMES, L.F., PANTER, K.E., NIELSEN, D.B. et al. The effect of natural toxins on reproduction in livestock. J. Anim. Sci., v.70, p.1573-1579, 1992.
• JAMES, L.F., SHUPE, J.L., BINNS, W. et al. Abortive and teratogenic effects of locoweed on sheep and cattle. Am. J. Vet. Res, v.28, p.1379-1388, 1967.
• JENSEN, PIER, A.C., KALTENBACH, C.C., MURDOCH, W. et al. Evaluation of histopathologic and physiologic changes in cows having premature births after consuming Ponderosa pine needles. Am. J. Vet. Res., v.50, p.285 -289, 1989.
• KEELER, R.F., STUART, L.D. The nature of congenital limb defects induced in lambs by maternal ingestion of Veratrum californicum Clin. Toxicol., v.25, p.273-286, 1987.
• KEELER, R.F., YOUNG, S., SMART, R. Congenital tracheal stenosis in lambs induced by maternal ingestion of Veratrum californicum Teratology, v.31, p.83-88, 1985.
• KING, G.J., ATHINSON, B.A., ROBERTSON, H.A. Implantation and early placentation in domestic ungulates. J. Reprod. Fert., Suppl., v.31, p.17-30, 1982.
• LAWN, A.M., CHIQUOINE, A.D., AMOROSO, E.C. The development of the placenta in the sheep and goat: an electron microscope study. J. Anat, v.105, p.557-578, 1969.
• LUNA, L.G. Manual of histologic staining methods of the Armed Forces Institute of Pathology, 3.ed, New York: Mcgraw Hill., 1968.
• MAMEDE, M.C.H. Flora da Serra do Cipó, Minas Gerais, Malpighiaceae. Bol. Bot., v.9, p.157-198, 1987.
• MARQUES JUNIOR, A.P. Leucocyte chemotaxis activity by cotiledons of dairy cows with normal delivery and retained placenta Urbana: University of Illinois, 1988. (PhD, Thesis).
• MELO, M.M. Plantas tóxicas para bovinos. Cad. Téc. Esc. Vet. UFMG, n.24, p.5-52, 1998.
• PANTER, K.E., BUNCH, T.D., JAMES, L.F. et al. Ultrasonographic imaging to monitor fetal and placenta developments in ewes fed locoweed (Astragallus lentiginosus). Am. J.Vet. Res, v.48, p.686-690, 1987.
• PANTER, K.E., JAMES, L.F., MOLYNEUX, R.J. Ponderosa pine needle-induced parturition in cattle. J. Anim. Sci., v.70, p.1604-1608, 1992.
• PANTER, K.E., KEELER, R.F., BUNCH, T.D. et al. Congenital skeletal malformations and cleft palate induced in goats by ingestion of Lupinus, Conium and Nicotiana species. Toxicon, v.28, p.1377, 1990a.
• PANTER, K.E., KEELER, R.F., BUNCH, T.D. et al. Multiple congenital contractures (MCC) and cleft palate induced in goats by ingestion of piperidine alkaloid-containing plants. Reduction in fetal movement as the problem cause. Clin. Toxicol, v.28, p.69, 1990b.
• ROITMAN, J.N., JAMES, L.P., PANTER, K.E. Constituents of broom snakeweed (Gutierrezia sarothae) an abortifacient rangeland plant. In: COLEGATE, S.M., DORLING, P.R., Plant-associates Toxins. Agricultural, Phytochemical & Ecological Aspects s.d., 1996. p.345-350.
• STEVENSON, A.H., JAMES, L.F., CALL, J.W. Pine needle (Pinus ponderosa) induced abortion in range cattle. Cornell Vet., v.62, p.519, 1972.
• STUART, L.D., JAMES, L.F., PANTER, K.E. et al. Pine needle abortion in cattle: pathological observations. Cornell Vet, v.19, p.61-69, 1989.
• TAYLOR, M.J., JENKIN, G., ROBINSON, J.S. et al. Effect of intrauterine death and fetectomy on ovine placental lactogen production. Res. Vet. Sci., v.35, p.22-24, 1983.
• THORBURN, G.D., CHALLIS, J.R.C., CURRIE, W.B. Control of parturition in domestic animals. Biol. Reprod., v.16, p.18, 1977.
• TOKARNIA, C.H., PEIXOTO, P.V., DOBEREINER, J. et al. Tetrapterys spp. (Malpighiaceae), a causa de mortandades em bovinos caracterizadas por alteraçőes cardíacas. Pesq. Vet. Bras., v.9, p.23-44, 1989.
• TOKARNIA, C.H., DOBEREINER, J., PEIXOTO, P.V. Plantas tóxicas do Brasil. Helianthus, Rio de Janeiro, 2000. 310p.
• VAN KAMPEN, K.R., BINNS, W., JAMES, L.F. et al. Early embryonic death in ewes given Veratrum californicum Am. J. Vet. Res, v.30, p.517-519, 1969.
• VAN REMSBURG, S.J. Malnutrition of fetus as a cause of abortion. Afr. Vet. Med. Ass, v.42, p.305-308, 1971.
• VASCONCELOS, A.C., VASCONCELOS, M.M.A. Apoptose ou morte celular programada. Um novo conceito em patologia. Rev. Med. Minas Gerais, v.5, p.103-108, 1995.
• WATHES, D.C., WOODING, F.B.P. An electron microscopic study of implantation in the cow. Am. J. Anat., v.159, p.285-306, 1981.
• WILLIAMS, W.F., MARGOLIS, M.J., MANSPEAKER, J. et al. Peripartum changes in the bovine placenta related to fetal membrane retention. Theriogenology, v.28, p.211-223, 1987.
• WIMSATT, W.A. Observations on the morphogenesis, cytochemistry and significance of the binucleate giant cells of the placenta of ruminants. Am. J. Anat, v.89, p.233-282, 1951.
• WOODING, F.B.P. Electron microscopic localization of binucleate cells in sheep placenta using phosphotungstic acid. Biol. Reprod., v.22, p.357-365, 1980.
• WOODING, F.B.P., FLINT, A.P.F., HEAP, R.B. et al. Control of binucleate cell migration in the placenta of sheep and goats. J. Reprod. Fertil, v.76, p.499-512, 1986.
• WOODING, F.B.P., STAPLES, L.D. Functions of trophoblast papillae and binucleate cells in implantation in sheep. J. Anat., v.13, p.110-112, 1981.

Publication Dates

• Publication in this collection
  26 June 2001
• Date of issue
  Feb 2001

History

• Received
  26 Oct 2000