Veterinary Pathology Online

http://vet.sagepub.com/ Leptospirosis in Equine Fetuses, Stillborn Foals, and Placentas

K. B. Poonacha, J. M. Donahue, R. C. Giles, C. B. Hong, M. B. Petrites-Murphy, B. J. Smith, T. W. Swerczek, R. R. Tramontin and P. A. Tuttle Vet Pathol 1993 30: 362 DOI: 10.1177/030098589303000405 The online version of this article can be found at: http://vet.sagepub.com/content/30/4/362

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Vet Pathol30:362-369 (1993)

Leptospirosis in Equine Fetuses, Stillborn Foals, and Placentas

K. B. POONACHA,M. DONAHUE, C. GILES, B. HONG, J. R. C. M. B. PETRITES-MURPHY, SMITH, W. SWERCZEK, B. J. T. R. R. TRAMONTIN, P. A. TUTTLE AND
Livestock Disease Diagnostic Center, Department of Veterinary Science, College of Agriculture, University of Kentucky, Lexington, KY

Abstract. Leptospirosis was diagnosed in 5 1 equine fetuses and 16 stillborn foals with gestational ages from 3% to 11 months. Diagnosis was based on one or more of the following: positive fetal antibody titer, positive fluorescent antibody test, demonstration of spirochetes in kidney and/or placental sections stained by the Warthin-Starry technique, high leptospiral titers in aborting mares, or isolation of Leptospira spp. from fetal organs. Gross lesions were observed in 80.3% of the fetuses, stillborn foals, and placentas. Gross placental lesions included nodular cystic allantoic masses, edema, areas of necrosis of the chorion, and necrotic mucoid exudate coating the chorion. The liver (23 cases) was enlarged, mottled, and pale to yellow. The kidneys (seven cases) were swollen and edematous with pale white radiating streaks in cortex and medulla. Microscopic lesions were observed in 96% of fetuses, stillborn foals, and placentas. Placental lesions consisted of thrombosis, vasculitis, mixed inflammatory cell infiltration of the stroma and villi, cystic adenomatous hyperplasia of allantoic epithelium, and villous necrosis and calcification. Fetal lesions included hepatocellular dissociation, mixed leukocytic infiltration of the portal triads, giant cell hepatopathy, suppurative and nonsuppurative nephritis, pulmonary hemorrhages, pneumonia, and myocarditis. Spirochetes were demonstrated with the Warthin-Starry stain in the allantochorion and/or kidney of 69 of the 7 1 cases. Using the direct fluorescent antibody technique, 56/60 cases tested positively for leptospires. Leptospires were isolated from fetal tissues in 20/42 cases. Sixteen of the isolates were identified by restriction enzyme analysis as Leptospira interrogans serogroup Pomona serovar kennewicki; case Nos. 36 and 41 were serovar grippotyphosa. The other two isolates were not identified. Microagglutination titers against leptospires were demonstrated in the body fluid of 47/67 cases tested and titers ranged from 1 : 50 to greater than 1 : 1,638,400 against Leptospira interrogans serovars pomona, grippotyphosa, copenhageni, hardjo, canicola, and bratislava. Sixty-two of 7 1 aborting mares tested had titers ranging from 200 to greater than 3,276,800. Leptospiral antibody titers in the body fluid and gross and histopathologic lesions did not differ with age, breed, or sex or between fetuses and stillborn foals.

Key words: Abortion; equine fetus; horses; leptospirosis; placenta.

Serovars of Leptospira interrogans cause abortion, stillbirth, and the birth of weak offspringin cattle, sheep, 1~12~13,20,22,33 There have been several reports and of abortion, stillbirth, and premature live birth in horses due to leptospiral infection.1,6.9.10,14,17-19,24-26,34.36.38,39 Serogroup Pomona was involved in the majority of such cases.1,'0,'4,*7,'9,34,36 serogroupswere also isoOther lated from affected f e t u ~ e s . ~ J O J ~ > ~ ~ Seroepidemiologic studies in several countries, including the United States, have revealed that horses have antibodies against a wide range of leptospiral serovars.3.5.'5.'6.21~2s,31,37 This paper describes the pathologic findings in 71 cases of equine abortions (5 5 cases) and stillbirths (1 6 cases) from horses infected with leptospires. The results of immunofluorescent studies, fetal and maternal

serologic tests, and isolation attempts are also discussed.

Materials and Methods
Between February 1986 and March 1991, specimens from 2,945 equine abortion cases were submitted to the Livestock Disease Diagnostic Center in Lexington, Kentucky (USA). The specimens consisted of stillborn foals (678), placentas (295), and foals and their placentas (1,972). Gross, histopathologic, serologic, and microbiologic examinations were performed on each case. Gross lesions were recorded and samples were collected for microbiologic and serologic examination. Kidney, liver, lung, heart, brain, lymph node, intestine, spleen, thymus, and placenta were fixed in 10% neutral buffered formalin for

362

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Table 1. Age and breed of 7 1 cases of equine abortion and stillbirth due to leptospirosis.
Breed Age of Gestation (Days)
< 179

180-2 19

220-259

260-299

>300

Total

Thoroughbred Standardbred Saddlebred Quarter Horse Miniature Horse Tennessee Walker Arabian Total

12 1

I 1 0 0 0

21 2

15

0 0 1 1 0 25

0 0 0 1 14

11 1 1

0 0 0 0 0 16

15 I

60 5 2
1

1 1
1

71

histopathologic examination. The sections were trimmed, dehydrated in alcohol, embedded in paraffin, sectioned at 6 pm, and stained with hematoxylin and eosin. In addition, sections of kidney, placenta, and/or liver from cases diagnosed as leptospirosis by serologic testing and/or immunofluorescent microscopic examination were stained by the Warthin-Starry method for spirochetes. Heart blood and pericardial fluid from all fetuses and stillborn foals and blood from the aborting mares were collected and tested for leptospiral antibodies by the microscopic agglutination test (MAT) at 1 : 50 against antigens of Leptospira interrogans serovars pomona, canicola, copenhageni (representative of Icterohaemorrhagiae serogroup), grippotyphosa, hardjo, and brati~lava.~ Aerobic cultures of representative organs (liver, lung, and placenta) and stomach content and immunofluorescent examination of liver, lung, spleen, and thymus for equine herpes I were performed. Stomach contents were examined for spirochetes by darkfield microscopy. Direct fluorescent antibody tests (DFAT) for leptospiral organisms were performed on kidney and placenta of 1,570 cases (53.3O/0)..~ Culture for leptospiral organisms was attempted on fetal liver and kidney that were positive by DFAT or Because Table 2. Summary of findings in aborted equine fetuses and stillborn foals including placentas evaluated for evidence of leptospiral infection.
HistoPositive FluoLeptorescent rescent spires Anti- Antibody Isolated body Test Titers Positive Flue-

of heavy contamination, the placenta was not cultured for leptospires.

Results Leptospirosis was diagnosed in 71 aborted equine fetuses (55 cases) and stillborn foals (16 cases) with gestational ages from 3 /2 months to term (Tables 1,2). The diagnosis was based on one or more of the following: positive fetal antibody titer, positive florescent antibody test, demonstration of spirochetes in kidney and/or placental sections stained by the Warthin-Starry technique, high leptospiral titers in aborting mares, or isolation of Leptospiru spp. from fetal organs.
Gross pathologic findings

Gross lesions were noted in 57 of these 71 cases (80.3%), comprising 38 fetuses and 40 placentas. Fourteen fetuses (case Nos. 2,4, 6, 7, 9, 10, 24, 27, 29, 32, 39-41, 59) were emaciated. The remaining 15 cases did not reveal any gross lesions.

Year

Number ~ r o s s pathonosed Lesions Dag-

z&,
1 4 14 36 6 7 68

986 987 988 1989 1990 1991 Total

4 14 38 7 7 71

1 3 11 30 6 6 57

NA* 4 11 27 2 3 47

NA NA

8t 35 6 7 56

NA 1 NA 12 2 5

20
Fig. 1. Kidney; 296-day-old female Saddlebred fetus No. 24. Cut section shows edema and white radiating streaks.

t Only eight of 14 cases were tested. Fluorescent antibody tests were not performed before May 1988.

* NA = not attempted.

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Table 3. Distribution of histopathologic lesions in various organs in 7 1 cases of aborted equine fetuses and stillborn foals including placentas associated with leptospirosis.
Organs Number of Number of Number (O/O) of Cases with Cases without Cases Not Lesions Examined Lesions

Allantochonon Liver Kidney Lung Amnion Umbilical cord Heart Lymph node Spleen Brain Thymus

58 (95.1) 57 (82.6) 30 (44.8) 17 (34.0) 16 (43.2) 15 (51.7) 9 (15.0) 9 (30.0) 4 (7.5) 2 (4.7) 2 (5.0)

3 12 37 50 21 14 51 21 49 41 38

10 2 4 4 34 42 11 41 18 28 31

Seven fetuses (case Nos. 1, 22-24, 56, 6 1, 70) had lesions in the kidney that consisted of swelling, perirenal edema, and/or white radiating streaks (Fig. l). Twenty-seven fetuses (case Nos. 4, 7, 9, 11, 13, 16, 26, 28, 33, 34, 37, 40, 43, 45, 4 7 4 9 , 53, 54, 56, 57, 60, 62, 65, 69-71) had lesions in the liver. The most common gross lesions were swelling, yellowish discoloration, and mottling. Widespread gross lesions were observed in the allantochorion, amnion, and umbilical cord. Forty of 7 l (56.3%) of the cases with allantochorions had gross lesions that consisted of greenish discoloration of the allantoic surface and nodular cystic allantoic masses. The chorion had multifocal areas of necrosis, was dark red, reddish brown, or tan, and occasionally was coated with a thick layer of reddish brown necrotic mucoid exudate. Five of 38 amniotic membranes had edema, raised circular calcified plaques, and areas of necrosis. Lesions in the umbilical cords (2/33) consisted of ede-

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Fig. 6. Kidney; 300-day-old female Thoroughbred stillborn foal No. 56. Microabscesses and inflammatory cell infiltrates have replaced tubules. HE. Bar = 250 pm. Fig. 7.

Higher magnification of Fig. 6. The microabscesses consist of a collection of neutrophils. HE. Bar

50 p m .

Fig. 8. Kidney; 300-day-old female Thoroughbred stillborn foal No. 56. Langhans multinucleated giant cells scattered among inflammatory cells. HE. Bar = 25 pm. Fig. 9. Heart; 240-day-old female Thoroughbred fetus No. 34. The myocardium is focally infiltrated with mixed inflammatory cells. HE. Bar = 50 pm.
t

Fig. 2. Liver; 2 10-day-old female Thoroughbred fetus No. 3 1. Many multinucleated giant hepatocytes are scattered throughout the hepatic parenchyma. HE. Bar = 25 pm.
=

Fig. 3. Liver; 240-day-old female Thoroughbred fetus No. 53. Note severe diffuse dissociation of hepatocytes. HE. Bar 50 pm.

Fig. 4. Liver; 328-day-old female Arabian stillborn foal No. 60. Note portal area infiltrated by mixed leukocytes. HE. Bar = 25 pm. Fig. 5. Kidney; 300-day-old female Thoroughbred stillborn foal No. 56. Focal interstitial nephritis with infiltration of lymphocytes and plasma cells between dilated tubules. HE. Bar = 50 pm.

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Fig. 10. Allantochorion; 240-day-old male Thoroughbred fetus No. 54. Note multiple, variously sized, cystic and hyperplastic allantoic epithelium with secretion and cellular infiltration. HE. Bar = 250 pm.

ma, multiple sacculations filled with fluid, and coating of the surface with a fibrinous exudate. Four of 67 fetal lungs were hemorrhagic and consolidated.
Histopathologic findings

Histopathologic examination revealed lesions in 96% of the 71 fetuses and/or placentas (Table 3). Liver. Fifty-seven of 69 cases (82.6%) had lesions in the liver. There were 39 cases with mild to moderate, multifocal portal and perivascular mixed leukocytic infiltration, 19 cases with hepatocellular dissociation, and 28 cases with a few to many giant hepatocytes (Figs. 2-4). Giant hepatocytes were binucleated, trinucleated, and multinucleated types with abundant cytoplasm. Other lesions in the liver included hepatocellular vacuolar degeneration, focal to multifocal fibrosis, individual hepatocyte and Kuppfer cell necrosis, intrahepatic bile stasis, fibrin within the blood vessels, subcapsular hemorrhages, and occasionally multiple necrotic foci. In two cases, the liver was not examined. Kidney. In 30 of 67 cases (44.8%; 21 fetuses and nine stillborn foals), the kidneys had microscopic lesions, which consisted of multiple focally extensive microabscesses with a few to several multinucleated giant cells (case Nos. 1, 6, 22, 24, 26, 56, 70), dilated tubules (case Nos. 1-3, 7, 12, 22, 23, 26, 36, 54, 56, 58, 60, 61), and focal to multifocal nonsuppurative interstitial nephritis (case Nos. 11, 19, 23, 25, 28, 36,

43, 44, 51) (Figs. 5-8). There was one case each of capsular fibrosis (case No. 56), subcapsular and interstitial hemorrhages (case No. 55), and multifocal calcification (case No. 31). Kidneys of 37 cases did not reveal any lesions. In four cases, the kidneys were not examined. Heart. In case Nos. 33, 34, 37, 44, 46, 52, 53, 56, and 57, the lesions consisted of a few multifocal infiltrations of mixed leukocytes in the myocardium (Fig. 9). In 85% of the cases ( 5 1/60), the heart did not have any lesions. In 11 cases, the heart was not examined. Lung. Pulmonary lesions were present in 17/67 cases examined (Nos. 1, 5 , 8, 9, 12, 21, 30, 44, 50, 60, 61, 63,65,66,68,69,7 1) and consisted of various degrees of bronchopneumonia and subpleural, interlobular, and alveolar hemorrhages. The pneumonic changes were mainly minimal to mild focal neutrophilic infiltration. In 50 cases, the lungs did not have any lesions. Brain. Case Nos. 54 and 57 had lesions in the brain, which consisted of mild, focal, nonsuppurative meningoencephalitis. In 28 cases, the brain was not examined. Lymphoid organs. In nine cases (Nos. 10, 12, 19, 22, 24, 34, 46, 67, 71), the lymph nodes had mild lymphoid necrosis and neutrophilic infiltration with reticuloendothelial cells filling the sinuses. Severe capsular hemorrhages and lymphoid necrosis were present in the spleen in four cases (Nos. 5 , 34, 66, 71). The thymus of case Nos. 10 and 7 1 had lymphoid necrosis. Placenta. A wide range of histologic lesions were observed in the allantochorion, amnion, and umbilical cord. Fifty-eight cases (95.1%) had lesions in the allantochorion. The most frequent lesions were hyperplastic, dilated, cystic adenomatous allantoic epithelium (case Nos. 2, 4, 6, 9, 10, 16, 18, 24, 51, 54, 57, 58, 66, 69, 70) and mild to severe, focal to multifocal, or diffuse mixed leukocytic infiltration of stroma and chorionic villi (48 cases) (Figs. 10-12). Vasculitis and vascular thrombosis were also observed in case Nos. 2, 5 , 28, 51, and 54 (Fig. 13). Thirty-six cases had stromal edema, atrophy of the villi, and focal necrosis and calcification of the villi. In ten cases, the allantochorion were not examined. In 16 cases (Nos. 4,9, 11, 22, 24, 28, 30, 31, 34, 37, 50, 53, 5 5 , 63, 66, 67), the amnion had edema, multifocal, mild, neutrophilic infiltration, and necrotic calcified foci with occasional thrombosis of the blood vessels. In 15 cases (Nos. 5 , 11, 18, 19, 21, 22, 31, 34, 42, 46, 50, 53, 55, 63, 69), the umbilical cord had edema, mild to severe and focal to multifocal hemorrhages, inflammatory cell infiltration, and necrotic material coating the surface. Spirochetes were demonstrated with the WarthinStarry stain in the kidney and/or placenta of 69 of the 71 cases (Fig. 14). Lesions characteristic of herpes virus infection were

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Fig. 11. Allantochorion; 240-day-old female Thoroughbred fetus No. 53. Note mild cellular infiltration of the chononic villi. HE. Bar = 250 pm. Fig. 12. Higher magnification of Fig. 11. The chorionic villi are infiltrated by mixed leukocytes. HE. Bar = 50 pm. Fig. 13. Allantochorion; 240-day-old male Thoroughbred fetus No. 54. Note vasculitis and thrombosis with infiltration of mixed leukocytes in the surrounding stroma. HE. Bar = 50 pm. Fig. 14. Allantochorion; 270-day-old female Thoroughbred fetus No. 5 1. Numerous spirochetes are scattered throughout the stroma. Warthin-Starry stain. Bar = 10 pm.

observed in the liver, lung, thymus, spleen, lymph node, more than one serovar in their body fluid and/or heart blood. Antibody titers ranged from 50 to greater than and adrenal gland of one case. 1,638,400. In 22 cases, the fetal body fluid was negative Serologic findings for leptospiral antibodies. Case Nos. 1 and 29 were Leptospiral antibodies were detected in the fluid and/ not tested. A total of 62 of 71 aborting mares were tested for or heart blood of 47 fetuses. Forty had titers against serovar pomona, four against grippotyphosa (case Nos. the presence of leptospiral antibodies. All 62 mares 23, 25, 36, 41), two against bratislava (case Nos. 9, had high antibody titers, which ranged from 1 : 200 to 27), and one against hardjo (case No. 42). Seventy- greater than 3,276,800. Forth-four mares (7 1%) were seven percent (36/47) of seropositive fetuses reacted positive for the same serovars as those found in the to only one serovar. Twenty-three percent (1 1/47) of fetal fluids. Thirty-eight (86.4%) of these mares had serologically positive fetuses had antibody titers against leptospiral antibody titers equal to or greater than those

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in the fetal fluids. Those mares tested also had titers against other serovars.
Microbiologic findings

Leptospires were demonstrated in 56 fetuses by direct fluorescent antibody tests and were isolated from the tissues of 20 of 42 fetuses in which culture was attempted. Sixteen of the isolates were identified by restriction enzyme analysis as serogroup Pomona serovar kennewicki,and case Nos. 36 and 4 1 were serovar grippotyphosa. Bacteria other than leptospires were found in 18 of the 71 fetuses, stillborn foals, and placentas.
Discussion Leptospirosis was diagnosed in 55 aborted fetuses and 16 stillborn foals with gestational ages from 3% months to full term. A diagnosis of leptospiral infection was based on one or more of the following: a positive fetal antibody titer, positive fluorescent antibody test, demonstration of typical spirochetes in kidney and/or placental sections by the Warthin-Starry technique, high leptospiral titers in aborting mares, or isolation of Leptospira spp. from fetal organs. The gross lesions reported in this study are typical of fetal leptospirosis and are consistent with those in previously reported cases in equines and other animals.'OJ7 The kidney lesions described appear to be typical of leptospirosis but have not been previously reported. There were no significant correlations between the fetal emaciation and the extent of placental lesions. Giant cell hepatocytosis was a common finding and has been reported in equine f e t u s e ~and~in cyto~, ~ megalovirus and reovirus infections in human fetuses.27,29,30 report, hepatic giant cell formation was In one thought to be due to leptospiral infection.36Hepatic lesions such as mixed leukocytic infiltration and hepatocellular dissociation have been reported in equine fetuses as due to leptospirosis.17,36 The lesions in the kidney seem to be specific for leptospiral infections. Nonsuppurative interstitial nephritis and tubular dilation have been reported in leptospiral infection.l 7 However, microabscesses in the kidneys of equine fetuses also appear to be specific for leptospiral infections. In these cases, intralesional spirochetes were demonstrated by the Warthin-Starry stain. Spirochetes have not been seen with other infections in the equine fetus. Pulmonary hemorrhages, nonsuppurative myocarditis, and meningoencephalitis appear to be in association with leptospiral infection and have been previously reported.17 The placental lesions such as cystic adenomatous allantoic epithelium, mixed leukocytic infiltration of

stroma and villi, vasculitis, and thrombosis observed in association with leptospiral infection are not unique to leptospirosis but are also seen with other bacterial infections, such as those by Escherichia coli, @-haemolytic Streptococcus, Pseudomonas aeruginosa, Enterobacter agglomerans, and Actinobacillus e q ~ u l i . ~ ~ , ~ ~ Spirochetes were found in 69 of the 7 1 histopathologic specimens of kidney and/or placenta stained by the Warthin-Starry technique. Organisms were most easily found in the tubular lumens of the kidney, stroma, and villi of the allantochorion. In most cases, spirochetes were numerous. These findings were consistent with those of previous r e p ~ r t s . ~ J ~ J ~ , ~ ~ Seventy-seven percent (36/47) of seropositive fetuses reacted to only one serovar. Twenty-three percent had cross reactivity to more than one serovar in the body fluids and/or fetal heart blood. These findings contradict a previous reportlo in which they were unable to demonstrate antibodies against Leptospira spp. in body fluids. In our studies, all aborted mares carried significantly high titers to the same serovars that were detected in the fetal fluid and/or heart blood. These cases with high titers correlated very well with those cases from which leptospires were cultured from fetal tissues. Leptospiral antibody titers in the body fluid and/or heart blood and gross and histopathologic lesions did not differ with age, breed, or sex or between fetuses and stillborn foals.
Acknowledgements
The investigation reported in this paper (92-4-98) is published by permission of the Dean and Director of the Kentucky Agricultural Experiment Station and the College of Agriculture, University of Kentucky (Lexington, KY 405460076). The work was supported by a grant from the University of Kentucky Equine Research Foundation. We thank Dr. D. A. Miller, National Services Laboratories, for performing restriction enzyme analysis to characterize leptospiral isolates, Mrs. E. T. Napier for histologic preparation, and Ms. P. G. Scisco and Mrs. P. L. Shyrock for manuscript preparation.

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Request reprints from Dr. K. B. Poonacha, Livestock Disease Diagnostic Center, University of Kentucky, 1429 Newtown Pike, Lexington, KY 405 1 1 (USA).

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