INFECTION AND IMMUNITY, Jan. 1985, p. 311-317 Vol. 47, No. 10019-9567/85/010311-07$02.00/0Copyright C 1985, American Society for Microbiology

Effects of Ovarian Hormones on Manifestation of PurulentEndometritis in Rat Uteruses Infected with Escherichia coli

YOSHIKAZU NISHIKAWA,l* AND TSUYOSHI BABA2Department of Veterinary Surgery and Obstetrics' and Department ofAnimal Microbiology,2 College of Agriculture,

University of Osaka Prefecture, Sakai, Osaka, 591, JapanReceived 21 February 1984/Accepted 9 October 1984

To assess the influence of hormones on uterine infections, Escherichia coli was infused into uterine lumensof ovariectomized or adrenoovariectomized rats receiving exogenous administration of various doses of ovarianhormones. Large numbers of E. coli were recovered from the rat uterine lumens, irrespective of hormonalinfluences. The number of leukocytes in the uterine flushings, representing the magnitude of purulentinflammation, differed significantly depending upon the hormonal regimen given to each host. Purulentendometritis was induced by E. coli in ovariectomized rats receiving progesterone or corn oil (hormonevehicle). Infections were asymptomatic in rats receiving estradiol, but promethazine-treated uterine horns weresusceptible to infection. When progesterone was administered along with estradiol, purulent inflammation wascaused by E. coli, but the number of leukocytes in the uterine lumens was significantly less than that obtainedfrom the rats treated with progesterone or corn oil. These effects of ovarian hormones on uterine infectionswere observed in adrenoovariectomized rats as well as in ovariectomized rats. It is suggested that estradiolalters the nature of endometrial epithelium and prevent manifestation of purulent endometritis; progesteroneantagonizes estradiol. Adrenal hormones appear not to participate in the pathogenesis of endometritis inducedby E. coli.

In rabbits (9), sheep (10), and cattle (8), uteruses in theluteal phase were more vulnerable to infection than those inthe follicular phase. In women, increased susceptiblity tochlamydial infections (11), development of vaginal candidi-asis (5, 22), and varying rates of the gonococcus isolationfrom cervical culture (17) were associated with the use oforal contraceptives or phases of the menstrual cycle. Al-though these reports suggest that ovarian hormones areimplicated in the alteration of the course of genital infec-tions, hormonal influence has only been demonstrated inlimited laboratory models (3, 16, 24). A previous report hasindicated that rat uteruses are another model for investigat-ing the pathogenesis of uterine infection (21), in whichEscherichia coli inoculated at diestrus or pseudopregnancyinduced purulent endometritis but when inoculated at pro-estrus-estrus caused asymptomatic infection. Although pro-gesterone is a major ovarian hormone in pseudopregnancy,estrogenic effects are predominant at proestrus-estrus.Therefore, it was probable that these ovarian hormoneswere involved in the pathogenesis of uterine E. coli infectionin rats.

Corticoids influence the course of experimental microbialinfections in laboratory animals (6, 7, 13-15, 18, 20), andcortisol inhibits the physiological action of estrogens (23,28).The purpose of the present study was to clarify the

relationship between hormones and uterine infections inrats. To estimate the influence of ovarian hormones, spayedrats were treated with the hormone and inoculated with E.coli. Adrenoovariectomized rats were used to examinewhether adrenal glands play any part in the influence ofovarian hormones on uterine infections. The effects ofestradiol on the uterine infection were also examined on theendometrial epithelium of the uterus which was chemicallysloughed off. Hormonal influences on uterine infections

* Corresponding author.

were evaluated on the basis of the numbers of E. coli andleukocytes found in uterine contents and by histologicalobservation.

MATERIALS AND METHODSAnimals. Virgin female Wistar rats, 7 to 8 weeks old, were

obtained from the Shizuoka Agricultural Cooperative (Shi-zuoka, Japan). They were caged in groups of six, in a roomat ca. 23°C with a lighting cycle of 7:00 a.m. to 7:00 p.m. Ratswere preconditioned in the room for at least 2 weeks. Feedand water were available ad libitum. A total of 145 rats wereused. Unless otherwise indicated, each group in a experi-ment consisted of five animals. Ovariectomy was performedthrough lateral incisions in rats under pentobarbital anesthe-sia. Adrenalectomy was conducted through dorsal incisionsconcurrently with the ovariectomy, and saline, instead ofwater, was available to these rats.Hormonal regimens. Estradiol and progesterone were pur-

chased from Sigma Chemical Co. (St. Louis, Mo.). At 2weeks after ovariectomy, these hormones were administeredsubcutaneously in 0.1 ml of corn oil. Details in each exper-iment are described in the figure legends.

Bacterial strain. A strain of E. coli (0:25, H:-) isolatedfrom the pus of a dog suffering from pyometra was used (21).

Preparation of inoculum. E. coli was grown on Trypto-soya agar (Nissui Pharmaceutical Corp., Ltd., Tokyo, Ja-pan) at 37°C for 18 to 20 h and suspended in saline to containca. 106 CFU per 0.02 ml.

Uterine infection. Uteruses were exposed surgically underthe anesthesia. Both uterine horns of each animal wereligated at the cervical ends to prevent possible drainage ofuterine contents. An E. coli suspension (106 CFU) wasinoculated into the lumen of one uterine horn through theuterine wall at the utero-tubal junction. The other horn wasleft noninoculated. At 24 h after injection, the rats wereexsanguinated by cardiac puncture. The plasma was sepa-rated and stored for measurement of corticosterone levels.

311

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from

312 NISHIKAWA AND BABA

Numbers of E. coli and leukocytes in the uterine contents.The inoculated horn was flushed with 1.0 ml of sterile salinesolution into a test tube and dispersed by being pressedthrough syringe needles. A 10-fold dilution of the flushingswas made serially in saline solution. A 0.1-ml sample wastransferred to a petri dish and mixed with about 20 ml ofmelted Endo agar. The plates were incubated at 37°C, andthe number of lactose-fermenting colonies was recorded tobe E. coli, because no bacteria indigenous to uterine lumensof ovariectomized rats were detected. Leukocytes werecounted by using a bacteria counting chamber (Erma Co.,Tokyo, Japan) and expressed as the number of leukocytes in0.02 ,ul of flushing. The noninoculated horn of the uterus wasisolated, cleared of fat, and weighed with a torsion balance.Then, the uterine luminal fluid was eliminated, and theweight of the horn was measured again. The secretion indexwas calculated with the following formula:

Secretion index = [(B - A) x 100]/A,where A represents the weight of uterine horn after theelimination of uterine luminal fluid and B is the weight ofuterine horn before the elimination.

Protein binding assay. Corticosterone was measured bythe protein binding method (32). Briefly, each of the plasmasamples was extracted first with methylene chloride (5.0 ml).Then, the extract was dissolved in 25% ethanol (1.0 ml). Thissolution was partitioned by carbon tetrachloride (5.0 ml,twice), and then, the carbon tetrachloride layers were againreversably partitioned with 50% methanol (5.0 ml). Themethanol layer was extracted by methylene chloride (5.0ml). Methylene chloride was transferred into a test tube anddried under nitrogen gas. To each tube, 1.0 ml of 0.05 Mborate buffer solution containing 0.7% canine serum and[3H]corticosterone (New England Nuclear Corp., Boston,Mass.) was added (ca. 5,000 cpm/ml). After being agitatedfor a few seconds, the test tubes were placed in a 37°C bathfor 5 min with constant agitation and cooled in an ice-waterbath for 15 min. Dextran-coated Florisil (40 mg) was thenadded to each tube to separate the unbound [3H]corticoste-rone. The tubes were agitated vigorously for 60 s in the bathand kept there until the Florisil settled. A 0.5-ml portion ofsupernatant was transferred into vials containing 5 ml ofscintillator solution, and radioactivity was counted in aAloka liquid scintillation spectrometer. The concentration ofcorticosterone was read from the processed standard curve.The interassay coefficient of variation was 13% (n = 6).

Histological study. Rats received estradiol (0.1 ,ug/day) orprogesterone (1 mg/day) or both estradiol and progesteroneregimens for 3 days. Preliminary dose-response experimentsrevealed that these doses of hormones are enough to affectthe course of uterine infection with E. coli (See Fig. 2 and 4).One uterine horn was inoculated with viable E. coli, and theother horn was injected with the Formalin-killed organisms.At 24 h after inoculation, the rats were killed, and the entireuterus was fixed in 10% Formalin, sectioned, and stainedwith hematoxylin-eosin.

Promethazine-hydrochloride treatment. Five rats were in-jected with estradiol (0.1 ,ug/day) for 3 days. Before inocu-lation with E. coli, promethazine (1 mg in 0.02 ml of saline)was infused into the lumen of right uterine horn through theuterine wall near the utero-tubal junction. Promethazine,supplied by K. Tsuchiya (Takeda Chemical Industries Ltd.,Osaka, Japan), causes massive sloughing of the epitheliallayer of endometrium (30). At 30 min later, the horn wasflushed with four 1-ml portions of saline; E. coli was theninoculated into the horn (promethazine plus E. coli). The left

horn, as a control, received only saline flushings without thepromethazine treatment and was inoculated with E. coli.The other group of five rats were also treated in a similarmanner as described above, except that the rats were notinoculated.

RESULTSEffects of ovarian hormones on uterine infection. A large

number of E. coli organisms were recovered from the uterihehorn of each rat (Fig. 1). In rats receiving progesterone orcorn oil, large numbers of leukocytes were observed in theuterine contents. Few leukocytes were recovered from uter-ine lumens of rats injected with estradiol alone. Whenprogesterone and estradiol were administered simultane-ously, the number of leukocytes found in the lumen was

8

SU~

dz

0-J

6

4

2

0

>

0

00

z

100 F-

10 H

X)*1100r-o

.0

4) 50u

3E 3E 3P3 P

Steroid Treatment

3C

FIG. 1. Influence of ovarian hormones on the number of E. coliand leukocytes recovered from the uterine lumen and influence ofthe hormones on the secretion index. Ovariectomized rats were

injected daily with 1.0 p.g of estradiol (E) or progesterone (P) or bothwith 0.1 ml of corn oil. Control rats (C) were administered with 0.1ml of corn oil alone. On the last day of the 3-day treatment, E. coliwas inoculated into the uterus. Animals were killed 24 h afterinoculation. The bars represent the mean of five animals per group,and the vertical lines on the bars indicate the standard deviation.

I Aft---AM

INFECT. IMMUN.

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from

UTERINE INFECTION AND OVARIAN HORMONES 313

n0 0.001 0.01 0.1Estradiol Administration

Elserved (Fig. 4). A 1.0-mg amount or more of progesteroneabolished the effect of estradiol. Mean concentrations ofcorticosterone in each group ranged from 162 to 210 ng perml of plasma. There was no correlation between the dose ofprogesterone and the level of corticosterone.Time course of the effect of progesterone treatment on

uterine infection. When progesterone was given for all 3days, a large number of leukocytes were observed (Fig. 5).

Histological findings. No histopathological changes wereobserved in uteruses of the estradiol-treated rats after inoc-ulation with viable E. coli (Fig. 6A). When progesterone wasadministered concurrently with estradiol, leukocytic exu-date was found in the uterine lumens (Fig. 6B3). In groupsreceiving progesterone or corn oil, induction of purulentendometritis was apparent (Fig. 6C). When Formalin-killedE. coli was injected, no inflammatory changes occurred,regardless of hormonal treatments (Fig. 6D and E).

Effect of ovarian hormones on uterine infection in adre-noovariectomized rats. Adrenoovariectomized rats receivedestradiol (0.1 ,ug/day) with or without progesterone (1.0mg/day) for 3 days. On the last day of a 3-day treatment, E.coli was inoculated into the uterine lumen. Few leukocytes(1.8 ± 1.8/0.02 ,ul of flushing; n = 7) were recovered fromuterine horns of rats injected with estradiol alone. When

8 r FE1

1.0 ug

FIG. 2. The effects of different doses of estradiol on the numberof E. coli and leukocytes recovered from the uterine lumen andeffects on the secretion index. Estradiol (0.001 to 1.0 pug) in corn oilwas administered daily for 3 days. On the last day of the 3-daytreatment, E. coli was inoculated into the uterine horn. Animalswere killed 24 h after inoculation. Each bar represents the mean +standard deviation of five rats in each group.

greater than that of the rats treated with estradiol alone (P <0.001), but still fewer than that in rats administered proges-terone or corn oil alone (P < 0.02).

Five animals receiving each of the four kinds of hormonalregimens were inoculated with Formalin-killed E. coli.Leukocytes were hardly found, irrespective of hormonalregimens; no indigenous bacteria which formed colonieswere detected (data not shown).

Effects of different doses of estradiol on uterine infection. Asthe amount of estradiol increased, the number of leukocytesdecreased, and the volume of uterine luminal fluid secretedincreased (Fig. 2). A 0.1-,ug amount or more of estradiolprevented purulent inflammation. Mean concentrations ofcorticosterone in each group ranged from 177 to 245 ng perml of plasma, and there was no correlation between the doseof estradiol and the level of corticosterone.Time course of the effect of estradiol treatment on uterine

infection. As the number of estradiol treatment increased,the secretion index increased, and the number of leukocytesdecreased (Fig. 3).

Effects of different doses of progesterone administered withestradiol on uterine infection. When the dose of progesteroneincreased, a progressive increase in number of leukocytesand a decreasing volume of uterine luminal fluid was ob-

w

0

0

z

0

-

41-

2

0

1004L)

0

d)

10

0

0

z

xa)

C:c

1-

0H - I I I I

2 3Estradiol Administration(Days)

FIG. 3. Time course of the effect of estradiol treatment on thenumbers of E. coli and leukocytes recovered from the uterine lumenand time course of the secretion index. Estradiol (0.1 ,ug/0.1 ml) incorn oil was given daily for 1, 2, or 3 days. On the last day ofestradiol treatment, E. coli was inoculated into the uterine horn.Animals were killed 24 h after inoculation. Each bar represents themean + standard deviation of five rats in each group. The leukocytenumber for day 2 is 7.4 ± 7.3.

86 i i

4

0u

LLii0dz0'10-J

x

C

a04-

G)

(.1)

2 -

100o-

50k

VOL. 47, 1985

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from

314 NISHIKAWA AND BABA

p injected along with estradiol antagonized the dose-depend-ently inhibitory effect of estradiol on the manifestation ofpurulent endometritis. Progesterone antagonizes the physi-ological effects of estrogens (31); therefore progesteronemay permit E. coli to cause purulent inflammation byinhibiting the effects of estradiol.

Significant changes in corticosterone levels were not in-duced by the administration of estradiol or progesterone inovariectomized rats. In adrenoovariectomized rats as well asin ovariectomized rats, estradiol prevented E. coli fromcausing purulent endometritis. It seems evident that adrenalglands are not involved in the effect of ovarian hormones onthe course of uterine infections.Because E. coli injected into the uterus at proestrus-estrus

caused no histopathological changes (21), it is likely thatestrogens are responsible for the prevention of endometritisduring proestrus-estrus.

8r-

-

Q

Li

0

0

0.125 0.25 0.5 1.0 2.0 mg

Progesterone Administration

FIG. 4. Effect of estradiol and progesterone on the number of E.coli and leukocytes recovered from the uterine lumen and effect ofthe hormones on the secretion index. Ovariectomized rats were

injected with estradiol (0.1 ,ug/day) and different doses (0.125 to 2.0mg/day) of progesterone for 3 days. On the last day of the 3-daytreatment, E. coli was inoculated. Each bar represents the mean

standard deviation of five rats in each group.

progesterone was administered along with estradiol, signifi-cantly large numbers of leukocytes (97.0 ± 51.0/0.02 ,ul offlushing; n = 8) were detected. Complete removal of adrenalwas confirmed by the protein-binding assay. Results indi-cated no corticosterone in the plasma which was collected atautopsy.

Effects of pretreatment with promethazine-hydrochlorideon uterine infection. Despite treatment with estradiol, E. colicaused purulent inflammation in promethazine-treated horns(Fig. 7). A large number of leukocytes and E. coli organismswere recovered from the lumen. Few leukocytes were foundin the control horn. Promethazine-treatment alone did notincrease the number of leukocytes (PZ).

DISCUSSIONThe results of present study show that estradiol prevents

the manifestation of purulent endometritis, and progesteroneantagonizes the effects of estradiol. Formation and accumu-lation of uterine luminal fluid caused by estrogens have beenwell established (1, 12, 19, 25); thus, the secretion index was

introduced as an indicator of the physiological response ofuteruses to estradiol. In spite of uterine infection with E.coli, estradiol prevented purulent endometritis at doses thatare known to induce an accumulation of uterine luminal fluidas indicated by the increased secretion index. Progesterone

snCo

4)

(.30

4)

0

z

6

4H

2 1-

0

100

10

x' 1004)

10c

0

50

cn

tr)~3E 3E 3E

+ +

P 2P 3PSteroid Treatment

FIG. 5. Time course of the effect of progesterone administeredalong with estradiol. Ovariectomized rats were injected with estra-diol (0.1 jxg/day) for 3 days. Progesterone (1.0 mg/day) was admin-istered along with estradiol on all 3 days (3E + 3P), on the last 2days (3E + 2P), or on the last day (3E + 1P) of a 3-day estradioltreatment. On the last day of the 3-day treatment, E. coli was

inoculated. Each bar represents the mean ± standard deviation offive rats in each group.

8

uLi0

6z0p0-J

4

2 _

VI> 10 00(I,

00

4)" 1006z

I00

0

'- 500U.)U)0 eift

a mm m m 0 0

I

INFECT. IMMUN.

6 _

I

I

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from

UTERINE INFECTION AND OVARIAN HORMONES 315

C,i, b' X§', ,"~~~~~Wi1;im

FIG. 6. Histological changes 24 h after the inoculation with viable (A, B, and C) or Formalin-killed (D and E) E. coli. Ovariectomized ratswere injected daily with 0.1 p.g of estradiol in 0.1 ml of corn oil (A). In the other groups (B and D), progesterone (1.0 mg/day) was administeredalong with estradiol. Controls received only corn oil (C and E). On the last day of a 3-day treatment, E. coli was inoculated. (A) The uterinehorn is filled and dilated with uterine luminal fluid. No inflammatory changes are observed. (B) Viable E. coli caused purulent inflammation.Cellular debris are seen in the uterine lumen. (C) Inoculation of viable E. coli resulted in purulent endometritis. Pus in the lumen dilated theuterine horn. (D) and (E) No histological changes are seen. Hematoxylin-eosin staining. Magnification, x20.

VOL. 47, 1985

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from

316 NISHIKAWA AND BABA

ence that may lead to purulent endometritis, because estra-diol increases the cell division (15a) and modifies the mor-phology (5a) and surface nature of carbohydrates (20a) ofendometrial epithelial cells.

ACKNOWLEDGMENTSWe are indebted to A. Arakawa of the Department of Veterinary

Internal Medicine for help with preparing the manuscript in English,T. Imori of the Department of Veterinary Surgery and Obstetrics forvaluable discussion, and H. Sugiyama of the Department of Veter-inary Pathology for photography.

ND

PZ PZ+

E.coli E.coliFIG. 7. The number of E. coli and leukocytes recovered from the

uterine lumen, treated with promethazine-HCl (PZ) or inoculatedwith E. coli or both, in ovariectomized rats administered estradiol.Animals were killed 24 h after treatment or inoculation. For details,see text. Each bar represents the mean ± standard deviation of fiverats in each group.

The mechanisms by which uterine infection does not bringabout endometritis under the influence of estradiol stillremain to be elucidated. Because Roth et al. (26) observedthat even suprapharmacological doses of estradiol in vivofailed to affect neutrophil function and total and differentialleukocyte counts, it seems unlikely that estradiol suppressesacute inflammation of rat uteruses through systemic hostresponses such as leukocytopenia or neutropenia. The findingthat purulent inflammation was observed in estradiol-treatedrats when E. coli was infused into the promethazine-treatedhorn of the uterus suggests that suppression of purulentendometritis by estradiol must be a localized effect inuteruses. Asymptomatic infection in estradiol-treated ratsmay be accounted for by the lack of susceptibility of theuterine epithelium to infection by E. coli.

Bacterial adherence to mucosal surface is known to be an

important process in the pathogenesis (2, 4, 27, 29). Re-cently, Nishikawa examined the endometrial mucosa of theuterus inoculated with E. coli by scanning electron micros-copy. Adherence of E. coli to the epithelium of ovariectom-ized rats was observed, but not on the mucosa of estradiol-treated rats (21a). It seems that estradiol modifies thesusceptibility of the endometrial epithelium for E. coli adher-

LITERATURE CITED1. Allen, E., B. F. Francis, L. L. Robertson, C. E. Colgate, C. G.

Johnston, E. A. Doisy, W. B. Kounts, and H. V. Gibson. 1924.The hormone of the ovarian follicle. Its localisation and actionin test animals, and additional points bearing upon the internalsecretion of the ovary. Am. J. Anat. 34:133-181.

2. Arbuthnott, J. P., and C. J. Smyth. 1979. Bacterial adhesion inhost/pathogen interactions in animals, p. 165-198. In D. C.Elwood, J. Melling, and P. Rutter (ed.), Adhesion of microor-ganisms to surfaces. Academic Press, Inc., New York.

3. Baker, D. A., and S. A. Plotkin. 1978. Enhancement of vaginalinfection in mice by herpes simplex virus type II with proges-terone. Proc. Soc. Exp. Biol. Med. 158:131-134.

4. Beachey, E. H. 1981. Bacterial adherence: adhesin-receptorinteractions mediating the attachment of bacteria to mucosalsurfaces. J. Infect. Dis. 143:325-345.

5. Catterall, R. D. 1971. Influence of gestogenic contraceptive pillson vaginal candidiasis. Br. J. Vener. Dis. 47:45-47.

5a.Enders, A. C. 1976. Anatomical aspects of implantation. J.Reprod. Fert. Suppl. 25:1-15.

6. Friedman, S. B., L. J. Grota, and L. A. Glasgow. 1972. Differ-ential susceptibility of male and female mice to encephalomyo-carditis virus: effects of castration, adrenalectomy, and theadministration of sex hormones. Infect. Immun. 5:637-644.

7. Giron, D. J., and P. T. Allen. 1970. Effect of estrogens and othersteroids on MM virus infection in mice. Infect. Immun.2:426-430.

8. Hawk, H. W., T. H. Brinsfield, G. D. Turner, G. W. Whitmore,and M. A. Norcross. 1964. Effect of ovarian status on acuteinflammatory responses in cattle uteri. Am. J. Vet. Res.25:362-366.

9. Hawk, H. W., G. D. Turner, and J. F. Sykes. 1960. The effect ofovarian hormones on the uterine defense mechanism during theearly stage of induced infection. Am. J. Vet. Res. 21:644-648.

10. Hawk, H. W., G. D. Turner, and J. F. Sykes. 1961. Variation inthe inflammatory response and bactericidal activity of the sheeputerus during the estrous cycle. Am. J. Vet. Res. 22:689-692.

11. Hilton, A. L., S. J. Richmond, J. D. Kilne, F. Hindley, andS. K. R. Clarke. 1974. Chlamydia A in the female genital tract.Br. J. Vener. Dis. 50:1-9.

12. Homburger, F. M., M. S. Grossman, and A. Tregier. 1955.Experimental hydrouteri (hydrometra) in rodents and somefactors determining their formation. Proc. Soc. Exp. Biol. Med.90:719-723.

13. Hurley, D. L., J. E. Balow, and A. S. Fauci. 1975. Experimentaldisseminated candidiasis. Il. Administration of glucocortico-steroids, susceptibility to infection, and immunity. J. Infect.Dis. 132:393-398.

14. Isenberg, H. D., S. L. Wiener, G. A. Isenberg, J. Sampson-Scherer, M. Urivetzky, and J. I. Berkman. 1976. Rat polyvinylsponge model for the study of infections: host factors andmicrobial proliferation. Infect. Immun. 14:490-495.

15. Kass, E. H. 1960. Hormones and host resistance to infection.Bacteriol. Rev. 24:177-185.

15a.Kirkland, J. L., G. N. Barrett, and G. M. Stancel. 1981.Decreased cell division of the uterine luminal epithelium ofdiabetic rats in response to 17p-estradiol. Endocrinology109:316-318.

16. Kita, E., H. Matsuura, and S. Kashiba. 1981. A mouse model forthe study of gonococcal genital infection. J. Infect. Dis.

8 r

0

0

z

0-j

6

4

2

0

o 1004O-.

0

_ 10q.-0

0z

_-

INFECT. IMMUN.

I

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from

UTERINE INFECTION AND OVARIAN HORMONES 317

143:67-70.17. Koch, M. L. 1947. A study of cervical cultures taken in cases of

acute gonorrhea with special reference to the phases of themenstrual cycle. Am. J. Obstet. Gynecol. 54:861-866.

18. Lehmann, P. F., and L. 0. White. 1975. Chitin assay used todemonstrate renal localization and cortisone-enhanced growthof Aspergillus fumigatus mycelium in mice. Infect. Immun.12:987-992.

19. Long, J. A., and H. M. Evans. 1922. The estrous cycle in the ratand its associated phenomena. Mem. Univ. Calif. 6:1-148.

20. Mishra, S. K., R. S. Sandhu, H. S. Randhawa, V. N. Damodaran,and S. Abraham. 1973. Effect of cortisone administration onexperimental nocardiosis. Infect. Immun. 7:123-129.

20a.Murphy, C. R., and A. W. Rogers. 1981. Effects of ovarianhormones on cell membranes in the rat uterus. III. The surfacecarbohydrates at the apex of the luminal epithelium. CellBiophys. 3:305-320.

21. Nishikawa, Y., T. Baba, and T. Imori. 1984. Effect of the estrouscycle on uterine infection induced by Eschericia coli. Infect.Immun. 43:678-683.

21a.Nishikawa, Y. 1985. Adherence of Escherichia coli in thepathogenesis of endometritis and effects of estradiol examinedby scanning electron microscopy. Infect. Immun. 47:318-321.

22. Oriel, J. D., B. M. Partridge, M. J. Denny, and J. C. Coleman.1972. Genital yeast infections. Br. Med. J. 4:761-764.

23. Pietras, E. J., and C. M. Szego. 1975. Steroid hormone-respon-sive isolated endometrial cells. Endocrinology 96:946-954.

24. Rank, R. G., H. J. White, A. J. Hough, Jr., J. N. Pasley, and

A. L. Barron. 1982. Effect of estradiol on chlamydial genitalinfection of female guinea pigs. Infect. Immun. 38:699-705.

25. Ringler, I. 1961. The composition of rat uterine luminal fluid.Endocrinology 68:281-291.

26. Roth, J. A., M. L. Kaeberle, and W. H. Hsu. 1982. Effect ofestradiol and progesterone on lymphocyte and neutrophil func-tions in steers. Infect. Immun. 35:997-1002.

27. Satterwhite, T. K., D. G. Evans, H. L. Dupont, and D. J. Evans,Jr. 1978. Role of Escherichia coli colonization factor antigen inacute diarrhoea. Lancet ii:181-184.

28. Spaziani, E., and C. M. Szego. 1958. The influence of estradioland cortisol on uterine histamine of the ovariectomized rat.Endocrinology 63:669-678.

29. Svanborg Eden, C., L. A. Hanson, U. Jodal, U. Lindberg, and A.Sohl Akerlund. 1976. Variable adherence to normal humanurinary tract epithelial cells of Escherichia coli strains associ-ated with various forms of urinary-tract infection. Lancetii:490-492.

30. Tachi, C., S. Tachi, and H. R. Lindner. 1970. Action ofantihistamines on the endometrium and the histamine theory ofdecidual induction. J. Reprod. Fertil. 23:169-172.

31. Tachi, C., S. Tachi, and H. R. Lindner. 1972. Modification byprogesterone of oestradiol-induced cell proliferation, RNA syn-thesis and oestradiol distribution in the rat uterus. J. Reprod.Fertil. 31:59-76.

32. Torii, R., and T. Imori. 1975. Simple assay method for bovineplasma progesterone, estrone, estradiol, cortisol, and corticos-terone. Jpn. J. Anim. Reprod. 20:153-164.

VOL. 47, 1985

on June 8, 2020 by guesthttp://iai.asm

.org/D

ownloaded from