Expression of alpha 1 and beta 3 integrins subunits in the endometrium of patients with tubal phimosis or hydrosalpinx

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1 REPRODUCTIVE BIOLOGY Expression of alpha 1 and beta 3 integrins subunits in the endometrium of patients with tubal phimosis or hydrosalpinx Ricardo Francalacci Savaris, Ph.D., a José Luiz Pedrini, M.Sc., a Renato Flores, M.D., b Gemir Fabris, M.D., c and Cláudio Galleano Zettler, Ph.D. d a Ambulatório de Fertilidade, b Serviço de Radiologia, and c Serviço de Videolaparoscopia, Grupo Hospitalar Conceição, Ministério da Saúde; and d Serviço de Patologia, Programa de Pós-Graduaçáo em Patologia; Fundação Faculdade Federal de Ciências Médicas de Porto Alegre, Porto Alegre, RS, Brazil Objective: To determine the expression of 1 and 3 integrin subunit on the endometrium of infertile patients with hydrosalpinx and infertile patients with tubal phimosis. Design: Case control study. Setting: Tertiary medical center. Patient(s): Infertile patients with radiologic or laparoscopic diagnosis of hydrosalpinx (n 11) or tubal phimosis (n 12) as the only cause of infertility, and fertile controls (n 17). Intervention(s): Immunohistochemical analysis of 1 and 3 integrin subunits was performed on endometrial biopsies obtained during the implantation window. Main Outcome Measure(s): Histologic score (HSCORE) on luminal and glandular endometrium of the patients with hydrosalpinx or tubal phimosis and the normal fertile controls. Result(s): The median ( SEM) HSCORE for 3 subunit expression in endometrial glands was and for tubal phimosis and hydrosalpinx, respectively, and for fertile controls. The median HSCORE for 3 subunit expression in luminal epithelium for tubal phimosis, hydrosalpinx, and fertile controls was , , and , respectively. No statistical difference was observed on the expression of 1 integrin subunit expression between the three groups. Conclusion(s): The endometrial expression of 3 integrin subunit is reduced in the presence of tubal phimosis or hydrosalpinx, during the window of implantation. (Fertil Steril 2006;85: by American Society for Reproductive Medicine.) Key Words: Beta 3 integrin subunit, alpha 1 integrin subunit, tubal phimosis, hydrosalpinx Hydrosalpinx is a word of Greek derivation that signifies a fallopian tube filled with water or fluid. In 1986, Donnez et al. proposed a classification for the different stages of hydrosalpinx (1). On the basis of that system, oviductal damage is subdivided into four degrees: [1] fimbrial phimosis, [2] ampullar dilatation 15 mm, [3] ampullar dilatation 15 mm and 25 mm, with well-preserved ampullary folds, and [4] ampullar dilation 25 mm, with well-preserved ampullary folds. This classification might represent the natural history of tubal damage that results from pelvic inflammatory disease. Received March 13, 2005; revised and accepted June 29, Supported by Conselho Nacional de Pesquisa, grant no / Reprint requests: Ricardo Francalacci Savaris, M.D., Universidade Federal do Rio Grande do Sul, Serviço de Ginecologiae Obstetrícia, Rua Ramino Barcelos, 2350/1125, Porto Alegre, RS , Brazil (FAX: ; rsavaris@hcpa.ufrgs.br). The detrimental effects of hydrosalpinx on the outcome of IVF have been well documented (2 5). The mechanisms by which hydrosalpinx affects implantation rates remain unresolved. Most published studies are based on third degree or greater disease (2). Strandell et al. (3) showed improvement on pregnancy rates only when ultrasound-visible hydrosalpinges are surgically removed. The conclusions drawn from these studies are that [1] hydrosalpinges have a negative effect on IVF (2), and [2] hydrosalpingeal fluid has no obvious toxic effect on embryo development (6, 7). Many argue that endometrial receptivity is the rate-limiting factor for poor IVF outcome. This diminished endometrial receptivity could be related to mechanical and molecular factors. Hydrosalpingeal fluid might represent a mechanical barrier to implantation, especially when it leaks into the endometrial cavity. The presence of hydrosalpingeal fluid might disturb or prevent contact between the embryo and the en- 188 Fertility and Sterility Vol. 85, No. 1, January /06/$32.00 Copyright 2006 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert

2 dometrial surface (5, 8, 9). Such lavage of the endometrial cavity might be evidenced by the chronic vaginal discharge seen with this condition (10). Hydrosalpinges might also decrease implantation rates by affecting endometrial receptivity. Although not fully understood, several candidate genes and proteins that have a putative role in the implantation process might have altered expression patterns in the presence of hydrosalpinx. Some of these molecular markers include the integrins, more specifically 1 1, 4 1, and v 3 (11). Integrins are perhaps the best-characterized endometrial biomarker. They exhibit a decreased expression in the presence of hydrosalpinx, and after surgical removal their normal levels are restored (12, 13). Because hydrosalpinx has different stages of classification for tubal damage, and because stages III and IV have been shown to have an adverse effect on integrin expression, an investigation of endometrial markers in patients with earlystage hydrosalpinx (stage I) is warranted. The purpose of this study was to verify that the expression of 1 and 3 integrin subunits during the window of implantation in infertile patients with tubal phimosis is low, as it is in patients with hydrosalpinx. MATERIALS AND METHODS Endometrial Samples Infertile patients with only pure tubal factor as the cause of infertility attending to the infertility outpatient clinic of Hospital Nossa Senhora da Conceição during were invited to participate in the study. Hydrosalpinx was diagnosed by hysterosalpingography and/or laparoscopy. The different stages of hydrosalpinx were classified according to Donnez et al. (1). Controls were obtained from among confirmed fertile patients with tubal ligation who were seeking tubal reanastomosis. A second source of controls was women whose partners were seeking vasectomy reversal. Human endometrium was obtained by pipelle suction curettage on postovulatory day 7, 8, 9, or 10 (LH 7 10), based on a measurement of the urinary LH surge (LH kit; Biomedical Products, Ryadh, Saudi Arabia). The endometrial samples were divided in two parts: one was snap-frozen in liquid nitrogen and stored at 80 C for immunohistochemistry, and the other was placed in 10% buffered formalin for paraffin section. Paraffin blocks were sectioned and stained with hematoxylin and eosin and dated according to the criteria of Noyes et al. (14). Endometrial biopsies performed during the study that were not in phase (dyssynchrony of 2 days, based on the time of ovulation) were excluded. Immunohistochemistry Serial cryosections of frozen endometrium, 8 m thick, were placed onto poly-l-lysine-coated slides. Cryosections were fixed in 4% paraformaldehyde for 10 minutes and rinsed for 3 minutes in phosphate-buffered saline (PBS). Endogenous peroxidases were quenched with 0.3% H 2 O 2 in absolute methanol (Mallinckrodt, Paris, KY) for 30 minutes at room temperature. After 3 2-minute rinse in PBS, sections were covered with 0.4% Triton-X 100 (Sigma T-8532; Sigma, St. Louis, MO) for 10 minutes to induce membrane stability. After three additional 2-minute rinses in PBS, nonspecific epitopes were blocked with 2% normal goat serum for 10 minutes. After removing the excess serum, polyclonal antibodies to 1 integrin subunit (TS2/7) at a 1:10,000 dilution and to 3 integrin subunit (SSA6) at a 1:2,000 dilution were placed as primary antibodies in a moist chamber at 4 C overnight. After a 3 2-minute rinse in PBS, nonspecific epitopes were blocked again with 2% normal goat serum for 10 minutes and excess removed. The secondary antibody (Vector BA-9200, biotinylated goat antimouse IgG; Vector Laboratories, Burlingame, CA) was placed onto the slides for 30 minutes, in goat serum at a 1:100 dilution in a moist chamber at room temperature with Vectastain Elite ABC kits (Vector Laboratories). Diaminobenzidine (DAB Solution, Vector SK-4100) was added for 8 minutes, as a chromogen to complete the reaction, after 3 2-minute PBS rinse. After three additional 2-minute PBS rinses, slides were counterstained with hematoxylin and mounted. Two independent readers (R.F.S. and C.G.Z.), using the histologic score (HSCORE ) in a blinded fashion, evaluated the resulting staining under optical microscope. The HSCORE was calculated with the equation HSCORE Pi (i 1), where I intensity of staining with a value of 1, 2, or 3 (weak, moderate, or strong respectively), and Pi is the percentage of stained epithelial, stromal, or endothelial cells for each intensity, varying from 0 to 100%. This method has a low interobserver (r 0.85) and intraobserver (r 0.84) variation (11). Sample Size, Ethical Issues, and Statistical Analysis Results of immunohistochemical HSCORE were compared by the Kruskal-Wallis test with Dunn posttest comparison with significance of P.05. Staining was judged negative when HSCORE was 0.7, on the basis of previous receiver operating curve analysis (15). This cut-off was used for considering positive and negative staining. Correlation coefficient and index were calculated for interobserver and intraobserver variation in HSCORE assessment of endometrial samples. For intraobserver variation, the same observer re-examined the samples 1 month later, and HSCOREs were reassigned. Interobserver variation was established by having the same sample reread by a second experienced observer (C.G.Z.). In case of disagreement, the slides were reviewed and a consensus view achieved. The coefficient measures pairwise agreement among a set of category judgments, correcting for expected chance agreement. Values of range from 1, for total disagreement, through 0, representing the agreement expected by chance, to 1 for perfect correlation. A value of 0.20 indicates a weak correlation, fair, moderate, good, and an excellent correlation (16). Fertility and Sterility 189

3 TABLE 1 Demographic characteristics of patients (phimosis and hydrosalpinx) and control subjects undergoing endometrial biopsy during the midluteal phase. Control Phimosis Hydrosalpinx Characteristic (n 19) (n 12) (n 11) Age (y) Mean SD a Minimum Maximum Day of biopsy (LH ) Mean SD b Minimum Maximum Histologic date Mean SD c Minimum Maximum a P.49. P.22. P.9. The sample size was calculated according to a formula described elsewhere (17); it considered and error of 0.05 and 0.2 respectively, in a population in which the variance of the expression of integrins is 0.79 (18), and a minimal difference among the HSCORE of 1.4 (i.e., the double for the 0.7 cut-off), or 35%. The result was a minimum of 7 subjects in each group. The use of human tissue for research was based on informed consent and was approved by the institutional review board of General Hospital of Grupo Hospitalar Conceição of Porto Alegre. Data analysis was performed with commercial softward (GraphPad InStat 3.05 for Windows; GraphPad Software, San Diego, CA). RESULTS A total of 48 patients fulfilled the inclusion criteria and were enrolled in the study. Six patients were excluded for endometrial disynchrony or lack of material for histologic analysis. The demographics of the population, composed of 42 women are shown in Table 1. No difference was found among the groups when age, day of the biopsy by LH surge, or histologic dating was analyzed. All 42 samples were collected during the putative window of implantation (luteal days 7 10) from patients in whom the timing of biopsy was defined by a midcycle LH surge (luteal day 0) and confirmed by histologic criteria. Overall intraobserver and interobserver variation is shown in Figure 1, with HSCORE as the continuous variable. The correlation coefficients for intraobserver and interobserver variation were 0.92 and 0.84, respectively, for assessing 3 in the glands, yielding a index of 0.89 and 0.84 for intraobserver and interobserver variation, respectively. Immunohistochemical staining for the two epithelial cycledependent integrin subunits was performed on each biopsy. The expression of 1 integrin subunits shows that ovulation has occurred, and 3 is related to the window of implantation. As shown in Figure 2, there was significantly less overall 3 expression in the endometrial epithelium of women with hydrosalpinges and women with tubal phimosis when compared with fertile controls (P.0026). No difference was observed on the expression of 1 integrin subunit between groups. As expected, no expression of 1 was observed in the luminal epithelium of all groups. DISCUSSION Hydrosalpinx has different stages of classification for tubal damage, and because stages III and IV have an adverse effect on integrin expression, we considered the possibility that endometrial markers would also be affected by hydrosalpinx during its early stages (i.e., stage I). This hypothesis came from clinical observations that constant exposure to Chlamydia trachomatis leads to the production of increased levels of chlamydial heat shock proteins that elicit intense immune and inflammatory reactions. These reactions produce tissue scarring and endometrial and fallopian tube damage (19). Results of both epidemiologic studies and animal model studies are consistent with the hypothesis that both symptomatic and asymptomatic C. trachomatis infection of the female genital tract can induce reproductive tract damage (20). 190 Savaris et al. Integrins in tubal phimosis Vol. 85, No. 1, January 2006

4 FIGURE 1 Intraobserver (A) and interobserver (B) variation, according to HSCORE determination for assessment of 1 and 3 integrin subunit with immunohistochemistry. RFS and CGZ are observer initials. FIGURE 2 Semiquantitative HSCORE for 1 (A) and 3 (B) integrin subunits in endometrial samples of women with hydrosalpinges or tubal phimosis and in fertile controls during the putative window of implantation. *P.01, control vs. phimosis; **P.05, control vs. hydrosalpinx. To verify such influence on endometrial receptivity, we decided to use only the 1 and 3 integrins subunits for their unique characteristics. The 1 integrin subunit shows that ovulation has occurred, whereas 3 shows that the endometrium was receptive for implantation. The HSCORE was chosen because it is an established method for scoring the integrins. The consistency of our reading method can be verified by the overall correlation coefficients. For intraobserver and interobserver variation, the index was 0.92 and 0.84, respectively, which is in accordance with others (21). These results confirm the appropriateness of HSCORE as a quantification test. With our results, considering that the standard deviation of our controls was slightly different from that in the literature, we were able to detect a difference of 32% (instead of 22%) on HSCORE (with an error of 0.05 and error of 0.2) that tubal phimosis is associated with reduced expression of 3 integrin subunit during the window of implantation. Although the number of subjects is sufficient to detect a specific difference in HSCORE, one might say that 12 patients are too few to external validity. To the best of our knowledge, the data presented in this study represent the first published report of the detrimental effects of tubal phimosis on markers of uterine receptivity. The low 3 integrin subunit expression in endometrium is similar between patients with tubal phimosis and those with hydrosalpinx. As expected, no expression of 1 subunit was observed on the luminal site of all samples. The glandular expression of 1 subunit did not differ among the three groups, demonstrating that ovulation had occurred and that the samples were consistent to histologic results. These data also suggest that not all patients with tubal phimosis have an abnormal endometrium. In the present study, 33% (4 of 12) of the women with tubal phimosis had a normal integrin expression. This does not, however, ex- Fertility and Sterility 191

5 plain the infertility condition of those patients. It was interesting that almost one third of controls (5 of 19) were negative for 3 integrin subunit. The possible explanation for this finding could be related to the early endometrial biopsy (LH 7 8), although 2 patients had their endometrial biopsies performed closer to the putative closure of the window of implantation (LH 9 10). Eytan et al. (8) hypothesized that hydrosalpinx induces internal pressure within the fallopian tube and thus affects the normal pressure within the uterus. This reflux phenomenon would satisfactorily explain the associated reduced implantation rate in patients with large hydrosalpinx. Nevertheless, it does not explain why patients with tubal phimosis have difficulty becoming pregnant, because there is no accumulation of fluid in the fallopian tube. One possible explanation would be related to the production of heat shock protein by C. trachomatis. Heat shock protein elicits intense immune and inflammatory reactions, leading to tissue scarring and fallopian tube damage (19). Sharara et al. (22) found that the prevalence of elevated serum chlamydia IgG antibody in patients presenting for IVF was higher than in the general population. After treating these patients with doxycycline, the presence of elevated IgG antibodies against chlamydia was not associated with poor IVF outcome as compared with the control group. These investigators recommend that all couples with elevated titers for chlamydia or hydrosalpinx should be treated with doxycycline before IVF is attempted (22). In accordance with these results, Hurst et al. (23) offered extended antibiotic treatment with doxycycline as an alternative to tubal surgery, and compared with other non-hydrosalpinx tubal infertility patients, the outcome of IVF was similar across the groups. It is possible that our results represent another aspect of the studies described by Sharara and Hurst. The inflammation from acute or chronic bacterial infection seems to be a plausible explanation for the etiology of the infertility. The initial inflammation would probably induce the low 3 integrin subunit expression and alter the mechanism of implantation, even before the formation of large hydrosalpinx. This explanation does not fit in the case of large hydrosalpinges, in which salpingectomy restores normal expression of v 3 (12) and increases the success of IVF outcome (4). This study clearly shows that the different stages of hydrosalpinges have a detrimental effect on endometrial markers of receptivity, and the mechanical theory of reflux currents that might thrust embryos away from the implantation site is unlikely to explain all cases. Additional studies to verify the effect of chlamydia and heat shock protein on integrin expression might cast some light on this issue. REFERENCES 1. Donnez J, Casanas-Roux F. Microsurgery of distal tubal lesions. Analysis of 270 operated cases [French]. J Gynecol Obstet Biol Reprod (Paris). 1986;15: Camus E, Poncelet C, Goffin F, Wainer B, Merlet F, Nisand I, et al. Pregnancy rates after in-vitro fertilization in cases of tubal infertility with and without hydrosalpinx: a meta-analysis of published comparative studies. Hum Reprod 1999;14: Strandell A, Lindhard A. Hydrosalpinx and ART. Salpingectomy prior to IVF can be recommended to a well-defined subgroup of patients. Hum Reprod 2000;15: Johnson NP, Mak W, Sowter MC. Laparoscopic salpingectomy for women with hydrosalpinges enhances the success of IVF: a Cochrane review. Hum Reprod 2002;17: Mansour RT, Aboulghar MA, Serour GI, Riad R. Fluid accumulation of the uterine cavity before embryo transfer: a possible hindrance for implantation. J In Vitro Fert Embryo Transf 1991;8: Strandell A, Sjögren A, Bentin-Ley U, Thorburn J, Hamberger L, Brännström M. Hydrosalpinx fluid does not adversely affect the normal development of human embryos and implantation in vitro. Hum Reprod 1998;13: Granot I, Dekel N, Segal I, Fieldust S, Shoham Z, Barash A. Is hydrosalpinx fluid cytotoxic? Hum Reprod 1998;13: Eytan O, Azem F, Gull I, Wolman I, Elad D, Jaffa AJ. The mechanism of hydrosalpinx in embryo implantation. Hum Reprod 2001;16: Andersen AN, Yue Z, Meng FJ, Petersen K. Low implantation rate after in-vitro fertilization in patients with hydrosalpinges diagnosed by ultrasonography. Hum Reprod 1994;9: Watermeyer SR, Bhal K. Chronic vaginal discharge secondary to a hydrosalpinx. J Obstet Gynaecol 2002;22: Lessey BA, Castelbaum AJ, Wolf L, Greene W, Paulson M, Meyer WR, et al. Use of integrins to date the endometrium. Fertil Steril 2000;73: Meyer WR, Castelbaum AJ, Somkuti S, Sagoskin AW, Doyle M, Harris JE, et al. Hydrosalpinges adversely affect markers of endometrial receptivity. Hum Reprod 1997;12: Bildirici I, Bukulmez O, Ensari A, Yarali H, Gurgan T. A prospective evaluation of the effect of salpingectomy on endometrial receptivity in cases of women with communicating hydrosalpinges. Hum Reprod 2001;16: Noyes RW, Hertig AT, Rock J. Dating the endometrial biopsy. Fertil Steril 1950;1: Lessey BA, Castelbaum AJ, Sawin SW, Buck CA, Schinnar R, Bilker W, et al. Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 1994;79: Jekel JF, Elmore JG, Katz DL. Understanding and reducing errors in clinical medicine. In: Jekel JF, Elmore JG, Katz DL, eds. Epidemiology, biostatistics and preventive medicine. 1st ed. Philadelphia: W.B. Saunders, 1996: Jekel JF, Elmore JG, Katz DL. Sample size, randomization, and probability theory. In: Jekel JF, Elmore JG, Katz DL, eds. Epidemiology, biostatistics and preventive medicine. 1st ed. Philadelphia: W.B. Saunders, 1996: Lessey BA, Castelbaum A, Sawin SW, Sun J. Integrins as markers of uterine receptivity in women with primary unexplained infertility. Fertil Steril 1995;63: Ajonuma LC, Ng EH, Chan HC. New insights into the mechanisms underlying hydrosalpinx fluid formation and its adverse effect on IVF outcome. Hum Reprod Update 2002;8: Paavonen J, Eggert-Kruse W. Chlamydia trachomatis: impact on human reproduction. Hum Reprod Update 1999;5: Lessey BA, Castelbaum AJ, Wolf L, Greene W, Paulson M, Meyer WR, et al. Use of integrins to date the endometrium. Fertil Steril 2000;73: Sharara FI, Queenan JT Jr, Springer RS, Marut EL, Scoccia B, Scommegna A. Elevated serum Chlamydia trachomatis IgG antibodies. What do they mean for IVF pregnancy rates and loss? J Reprod Med 1997; 42: Hurst BS, Tucker KE, Awoniyi CA, Schlaff WD. Hydrosalpinx treated with extended doxycycline does not compromise the success of in vitro fertilization. Fertil Steril 2001;75: Savaris et al. Integrins in tubal phimosis Vol. 85, No. 1, January 2006

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