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Identification of main risk factors for tubal infertility*
FERTILITY AND STERILITY Copyright
©
Vol. 61, No.3, March 1994
1994 The American Fertility Society
Printed on acid-free paper in U. S. A.
Identification of main risk factors for tubal infertility*
Luis Bahamondes, M.D., Ph.D.t:j:§ Jose Geraldo Romanello Bueno, M.D., Ph.D.t Ellen Hardy, Ph.D.t:j:
Sergio Vera, B.Sc. t Eliane Pimentel, R.N.:j: Marcia Ramos, B.Sc.:j:
Centro de Pesquisas e Controle das Doencas Materno-Infantis, and Universidade Estadual de Campinas, Campinas, Brazil
Objective: To determine the relationship between some reproductive variables and infertility caused by tubal obstruction. Design: A retrospective, case-control study. Setting: A tertiary care university hospital that is a referral center for infertility patients. Participants: Subjects were interviewed between March 1990 and December 1991. Cases were 215 consecutively recruited infertile women with either evidence of tubal obstruction found at laparoscopy or hydrosalpinx diagnosed by hysterosalpingography. Women with a history of surgical sterilization were excluded. Controls, selected in the same hospital, were women in the puerperium who had no history of infertility. Two controls were matched by age at the time of tubal obstruction diagnosis to each case. Results: History of pelvic surgery and use of alcohol were significantly associated with the risk of infertility caused by tubal obstruction. The use of barrier, oral, and medroxyprogesterone acetate (MPA) contraceptives was associated with a protective effect. When only women with secondary infertility were analyzed, history of pelvic surgery and number of lifetime sexual partners were significant risk factors, and the previous use of oral contraceptives was the only protective factor. Conclusions: History of pelvic surgery was the most important risk factor for tubal infertility. All precautions must be taken to avoid infection and adhesion formation when pelvic surgery is performed. In addition, women can be protected from tubal infertility by using barrier, oral, or MPA contraceptive methods. Fertil Steril1994;61:478-82 Key Words: Infertility, tubal obstruction, risk factors
One of the main causes of infertility is tubal obstruction. The prevalence of this type of infertility varied greatly in the different countries in which it
Received May 24, 1993; revised and accepted November 8, 1993, * Supported in part by the Special Programme of Research, Development and Research Training in Human Reproduction, World Health Organization, award H9/181/670-89-Bras-3 and by the Programa Latinoamericano de Capacitacion e Investigacion en Reproduccion Humana (PLACIRH), award PLI 076/90. t Centro de Pesquisas e Controle das Doenc;as Materno-Infantis (CEMICAMP). :j: Departamento de Tocoginecologia, Faculdade de Ciencias Medicas, Universidade Estadual de Campinas. § Reprint requests: Luis Bahamondes, M.D., Ph.D., Centro de Pesquisas e Controle das Doenc;as Materno-Infantis, Caixa Postal 6181, 13081-970 Campinas, SP, Brazil.
478
Bahamondes et al.
Risk factors for tubal infertility
was studied. In developed countries, tubal obstruction was found in 36% of infertile women; however, in Asia this percentage reached 39%, in Latin America 44%, and in Africa 85% (1). Tubal infertility was associated with sexually transmitted diseases (STDs), multiple sexual partners, early age at first sexual intercourse, race, socioeconomic and marital status, level of education, previous use of contraceptive methods, septic abortion, smoking, alcoholism, and abdominal or pelvic surgery (2, 3). Tubal obstruction, a condition often regarded as synonymous with permanent sterility, may be prevented if risk factors of its development are identified. The purpose of this study was to identify the main risk factors for tubal infertility in a group of Brazilian women. Fertility and Sterility
Table 1 Percentage Distribution of Cases and Controls by Age and Education
Age :0;19 20 to 24 25 to 29 30 to 34 ~35
Mean SD Education (y)* None 1 to 4 5 to 8 9 to 11 No. of women
=
Cases
Controls
3.70 20.40 32.10 30.70 12.60 28.50 4.98
3.70 20.90 32.10 30.70 12.60 28.50 4.98
2.80 47.40 28.80 21.00 215
5.80 44.90 31.20 18.10 430
* Cases and controls are not significantly different, P 0.4178.
MATERIALS AND METHODS
A case-control study was carried out in Campinas, Brazil, and consisted of 215 consecutive cases of infertile women who were examined at the State University of Campinas Hospital between March 1990 and December 1991 and of 430 fertile controls. The patients presented with either unilateral or bilateral tubal obstruction found at laparoscopy or bilateral closed hydrosalpinx that had been diagnosed by hysterosalpingography. Tubal infertility was diagnosed in the women after they and their partners had completed an infertility evaluation, and no other demonstrable cause of infertility was found. Patients who had undergone surgical sterilization were excluded. Primary infertility was present in 107 cases. More than one half of the women (58.2%) had been infertile for 1 to 5 years. The average duration of infertility was 5.7 years. The mean age of the subjects at the time of tubal obstruction diagnosis was 28.5 years. Most women (70%) were white. Tubal obstruction was diagnosed by laparoscopy in 178 cases (82.8%), and bilateral occlusion was observed in 147 women (68.4%). Each case was matched with two controls. These women were the same age as their respective cases at diagnosis. Controls were selected in the same hospital, among women in the immediate puerperium, who had no history of infertility, and were of similar socioeconomic status. Age and education of cases and controls are shown in Table 1. The variables studied were divided into four groups. The first group included age at first interVol. 61, No.3, March 1994
course, number of lifetime sexual partners, practice of anal sex, and history of STDs. The second included history of abortion, both legal and illegal, and history of abdominal or pelvic surgery. Illegal abortion, reported by the women, was defined as voluntary interruption of pregnancy, performed by nonmedical personnel. Abdominal and pelvic surgeries, either documented in hospital records or reported by women, were defined, respectively, as surgery of the abdominal viscera, and any surgery of the uterus, ovaries, and fallopian tubes. The third group included previous use of barrier methods, oral contraceptive (OC) agents, natural methods, intrauterine device (IUD), and medroxyprogesterone acetate (MPA) contraceptives. The fourth group included smoking and alcohol use. The surgical history of the women included 5 unspecified laparotomies, 22 appendectomies, 8 bowel operations, 26 ovarian cyst excisions and/or wedge resections, and 8 ectopic pregnancy (EP) resolutions all performed by laparotomy. Data were collected by using a structured pretested form administered individually at the clinic by the authors. Study code numbers were used to ensure the respondents' anonymity. Multiple logistic regression procedures were used to calculate odds ratios (ORs) and to test all potential risk factors for tubal infertility. Initially, all the variables were included in the logistic analysis, and those that did not contribute significantly (P> 0.05) were eliminated in a stepwise manner, using the likelihood ratio test for determination of the best fitting model (4, 5). None of the cases with primary infertility had ever used an IUD or MP A; therefore, a new logistic regression was performed, considering only women with secondary infertility. RESULTS
The first model showed that a greater risk of tubal infertility was associated with alcohol consumption and history of abdominal and pelvic surgery. A moderate risk was observed in women who practiced anal sex frequently (at least one time per week), who had multiple lifetime sexual partners, or who reported a history of abortion when compared with those without these histories. A lower probability of developing the disease was observed in women with a history of having had a STD, of smoking, and of early age at first sexual intercourse. Among the contraceptives studied, barrier and hormonal methods, both OCs and MP A were found Bahamondes et al.
Risk factors for tubal infertility
479
Table 2 Risk Factors for Infertility Caused by Tubal Obstruction Variables
95% CI*
Variables
Coefficient
OR
1.0 11.2
5.1 to 24.7
1.0 8.0 11.0
Pelvic surgery Alcohol consumption Barrier contraceptives OCs MPA
2.7260 2.3087 -1.8053 -1.3218 -1.0642
15.27 10.06 0.16 0.27 0.35
4.8 to 13.4 4.8 to 25.3
1.0 3.6 4.6
2.0 to 6.8 1.5 to 13.6
1.0 1.4 1.7 4.2
0.9 to 2.2 1.0 to 2.9 1.8 to 9.7
1.0 3.3 4.0
1.9 to 5.8 1.9 to 8.7
1.0 3.4
1.1 to 10.6
1.0 2.1
1.0 to 4.3
1.0 1.9 1.9 1.9
1.4 to 2.7 1.3 to 2.7 1.1 to 3.2
1.0 1.6
1.1 to 2.4
1.0 0.6 0.5 0.4 0.3 0.2
0.2 0.2 0.2 0.2 0.1
OR
Alcohol consumption None Frequent Surgery history No Abdominal Pelvic Anal sex No Occasionally Frequently No. of lifetime sexual partners One Two Three Four or more Abortion history No abortion One Two or more Illegal abortion No abortion One or more History of STD No Yes Smoking habit No smoking Smoking 5 to 10 cigarettesjd 11 or more cigarettesjd Age at first intercourse 15 years old or older Up to 15 years old Contraceptive methods No IUD Natural Barrier Oral MPA
Table 3 Multiple Logistic Regression Model Including All Women
to to to to to
1.3 1.7 0.9 0.5 0.5
* CI, Confidence interval.
to protect against tubal obstruction. The use of IUDs and natural contraceptive methods were not associated with this protection (Table 2). The first logistic regression showed that only history of pelvic surgery and of alcohol consumption were significant. Barrier, OCs and MPA, were protective factors (Table 3). Regression considering only secondary infertility cases showed that history of pelvic surgery and greater number oflifetime sexual partners were risk factors and that a previous use of OCs was the only protective factor (Table 4). DISCUSSION
In our study, univariate analysis showed that sexual activity at an early age, a greater number of 480
Bahamondes et al.
Risk factors for tubal infertility
95% CI 6.0 4.0 0.1 0.2 0.1
to to to to to
38.6 25.3 0.5 0.3 0.8
lifetime sexual partners, practice of anal sex, history of STD(s) and of abortion, and smoking and alcohol consumption were associated with tubal infertility. Some of these variables are clearly related to reproductive tract infection; however, it is difficult to link smoking and alcohol use directly to reproductive tract infection. Sexual activity at an early age and a greater number of lifetime sexual partners are probably correlated. Consequently, women who initiate sexual activity at an early age probably will have more sexual partners and, subsequently, an increased STD and pelvic inflammatory disease (PID) risk (2, 3). The practice of anal sex could also increase this risk of infection. History of STD was found to be a lowrisk variable. It was not a higher risk probably because subjects were not aware of and did not refer to asymptomatic STD episodes (6). Our study showed the association between illegal abortion and tubal obstruction. In countries in which abortion is legal and performed by physicians, the procedure does not contribute significantly to an increase in tubal infertility risk (7). Barrier contraceptive methods have been shown to protect against STDs and to reduce PID risk (8). This effect is evident in condom users, especially when condoms are lubricated with nonoxynol-9, which has a germicide effect (9). Our results confirmed this protective effect. Oral contraceptives and MP A also were found to be protective, probably because of their progestinic component. This hormone thickens cervical mucus, blocking the ascent of the etiologic agents of PID to the upper genital tract (10, 11). In addition, hormonal contraceptives
Table 4 Multiple Logistic Regression Model Considering Only Women With Secondary Infertility Variables
Coefficient
OR
95% CI
Pelvic surgery No. of sexual partners OCs
2.6637 1.2172 -0.8814
14.35 3.38 0.41
5.2 to 39.4 2.1 to 5.5 0.3 to 0.7
Fertility and Sterility
reduce menstrual blood flow, decreasing the medium available for bacterial growth. However, caution is necessary when interpreting the protective effect of MPA because this effect disappeared when only subjects with secondary infertility were considered. Previous use of copper IUD was not a risk factor, not even when only women with secondary infertility were analyzed. Copper IUDs have not been associated with high termination rate for infection, with an increase in PID prevalence, or with tubal infertility. This may be because copper ions produce an aseptic inflammatory reaction in utero, rendering it unfit for the development of pathogenic bacteria (12, 13). Smoke by-products seem to exert some direct influence over the reproductive system. The relative risk of tubal obstruction in primary infertility was higher among smokers than among women who had abandoned the habit (14). Our study showed a double risk for smokers in the univariate analysis but none in the multivariate analysis. This habit is probably linked with tubal obstruction through its association with other social behaviors . The logistic regression analysis including all women showed that history of pelvic surgery and alcohol consumption remained the only risk factors. Barrier methods, OCs, and MP A were protective. When only women with secondary infertility were considered, history of pelvic surgery and greater number oflifetime sexual partners were risk factors, and only OCs were protective. History of pelvic surgery was a risk of tubal obstruction. This was also reported by Lalos (15), who found that EP and ovarian cysts were the most frequent indications for laparotomies. During their reproductive years, many women undergo gynecological surgeries. These carry a potential risk of causing tubal obstruction through peritoneal adhesions (16). In Brazil, many women are submitted to unnecessary ovarian follicular cyst excision and ovarian wedge resection. It is important to avoid unjustified pelvic surgery, especially before or during women's reproductive years. If surgery is necessary, safe surgical techniques should be used to reduce trauma and adhesions. Alcohol consumption was a risk factor in our study, but it is difficult to explain how this habit could result in tubal obstruction because it does not cause infection. The effect of alcohol consumption may be the result of its association with other high risk social habits. In addition, women may be more Vol. 61, No.3, March 1994
inclined to admit that they drink alcohol than to inform an interviewer about the actual number of their lifetime sexual partners or histories of illegal abortion. It is necessary to point out that our controls may have changed their alcohol consumption and smoking habits during pregnancy, which could partially explain the high OR for tubal infertility in smokers and women who consumed alcohol. Almost all reproductive tract infections are preventable. Prevention should involve the following three levels: [1] primary, with the objective of blocking transmission of the disease; [2] secondary, to avoid the ascent of infection to the upper genital tract; and [3] tertiary, to impede progression to the fallopian tubes, thereby avoiding consequent obstruction and infertility. In addition, it is necessary that the community adopt a better understanding of the process through which changes in sexual behavior occur. It is imperative that a comprehensive educational process be established, starting in adolescence, with the objective of sensitizing the population to the risks of early initiation a sexual activity, frequent change of sexual partners, and practice of anal sex and unprotected intercourse. Although reproductive tract infections are important causes of tubal obstruction, it is important to emphasize that pelvic surgery is one of the principal etiologic agents for this kind of infertility.
REFERENCES 1. Cates W, Farley TM, Rowe P J. Worldwide patterns of infer-
tility: is Africa different? Lancet 1985;2:596-8. 2. Aral SO, Soskoline V, Joesoef RM, O'Reilly KR. Sex partner recruitment as risk factor for STD: clustering of risky modes. Sex Transm Dis 1991;18:10-7. 3. Cates W, Rolfs RT, Aral SO. Sexually transmitted diseases, pelvic inflammatory disease and infertility: an epidemiologic update. Epidemiol Rev 1990;12:199-220. 4. Schlesselman JJ, Stolley PD. Case-control studies-design, conduct, analysis. New York: Oxford University Press, 1982. 5. Cox DR. The analysis of binary data. 1th ed. London: Methuen and Co. Ltd., 1970. 6. Maslow A, Davis C, Choong J, Wyrick P. Estrogen enhances attachment of Chlamydia trachomatis to human endometrial epithelial cells in vitro. Am J Obstet Gynecol 1988;159:1006-14. 7. Daling JR, Weiss NS, Voigt L, Spadoni LR, Soderstrom R, Moore DE et al. Tubal infertility in relation to prior induced abortion. Fertil Steril 1985;43:389-94. 8. Washington AE, Aral S, Wolner-Hansen P, Grimes S, Holmes K. Assessing risk for pelvic inflammatory disease and its sequelae. JAMA 1991;266:2581-6.
Bahamondes et al.
Risk factors for tubal infertility
481
9. Washington AE, Cates W, Wasserheit J. Preventing pelvic inflammatory disease. JAMA 1991;266:2574-80. 10. Ruden G, Fahraeus L, Molin L, Ahman K. Do contraceptives influence the incidence of acute pelvic inflammatory disease in women with gonorrhoea? Contraception 1979;20: 149-57. 11. Gray RH. Reduced risk of pelvic inflammatory disease with injectable contraceptives. Lancet 1985;1:1046. 12. Cramer DW, Schiff I, Schoenbaum SC, Gibson M, Belisle S, Albrecht B, et al. Tubal infertility and the intrauterine device. N Engl J Med 1985;312:941-7.
482
Bahamondes et al.
Risk factors for tubal infertility
13. Diaz J, Pinto-Neto AM, Diaz M, Marchi N, Bahamondes L. Long-term evaluation of the clinical performance of the TCu 200B and the 380A in Campinas, Brazil. Adv Contracept 1992;8:67-72. 14. Laurent SL, Thompson SJ, Addy C, Garrison CZ, Moore EE. An epidemiologic study of smoking and primary infertility in women. Fertil SteriI1992;57:565-72. 15. Lalos O. Risk factors for tubal infertility among infertile and fertile women. Eur J Obstet Gynecol Reprod Bioi 1988;29:129-36. 16. Weibel MA, Majno G. Peritoneal adhesions and their relation to abdominal surgery. Am J Surg 1973;126:345-53.
Fertility and Sterility
©
Vol. 61, No.3, March 1994
1994 The American Fertility Society
Printed on acid-free paper in U. S. A.
Identification of main risk factors for tubal infertility*
Luis Bahamondes, M.D., Ph.D.t:j:§ Jose Geraldo Romanello Bueno, M.D., Ph.D.t Ellen Hardy, Ph.D.t:j:
Sergio Vera, B.Sc. t Eliane Pimentel, R.N.:j: Marcia Ramos, B.Sc.:j:
Centro de Pesquisas e Controle das Doencas Materno-Infantis, and Universidade Estadual de Campinas, Campinas, Brazil
Objective: To determine the relationship between some reproductive variables and infertility caused by tubal obstruction. Design: A retrospective, case-control study. Setting: A tertiary care university hospital that is a referral center for infertility patients. Participants: Subjects were interviewed between March 1990 and December 1991. Cases were 215 consecutively recruited infertile women with either evidence of tubal obstruction found at laparoscopy or hydrosalpinx diagnosed by hysterosalpingography. Women with a history of surgical sterilization were excluded. Controls, selected in the same hospital, were women in the puerperium who had no history of infertility. Two controls were matched by age at the time of tubal obstruction diagnosis to each case. Results: History of pelvic surgery and use of alcohol were significantly associated with the risk of infertility caused by tubal obstruction. The use of barrier, oral, and medroxyprogesterone acetate (MPA) contraceptives was associated with a protective effect. When only women with secondary infertility were analyzed, history of pelvic surgery and number of lifetime sexual partners were significant risk factors, and the previous use of oral contraceptives was the only protective factor. Conclusions: History of pelvic surgery was the most important risk factor for tubal infertility. All precautions must be taken to avoid infection and adhesion formation when pelvic surgery is performed. In addition, women can be protected from tubal infertility by using barrier, oral, or MPA contraceptive methods. Fertil Steril1994;61:478-82 Key Words: Infertility, tubal obstruction, risk factors
One of the main causes of infertility is tubal obstruction. The prevalence of this type of infertility varied greatly in the different countries in which it
Received May 24, 1993; revised and accepted November 8, 1993, * Supported in part by the Special Programme of Research, Development and Research Training in Human Reproduction, World Health Organization, award H9/181/670-89-Bras-3 and by the Programa Latinoamericano de Capacitacion e Investigacion en Reproduccion Humana (PLACIRH), award PLI 076/90. t Centro de Pesquisas e Controle das Doenc;as Materno-Infantis (CEMICAMP). :j: Departamento de Tocoginecologia, Faculdade de Ciencias Medicas, Universidade Estadual de Campinas. § Reprint requests: Luis Bahamondes, M.D., Ph.D., Centro de Pesquisas e Controle das Doenc;as Materno-Infantis, Caixa Postal 6181, 13081-970 Campinas, SP, Brazil.
478
Bahamondes et al.
Risk factors for tubal infertility
was studied. In developed countries, tubal obstruction was found in 36% of infertile women; however, in Asia this percentage reached 39%, in Latin America 44%, and in Africa 85% (1). Tubal infertility was associated with sexually transmitted diseases (STDs), multiple sexual partners, early age at first sexual intercourse, race, socioeconomic and marital status, level of education, previous use of contraceptive methods, septic abortion, smoking, alcoholism, and abdominal or pelvic surgery (2, 3). Tubal obstruction, a condition often regarded as synonymous with permanent sterility, may be prevented if risk factors of its development are identified. The purpose of this study was to identify the main risk factors for tubal infertility in a group of Brazilian women. Fertility and Sterility
Table 1 Percentage Distribution of Cases and Controls by Age and Education
Age :0;19 20 to 24 25 to 29 30 to 34 ~35
Mean SD Education (y)* None 1 to 4 5 to 8 9 to 11 No. of women
=
Cases
Controls
3.70 20.40 32.10 30.70 12.60 28.50 4.98
3.70 20.90 32.10 30.70 12.60 28.50 4.98
2.80 47.40 28.80 21.00 215
5.80 44.90 31.20 18.10 430
* Cases and controls are not significantly different, P 0.4178.
MATERIALS AND METHODS
A case-control study was carried out in Campinas, Brazil, and consisted of 215 consecutive cases of infertile women who were examined at the State University of Campinas Hospital between March 1990 and December 1991 and of 430 fertile controls. The patients presented with either unilateral or bilateral tubal obstruction found at laparoscopy or bilateral closed hydrosalpinx that had been diagnosed by hysterosalpingography. Tubal infertility was diagnosed in the women after they and their partners had completed an infertility evaluation, and no other demonstrable cause of infertility was found. Patients who had undergone surgical sterilization were excluded. Primary infertility was present in 107 cases. More than one half of the women (58.2%) had been infertile for 1 to 5 years. The average duration of infertility was 5.7 years. The mean age of the subjects at the time of tubal obstruction diagnosis was 28.5 years. Most women (70%) were white. Tubal obstruction was diagnosed by laparoscopy in 178 cases (82.8%), and bilateral occlusion was observed in 147 women (68.4%). Each case was matched with two controls. These women were the same age as their respective cases at diagnosis. Controls were selected in the same hospital, among women in the immediate puerperium, who had no history of infertility, and were of similar socioeconomic status. Age and education of cases and controls are shown in Table 1. The variables studied were divided into four groups. The first group included age at first interVol. 61, No.3, March 1994
course, number of lifetime sexual partners, practice of anal sex, and history of STDs. The second included history of abortion, both legal and illegal, and history of abdominal or pelvic surgery. Illegal abortion, reported by the women, was defined as voluntary interruption of pregnancy, performed by nonmedical personnel. Abdominal and pelvic surgeries, either documented in hospital records or reported by women, were defined, respectively, as surgery of the abdominal viscera, and any surgery of the uterus, ovaries, and fallopian tubes. The third group included previous use of barrier methods, oral contraceptive (OC) agents, natural methods, intrauterine device (IUD), and medroxyprogesterone acetate (MPA) contraceptives. The fourth group included smoking and alcohol use. The surgical history of the women included 5 unspecified laparotomies, 22 appendectomies, 8 bowel operations, 26 ovarian cyst excisions and/or wedge resections, and 8 ectopic pregnancy (EP) resolutions all performed by laparotomy. Data were collected by using a structured pretested form administered individually at the clinic by the authors. Study code numbers were used to ensure the respondents' anonymity. Multiple logistic regression procedures were used to calculate odds ratios (ORs) and to test all potential risk factors for tubal infertility. Initially, all the variables were included in the logistic analysis, and those that did not contribute significantly (P> 0.05) were eliminated in a stepwise manner, using the likelihood ratio test for determination of the best fitting model (4, 5). None of the cases with primary infertility had ever used an IUD or MP A; therefore, a new logistic regression was performed, considering only women with secondary infertility. RESULTS
The first model showed that a greater risk of tubal infertility was associated with alcohol consumption and history of abdominal and pelvic surgery. A moderate risk was observed in women who practiced anal sex frequently (at least one time per week), who had multiple lifetime sexual partners, or who reported a history of abortion when compared with those without these histories. A lower probability of developing the disease was observed in women with a history of having had a STD, of smoking, and of early age at first sexual intercourse. Among the contraceptives studied, barrier and hormonal methods, both OCs and MP A were found Bahamondes et al.
Risk factors for tubal infertility
479
Table 2 Risk Factors for Infertility Caused by Tubal Obstruction Variables
95% CI*
Variables
Coefficient
OR
1.0 11.2
5.1 to 24.7
1.0 8.0 11.0
Pelvic surgery Alcohol consumption Barrier contraceptives OCs MPA
2.7260 2.3087 -1.8053 -1.3218 -1.0642
15.27 10.06 0.16 0.27 0.35
4.8 to 13.4 4.8 to 25.3
1.0 3.6 4.6
2.0 to 6.8 1.5 to 13.6
1.0 1.4 1.7 4.2
0.9 to 2.2 1.0 to 2.9 1.8 to 9.7
1.0 3.3 4.0
1.9 to 5.8 1.9 to 8.7
1.0 3.4
1.1 to 10.6
1.0 2.1
1.0 to 4.3
1.0 1.9 1.9 1.9
1.4 to 2.7 1.3 to 2.7 1.1 to 3.2
1.0 1.6
1.1 to 2.4
1.0 0.6 0.5 0.4 0.3 0.2
0.2 0.2 0.2 0.2 0.1
OR
Alcohol consumption None Frequent Surgery history No Abdominal Pelvic Anal sex No Occasionally Frequently No. of lifetime sexual partners One Two Three Four or more Abortion history No abortion One Two or more Illegal abortion No abortion One or more History of STD No Yes Smoking habit No smoking Smoking 5 to 10 cigarettesjd 11 or more cigarettesjd Age at first intercourse 15 years old or older Up to 15 years old Contraceptive methods No IUD Natural Barrier Oral MPA
Table 3 Multiple Logistic Regression Model Including All Women
to to to to to
1.3 1.7 0.9 0.5 0.5
* CI, Confidence interval.
to protect against tubal obstruction. The use of IUDs and natural contraceptive methods were not associated with this protection (Table 2). The first logistic regression showed that only history of pelvic surgery and of alcohol consumption were significant. Barrier, OCs and MPA, were protective factors (Table 3). Regression considering only secondary infertility cases showed that history of pelvic surgery and greater number oflifetime sexual partners were risk factors and that a previous use of OCs was the only protective factor (Table 4). DISCUSSION
In our study, univariate analysis showed that sexual activity at an early age, a greater number of 480
Bahamondes et al.
Risk factors for tubal infertility
95% CI 6.0 4.0 0.1 0.2 0.1
to to to to to
38.6 25.3 0.5 0.3 0.8
lifetime sexual partners, practice of anal sex, history of STD(s) and of abortion, and smoking and alcohol consumption were associated with tubal infertility. Some of these variables are clearly related to reproductive tract infection; however, it is difficult to link smoking and alcohol use directly to reproductive tract infection. Sexual activity at an early age and a greater number of lifetime sexual partners are probably correlated. Consequently, women who initiate sexual activity at an early age probably will have more sexual partners and, subsequently, an increased STD and pelvic inflammatory disease (PID) risk (2, 3). The practice of anal sex could also increase this risk of infection. History of STD was found to be a lowrisk variable. It was not a higher risk probably because subjects were not aware of and did not refer to asymptomatic STD episodes (6). Our study showed the association between illegal abortion and tubal obstruction. In countries in which abortion is legal and performed by physicians, the procedure does not contribute significantly to an increase in tubal infertility risk (7). Barrier contraceptive methods have been shown to protect against STDs and to reduce PID risk (8). This effect is evident in condom users, especially when condoms are lubricated with nonoxynol-9, which has a germicide effect (9). Our results confirmed this protective effect. Oral contraceptives and MP A also were found to be protective, probably because of their progestinic component. This hormone thickens cervical mucus, blocking the ascent of the etiologic agents of PID to the upper genital tract (10, 11). In addition, hormonal contraceptives
Table 4 Multiple Logistic Regression Model Considering Only Women With Secondary Infertility Variables
Coefficient
OR
95% CI
Pelvic surgery No. of sexual partners OCs
2.6637 1.2172 -0.8814
14.35 3.38 0.41
5.2 to 39.4 2.1 to 5.5 0.3 to 0.7
Fertility and Sterility
reduce menstrual blood flow, decreasing the medium available for bacterial growth. However, caution is necessary when interpreting the protective effect of MPA because this effect disappeared when only subjects with secondary infertility were considered. Previous use of copper IUD was not a risk factor, not even when only women with secondary infertility were analyzed. Copper IUDs have not been associated with high termination rate for infection, with an increase in PID prevalence, or with tubal infertility. This may be because copper ions produce an aseptic inflammatory reaction in utero, rendering it unfit for the development of pathogenic bacteria (12, 13). Smoke by-products seem to exert some direct influence over the reproductive system. The relative risk of tubal obstruction in primary infertility was higher among smokers than among women who had abandoned the habit (14). Our study showed a double risk for smokers in the univariate analysis but none in the multivariate analysis. This habit is probably linked with tubal obstruction through its association with other social behaviors . The logistic regression analysis including all women showed that history of pelvic surgery and alcohol consumption remained the only risk factors. Barrier methods, OCs, and MP A were protective. When only women with secondary infertility were considered, history of pelvic surgery and greater number oflifetime sexual partners were risk factors, and only OCs were protective. History of pelvic surgery was a risk of tubal obstruction. This was also reported by Lalos (15), who found that EP and ovarian cysts were the most frequent indications for laparotomies. During their reproductive years, many women undergo gynecological surgeries. These carry a potential risk of causing tubal obstruction through peritoneal adhesions (16). In Brazil, many women are submitted to unnecessary ovarian follicular cyst excision and ovarian wedge resection. It is important to avoid unjustified pelvic surgery, especially before or during women's reproductive years. If surgery is necessary, safe surgical techniques should be used to reduce trauma and adhesions. Alcohol consumption was a risk factor in our study, but it is difficult to explain how this habit could result in tubal obstruction because it does not cause infection. The effect of alcohol consumption may be the result of its association with other high risk social habits. In addition, women may be more Vol. 61, No.3, March 1994
inclined to admit that they drink alcohol than to inform an interviewer about the actual number of their lifetime sexual partners or histories of illegal abortion. It is necessary to point out that our controls may have changed their alcohol consumption and smoking habits during pregnancy, which could partially explain the high OR for tubal infertility in smokers and women who consumed alcohol. Almost all reproductive tract infections are preventable. Prevention should involve the following three levels: [1] primary, with the objective of blocking transmission of the disease; [2] secondary, to avoid the ascent of infection to the upper genital tract; and [3] tertiary, to impede progression to the fallopian tubes, thereby avoiding consequent obstruction and infertility. In addition, it is necessary that the community adopt a better understanding of the process through which changes in sexual behavior occur. It is imperative that a comprehensive educational process be established, starting in adolescence, with the objective of sensitizing the population to the risks of early initiation a sexual activity, frequent change of sexual partners, and practice of anal sex and unprotected intercourse. Although reproductive tract infections are important causes of tubal obstruction, it is important to emphasize that pelvic surgery is one of the principal etiologic agents for this kind of infertility.
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