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Factors That Predispose to Premature Rupture of the Fetal Membranes
research and studies Factors That Predispose to Premature Rupture of the Fetal Membranes BONNIE FLOOD, RNC, MSN, AND RICHARD L. NAEYE, M D Causes of premature rupture of the fetal membranes were explored in a study of 25,820 pregnancies. Fourteen risk factors were analyzed using multivariate analysis. The following maternal factors had a positive association with premature ruptures: advanced maternal age, non-white race, multiparity, instrumentationof the cervix prior to pregnancy, cigarette smoking, incompetent cervix, low pregnancy weight gain, and recent coitus.
The cause of spontaneous rupture of the fetal membranes prior to the onset of labor is usually unexplained despite many published theories about its genesis. Physical and chemical characteristics of the membranes have all been examined as possible T h e present study examined 14 factors as possible risks in the genesis of premature membrane rupture: maternal age, race, parity, mother's marital status, her education and that of the infant's father, family income, prior instrumentation of the cervix, prepregnancy body weight, pregnancy weight gain, cigarette smoking during pregnancy, incompetent cervix, coitus within a few days of delivery, and length of gestation at the time of delivery.
Definition of Terms PROM: rupture of the fetal membranes prior to the onset of labor. Preterm PROM: rupture of the fetal membranes less than 259 days from the start of the last menstrual period.. Recent coitus: coitus that took place during the ten days before delivery. Chorioamnionitis: documented acute inflammatory cells spread diffusely along the surface of the chorion in the extraplacental membranes. Cervical instrumentation: dilatation and curettage or cervical biopsy before pregnancy. Data were not available to distinguish between cervical cone biopsies and punch biopsies.
Data Collection and Analysis Adapted with permission from Naeye RL. Factors that predispose to premature rupture of the fetal membranes. Obstet Gynecol 1982; 60:93. Submitted: August 1982. Accepted with revisions: May 1983.
March/April 1984JOGN Nursing
Data from a large prospective study were used in the analyses. The Collaborative Perinatal Project of the National Institute of Neurological and Communicative Dis-
orders and Stroke recorded information on gestation, labor, delivery, and the neonatal period in patients at 12 medical school-affiliated hospitals in different regions of the United States between 1959 and 1966. T h e current analyses included 25,820 singleton gestations that resulted in spontaneous deliveries. Pregnancies complicated by hydramnios or those that produced neonates with congenital malformations were excluded. Multivariate analysis was used to separate the individual effects of various factors on premature membrane ruptures.
Results Five thousand two hundred thirty of the women had two successive singleton births in the study. When preterm PROM was present in the first of these pregnancies, the recurrence rate was 2 1% in the second.'' When the first pregnancy went to term without PROM, only 4% of the next pregnancies ended with preterm PROM.''
119
fable 1. Factors Included in Multivariate Analysis for Relationship to Premature Rupture of the Fetal Membranes
Beta Values Length of gestation Maternal age Race, white Panty Prior cervical instrumentation Cigarette smoking during pregnancy Incompetent cervix Maternal pregnancy weight gain Recent coitus Maternal prepregnancy body weight Family income Years of education, father of baby Mother of baby unmarried Years of education, mother of baby
-0.087 P +0.074 P -0.052 P +0.045 P
< 0.001 < 0.001
+0.039 P < 0.001
Preterm delivery Older mothers Non-whites Multiparous women Prior instrumentation
+0.033P < 0.001 +0.019P < 0.01
Cigarette smoking Incompetent cervix
-0.015 +0.014
< 0.001
< 0.001
P < 0.05 P < 0.05
Low weight gain Recent coitus
+0.010P < 0.1 -0.005 P > 0.1
Overweight women
-0.004 P > 0.1 +0.004 P > 0.1
-0.002 P > 0.1
As might be expected, there was a strong association of PROM with preterm labor and delivery (Table 1). Other factors that had a strong, seemingly independent correlation with PROM were advanced maternal age, non-white mother, multiparity, instrumentation of the cervix before pregnancy, cigarette smoking, incompetent cervix, low pregnancy weight gain, and recent coitus. Discussion
T h e increased frequency of PROM in older mothers may indicate that fetal membranes are less strong in older than in young mothers. Findings in the study support the possibility that prior damage to the cervix or to the cervical canal by surgical instrumentation predisposes to PROM.’+’’ A study is needed that differentiates among various types of surgical instrumentation to assess fully this risk. Damage to the cervix may also be the explanation for the increase in PROM with increasing parity.
120
Premature Membrane Rupture Associated With
This study confirms previous reports that PROM is more frequent in women who smoke than in nonsmokers.’O~’’ However, the clinical significance of this finding is uncertain because it is present only in full-term gestations. l o T h e finding that PROM is associated with recent coitus differs from the reports of other investigators who have reported that coitus has no adverse effects.I2-l4 Orgasm can cause uterine contractions but it is far from certain that these contractions are strong enough to rupture normal membrane^.'^ A prospective study found that orgasm was an important cofactor with chorioamnionitis in the high frequency of premature membrane ruptures that follow coitus.I6 This raises the possibility that membranes locally weakened by infection are more susceptible to being ruptured by uterine contractions than uninfected membranes. Without female orgasm, seminal fluid does not ap ear to weaken the membranes. Other evidence indicates that
’r
chorioamnionitis, which is sometimes caused by coitus, can predispose to PROM.6-s*’sIn one study, chorioamnionitis was twice as frequent in membranes that ruptured just before the onset of labor as in membranes that ruptured just after labor began.” This suggests that chorioamnionitis antedated about half of the membrane ruptures that took place before the onset of labor. Why are the coital findings in the present study so different from those in previous studies? Using most of the same data base, Naeye previously reported that coitus did not increase the frequency of PROM.” These conflicting results are due to the different time frames in which coital data were collected in the two studies. In the previous study, Naeye used coital data from the last clinic visit, which usually reflected coital activity between the 30th and 10th days before delivery. Many women who had coitus before the last clinic visit reported no coitus between the last clinic visit and delivery. Those who continued coitus after the last clinic visit had a greater frequency of premature membrane ruptures than those who discontinued coitus after the last visit. The only other large population studies on the effects of coitus on the fetus are those of Mills et al. and of Zachau-Christiansen and Ross. 12*20Millset al. studied 10,98 1 pregnancies and collected coital data after delivery by asking the question, “In what months did you not have coitus during pregnancy?” An inherent problem with this method of data collection is that it depends on the long-term memory of the patient and one cannot be sure that a woman will give truthful information if her infant has been born prematurely, is sick, or has died. In addition, the month-long time frame that Mills et al. selected for their question is too long. It dilutes most of the adverse effects of
March/April 1984 JOGN Nursing
coitus, which last for only about seven days after the coital act.'6 In the study described in this article, women were asked at each clinic visit and at delivery how many times they had had coitus since the last clinic visit. Zachau-Christiansen and Ross found that women who continued coitus during pregnancy had a 40% greater frequency of newborns weighing under 2500 gm and nearly twice as many fetal/neonatal losses as mothers who discontinued coitus during pregnancy." Two additional studies, by Perkins and by Rayburn and Wilson, claim that coitus has no adverse effects during pregnan~y.''.'~Neither of these studies has enough cases to prove or disprove their thesis. Implications for Nursing Practice T h e risks of smoking to women's health in general and to the fetus during pregnancy have been well established." Counseling regarding the risks of smoking should be an important part of total health care in pregnancy. In this counseling, the nurse should not tell the woman that stopping smoking will prevent PROM because it has many other causes, and it is far from certain that smoking is involved in preterm PROM. Early in the prenatal period, the nurse's pregnancy care plan should include a discussion about smoking and its potential adverse effects, reference materials for the patient to take home to read after the discussion, and a list of resources that the patient could seek out to assist her to quit, or at least reduce, her smoking. Supporting and praising genuine efforts by the patient to try to stop smoking as pregnancy progresses can be helpful reinforcers. The nurse should set a positive example by not smoking in the gravida's presence, and no smoking pol-
March/April 1984 JOCN Nursing
icies should be enforced in the health-care environment. Pregnancy is a time of increased motivation for most women, an ideal time for the nurse to help the gravida understand that the risks of smoking to both herself and her fetus exceed the benefits. Should women be advised to discontinue coitus or otherwise change their sexual practices during pregnancy? T h e association between recent coitus and PROM and other adverse outcomes, however strong, does not constitute proof of a causal relationship. Such proof can be established only by intervention studies that prevent the adverse outcomes. Several such intervention studies are now in progress. However, the process for the nurse in providing routine counseling regarding sexuality in pregnancy may include Assessing the woman's level of satisfaction with her sexual relationship. This may change in each trimester as the patient's responses often change as pregnancy progresses. Counseling if the woman identifies areas in which she would like to change aspects of her sexual relationship, i e . , discussing pregnancy comfort measures, such as coital positions, vaginal lubrication, or alternatives to coitus if the patient is too uncomfortable, or giving permission to experience normal changes in sexual feelings throughout pregnancy. Determining if the patient has specific questions or concerns regarding her sexual activity, i.e., fears about harming the fetus, feeling disinterested or unsatisfied with coitus, and then planning for her individual needs accordingly. Identifying patients who present with a previous history of preterm PROM. T h e present study
demonstrates a strong tendency for recurrence in a subsequent pregnancy. Therefore, until more information is available, prenatal sexual counseling for these patients should emphasize the potential benefits of noncoital sexual alternatives after the first trimester of pregnancy. The question of whether or not coitus is risky during pregnancy has been in the news, so many patients are aware of it. For women who are not at risk, the benefits of a sexual relationship, with or without coitus, should be recognized and valued when it promotes feelings of security, love, affection, and tenderness. Conclusion .
Overall, the current study found a remarkable tendency for premature ruptures to repeat in successive pregnancies. To date, most non-epidemiologic research has been directed toward evaluating the strength or the collagen content of the remaining membranes on the possibility that a deficiency of collagen or abnormal collagen might be responsible for the ruptures. These studies have usually found no difference between membranes that ruptured prematurely and those that ruptured after the onset of labor.' These negative findings raise the possibility that localized defects rather than generalized weaknesses in the membranes are responsible for most premature ruptures. The rupture, by passing through these areas of defect, in turn destroys the damaged site. These localized abnormalities are far more difficult to study, but future research should give them more consideration because they are likely to hold the key to many of the ruptures that are currently unexplained. Nursing care for the uncomplicated pregnant patient should focus on the application of research data to the clinical situa-
121
tion in t h e context of t h e risk-benefit ratio for th e patient.
References 1 . Danforth DN, Hull RW. T h e microscopic anatomy of the fetal membranes with particular reference to the detailed structure of the amnion. Am J Obstet Gynecol
1958;75:536-47. 2. Embrey MP. On the strength of the foetal membranes. Br J Obstet Gynaecol 1954;6 1 :793-6. 3. Al-Zais NS, Bou-Resli MN, Goldspink G. Bursting pressure and collagen content of fetal membranes and their relation to premature rupture of the membranes. Br J Obstet Gynaecol 1980; 87:227-9. 4. Lavery JP, Miller CE. Deformation and creep in the human chorioamniotic sac. Am J Obstet Gynecol 1979;134:366-75. 5. Bourne G. The human amnion and chorion. London: Lloyd-Luke, 1962:175-92. 6. Artal R, Burgeson RE, Hobel CJ, et al. An in vitro model for the study of enzymatically mediated biomechanical changes in the chorioamniotic membranes. Am J Obstet Gynecol 1979;133:656-9. 7. Lukac J, Koren E. Mechanism of liquefaction of the human ejaculate. 11. Role of collagenase-like peptidase and seminal proteinase. J Reprod Fertil 1979;56:501-6. 8. Koren E, Milkovic S. Collagenase-
like peptidase in human, rat and bull spermatozoa. J Reprod Fertil 1973;32:349-56. 9. Evaldson G, Lagrelius A, Winiarski J . Premature rupture of the membranes. Acta Obstet Gynecol Scand 1980;59:385-93. 10. Naeye RL. Factors that predispose to premature rupture of the fetal membranes. Obstet Gynecol 1982;60:93-7. 1 1 . Meyer MB, Tonascia JA. Maternal smoking pregnancy complications and perinatal mortality. Am J Obstet Gynecol 1977;128:494-502. 12. Mills JL, Harlap S, Harley EE. Should coitus late in pregnancy be discouraged? Lancet 198 1 ;2: 1368. 13. Perkins RP. Sexual behavior and response in relation to complications of pregnancy. Am J Obstet Gynecol 1979; 134:498-505. 14. Rayburn WR, Wilson EA. Coital activity and premature delivery. Am J Obstet Gynecol 1980; 137: 972-4. 15. Goodlin RC, Schmidt W, Creevy DC. Uterine tension and fetal heart rate during maternal orgasm. Obstet Gynecol 1972;39:125-7. 16. Naeye RL, Ross S. Coitus and chorioamnionitis, a prospective study. Early Human Develop 1982;6:917. 17. Lavery JP, Miller CE. Effect of prostaglandin and seminal fluid on human chorioamnionitis membranes. JAMA 198 1 ;245:2425-7. 18. Knox IC, Hoerner JK. T h e role of
infection in premature rupture of the membranes. Am J Obstet Gynecol 1950;59:190-4. 19. Naeye RL, Peters EC. Causes and consequences of premature rupture of fetal membranes. Lancet 1980;l:192-4. 20. Zachau-Christiansen B, Ross RM. Babies human development during the first year. London: Wiley, 1975. 21. U.S. Department of Health, Education & Welfare. Pregnancy and infant health. In: T h e Health Consequences of Smoking. A Report of the Surgeon General. Washington DC: U.S. Department of Health, Education & Welfare, 1981.
Address for correspondence: Richard Naeye, MD, Professor and Chairman, Dept. of Pathology, Milton S. Hershey Medical Center, Hershey, PA 17033.
Bonnie Flood is perinatal outreach coordinator at the Hershey Medical Center in Hershey, Pennsylvania. She is a member of NAACOG and the National Perinatal Association. Richard Naeye is involved in several African as well as U.S. projects that are attempting to prevent preterm deliveries. He is chairman of the Department of Pathology at the Pennsylvania State University College of Medicine in Hershey, Pennsylvania.
ERRATUM
In the Subject Index appearing in the Nov/Dec 1983 issue of JOGN Nursing, the page reference following “Kegel exercises, prenatal” should be 403, not x20.
122
March/April 1984 JOGN Nursing
The cause of spontaneous rupture of the fetal membranes prior to the onset of labor is usually unexplained despite many published theories about its genesis. Physical and chemical characteristics of the membranes have all been examined as possible T h e present study examined 14 factors as possible risks in the genesis of premature membrane rupture: maternal age, race, parity, mother's marital status, her education and that of the infant's father, family income, prior instrumentation of the cervix, prepregnancy body weight, pregnancy weight gain, cigarette smoking during pregnancy, incompetent cervix, coitus within a few days of delivery, and length of gestation at the time of delivery.
Definition of Terms PROM: rupture of the fetal membranes prior to the onset of labor. Preterm PROM: rupture of the fetal membranes less than 259 days from the start of the last menstrual period.. Recent coitus: coitus that took place during the ten days before delivery. Chorioamnionitis: documented acute inflammatory cells spread diffusely along the surface of the chorion in the extraplacental membranes. Cervical instrumentation: dilatation and curettage or cervical biopsy before pregnancy. Data were not available to distinguish between cervical cone biopsies and punch biopsies.
Data Collection and Analysis Adapted with permission from Naeye RL. Factors that predispose to premature rupture of the fetal membranes. Obstet Gynecol 1982; 60:93. Submitted: August 1982. Accepted with revisions: May 1983.
March/April 1984JOGN Nursing
Data from a large prospective study were used in the analyses. The Collaborative Perinatal Project of the National Institute of Neurological and Communicative Dis-
orders and Stroke recorded information on gestation, labor, delivery, and the neonatal period in patients at 12 medical school-affiliated hospitals in different regions of the United States between 1959 and 1966. T h e current analyses included 25,820 singleton gestations that resulted in spontaneous deliveries. Pregnancies complicated by hydramnios or those that produced neonates with congenital malformations were excluded. Multivariate analysis was used to separate the individual effects of various factors on premature membrane ruptures.
Results Five thousand two hundred thirty of the women had two successive singleton births in the study. When preterm PROM was present in the first of these pregnancies, the recurrence rate was 2 1% in the second.'' When the first pregnancy went to term without PROM, only 4% of the next pregnancies ended with preterm PROM.''
119
fable 1. Factors Included in Multivariate Analysis for Relationship to Premature Rupture of the Fetal Membranes
Beta Values Length of gestation Maternal age Race, white Panty Prior cervical instrumentation Cigarette smoking during pregnancy Incompetent cervix Maternal pregnancy weight gain Recent coitus Maternal prepregnancy body weight Family income Years of education, father of baby Mother of baby unmarried Years of education, mother of baby
-0.087 P +0.074 P -0.052 P +0.045 P
< 0.001 < 0.001
+0.039 P < 0.001
Preterm delivery Older mothers Non-whites Multiparous women Prior instrumentation
+0.033P < 0.001 +0.019P < 0.01
Cigarette smoking Incompetent cervix
-0.015 +0.014
< 0.001
< 0.001
P < 0.05 P < 0.05
Low weight gain Recent coitus
+0.010P < 0.1 -0.005 P > 0.1
Overweight women
-0.004 P > 0.1 +0.004 P > 0.1
-0.002 P > 0.1
As might be expected, there was a strong association of PROM with preterm labor and delivery (Table 1). Other factors that had a strong, seemingly independent correlation with PROM were advanced maternal age, non-white mother, multiparity, instrumentation of the cervix before pregnancy, cigarette smoking, incompetent cervix, low pregnancy weight gain, and recent coitus. Discussion
T h e increased frequency of PROM in older mothers may indicate that fetal membranes are less strong in older than in young mothers. Findings in the study support the possibility that prior damage to the cervix or to the cervical canal by surgical instrumentation predisposes to PROM.’+’’ A study is needed that differentiates among various types of surgical instrumentation to assess fully this risk. Damage to the cervix may also be the explanation for the increase in PROM with increasing parity.
120
Premature Membrane Rupture Associated With
This study confirms previous reports that PROM is more frequent in women who smoke than in nonsmokers.’O~’’ However, the clinical significance of this finding is uncertain because it is present only in full-term gestations. l o T h e finding that PROM is associated with recent coitus differs from the reports of other investigators who have reported that coitus has no adverse effects.I2-l4 Orgasm can cause uterine contractions but it is far from certain that these contractions are strong enough to rupture normal membrane^.'^ A prospective study found that orgasm was an important cofactor with chorioamnionitis in the high frequency of premature membrane ruptures that follow coitus.I6 This raises the possibility that membranes locally weakened by infection are more susceptible to being ruptured by uterine contractions than uninfected membranes. Without female orgasm, seminal fluid does not ap ear to weaken the membranes. Other evidence indicates that
’r
chorioamnionitis, which is sometimes caused by coitus, can predispose to PROM.6-s*’sIn one study, chorioamnionitis was twice as frequent in membranes that ruptured just before the onset of labor as in membranes that ruptured just after labor began.” This suggests that chorioamnionitis antedated about half of the membrane ruptures that took place before the onset of labor. Why are the coital findings in the present study so different from those in previous studies? Using most of the same data base, Naeye previously reported that coitus did not increase the frequency of PROM.” These conflicting results are due to the different time frames in which coital data were collected in the two studies. In the previous study, Naeye used coital data from the last clinic visit, which usually reflected coital activity between the 30th and 10th days before delivery. Many women who had coitus before the last clinic visit reported no coitus between the last clinic visit and delivery. Those who continued coitus after the last clinic visit had a greater frequency of premature membrane ruptures than those who discontinued coitus after the last visit. The only other large population studies on the effects of coitus on the fetus are those of Mills et al. and of Zachau-Christiansen and Ross. 12*20Millset al. studied 10,98 1 pregnancies and collected coital data after delivery by asking the question, “In what months did you not have coitus during pregnancy?” An inherent problem with this method of data collection is that it depends on the long-term memory of the patient and one cannot be sure that a woman will give truthful information if her infant has been born prematurely, is sick, or has died. In addition, the month-long time frame that Mills et al. selected for their question is too long. It dilutes most of the adverse effects of
March/April 1984 JOGN Nursing
coitus, which last for only about seven days after the coital act.'6 In the study described in this article, women were asked at each clinic visit and at delivery how many times they had had coitus since the last clinic visit. Zachau-Christiansen and Ross found that women who continued coitus during pregnancy had a 40% greater frequency of newborns weighing under 2500 gm and nearly twice as many fetal/neonatal losses as mothers who discontinued coitus during pregnancy." Two additional studies, by Perkins and by Rayburn and Wilson, claim that coitus has no adverse effects during pregnan~y.''.'~Neither of these studies has enough cases to prove or disprove their thesis. Implications for Nursing Practice T h e risks of smoking to women's health in general and to the fetus during pregnancy have been well established." Counseling regarding the risks of smoking should be an important part of total health care in pregnancy. In this counseling, the nurse should not tell the woman that stopping smoking will prevent PROM because it has many other causes, and it is far from certain that smoking is involved in preterm PROM. Early in the prenatal period, the nurse's pregnancy care plan should include a discussion about smoking and its potential adverse effects, reference materials for the patient to take home to read after the discussion, and a list of resources that the patient could seek out to assist her to quit, or at least reduce, her smoking. Supporting and praising genuine efforts by the patient to try to stop smoking as pregnancy progresses can be helpful reinforcers. The nurse should set a positive example by not smoking in the gravida's presence, and no smoking pol-
March/April 1984 JOCN Nursing
icies should be enforced in the health-care environment. Pregnancy is a time of increased motivation for most women, an ideal time for the nurse to help the gravida understand that the risks of smoking to both herself and her fetus exceed the benefits. Should women be advised to discontinue coitus or otherwise change their sexual practices during pregnancy? T h e association between recent coitus and PROM and other adverse outcomes, however strong, does not constitute proof of a causal relationship. Such proof can be established only by intervention studies that prevent the adverse outcomes. Several such intervention studies are now in progress. However, the process for the nurse in providing routine counseling regarding sexuality in pregnancy may include Assessing the woman's level of satisfaction with her sexual relationship. This may change in each trimester as the patient's responses often change as pregnancy progresses. Counseling if the woman identifies areas in which she would like to change aspects of her sexual relationship, i e . , discussing pregnancy comfort measures, such as coital positions, vaginal lubrication, or alternatives to coitus if the patient is too uncomfortable, or giving permission to experience normal changes in sexual feelings throughout pregnancy. Determining if the patient has specific questions or concerns regarding her sexual activity, i.e., fears about harming the fetus, feeling disinterested or unsatisfied with coitus, and then planning for her individual needs accordingly. Identifying patients who present with a previous history of preterm PROM. T h e present study
demonstrates a strong tendency for recurrence in a subsequent pregnancy. Therefore, until more information is available, prenatal sexual counseling for these patients should emphasize the potential benefits of noncoital sexual alternatives after the first trimester of pregnancy. The question of whether or not coitus is risky during pregnancy has been in the news, so many patients are aware of it. For women who are not at risk, the benefits of a sexual relationship, with or without coitus, should be recognized and valued when it promotes feelings of security, love, affection, and tenderness. Conclusion .
Overall, the current study found a remarkable tendency for premature ruptures to repeat in successive pregnancies. To date, most non-epidemiologic research has been directed toward evaluating the strength or the collagen content of the remaining membranes on the possibility that a deficiency of collagen or abnormal collagen might be responsible for the ruptures. These studies have usually found no difference between membranes that ruptured prematurely and those that ruptured after the onset of labor.' These negative findings raise the possibility that localized defects rather than generalized weaknesses in the membranes are responsible for most premature ruptures. The rupture, by passing through these areas of defect, in turn destroys the damaged site. These localized abnormalities are far more difficult to study, but future research should give them more consideration because they are likely to hold the key to many of the ruptures that are currently unexplained. Nursing care for the uncomplicated pregnant patient should focus on the application of research data to the clinical situa-
121
tion in t h e context of t h e risk-benefit ratio for th e patient.
References 1 . Danforth DN, Hull RW. T h e microscopic anatomy of the fetal membranes with particular reference to the detailed structure of the amnion. Am J Obstet Gynecol
1958;75:536-47. 2. Embrey MP. On the strength of the foetal membranes. Br J Obstet Gynaecol 1954;6 1 :793-6. 3. Al-Zais NS, Bou-Resli MN, Goldspink G. Bursting pressure and collagen content of fetal membranes and their relation to premature rupture of the membranes. Br J Obstet Gynaecol 1980; 87:227-9. 4. Lavery JP, Miller CE. Deformation and creep in the human chorioamniotic sac. Am J Obstet Gynecol 1979;134:366-75. 5. Bourne G. The human amnion and chorion. London: Lloyd-Luke, 1962:175-92. 6. Artal R, Burgeson RE, Hobel CJ, et al. An in vitro model for the study of enzymatically mediated biomechanical changes in the chorioamniotic membranes. Am J Obstet Gynecol 1979;133:656-9. 7. Lukac J, Koren E. Mechanism of liquefaction of the human ejaculate. 11. Role of collagenase-like peptidase and seminal proteinase. J Reprod Fertil 1979;56:501-6. 8. Koren E, Milkovic S. Collagenase-
like peptidase in human, rat and bull spermatozoa. J Reprod Fertil 1973;32:349-56. 9. Evaldson G, Lagrelius A, Winiarski J . Premature rupture of the membranes. Acta Obstet Gynecol Scand 1980;59:385-93. 10. Naeye RL. Factors that predispose to premature rupture of the fetal membranes. Obstet Gynecol 1982;60:93-7. 1 1 . Meyer MB, Tonascia JA. Maternal smoking pregnancy complications and perinatal mortality. Am J Obstet Gynecol 1977;128:494-502. 12. Mills JL, Harlap S, Harley EE. Should coitus late in pregnancy be discouraged? Lancet 198 1 ;2: 1368. 13. Perkins RP. Sexual behavior and response in relation to complications of pregnancy. Am J Obstet Gynecol 1979; 134:498-505. 14. Rayburn WR, Wilson EA. Coital activity and premature delivery. Am J Obstet Gynecol 1980; 137: 972-4. 15. Goodlin RC, Schmidt W, Creevy DC. Uterine tension and fetal heart rate during maternal orgasm. Obstet Gynecol 1972;39:125-7. 16. Naeye RL, Ross S. Coitus and chorioamnionitis, a prospective study. Early Human Develop 1982;6:917. 17. Lavery JP, Miller CE. Effect of prostaglandin and seminal fluid on human chorioamnionitis membranes. JAMA 198 1 ;245:2425-7. 18. Knox IC, Hoerner JK. T h e role of
infection in premature rupture of the membranes. Am J Obstet Gynecol 1950;59:190-4. 19. Naeye RL, Peters EC. Causes and consequences of premature rupture of fetal membranes. Lancet 1980;l:192-4. 20. Zachau-Christiansen B, Ross RM. Babies human development during the first year. London: Wiley, 1975. 21. U.S. Department of Health, Education & Welfare. Pregnancy and infant health. In: T h e Health Consequences of Smoking. A Report of the Surgeon General. Washington DC: U.S. Department of Health, Education & Welfare, 1981.
Address for correspondence: Richard Naeye, MD, Professor and Chairman, Dept. of Pathology, Milton S. Hershey Medical Center, Hershey, PA 17033.
Bonnie Flood is perinatal outreach coordinator at the Hershey Medical Center in Hershey, Pennsylvania. She is a member of NAACOG and the National Perinatal Association. Richard Naeye is involved in several African as well as U.S. projects that are attempting to prevent preterm deliveries. He is chairman of the Department of Pathology at the Pennsylvania State University College of Medicine in Hershey, Pennsylvania.
ERRATUM
In the Subject Index appearing in the Nov/Dec 1983 issue of JOGN Nursing, the page reference following “Kegel exercises, prenatal” should be 403, not x20.
122
March/April 1984 JOGN Nursing