Reproductive D efects in Patients of Both Sexes w ith Cystic Fibrosis: A R eview
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1 ANNALS O F CLINICAL A N D LABORATORY SC IE N C E, Vol. 15, No. 2 Copyright 1985, Institute for Clinical Science, Inc. Reproductive D efects in Patients of Both Sexes w ith Cystic Fibrosis: A R eview THOMAS W. SEALE, P h.d.,* MARINUS FLUX, and OW EN M. RENNERT, M.D. Department of Pediatrics, University of Oklahoma Health Sciences Center, Oklahoma City, OK ABSTRACT C urrent knowledge of reproductive duct function in both male and female cystic fibrosis patients is reviewed. Almost all male patients are sterile because of azoospermia. The m echanistic basis of the obstructive defect leading to pre- and post-natal destruction of selected portions of the sp erm -co n d u ctin g netw ork rem ains unknow n. Fem ale cystic fibrosis patients are fertile. Pulmonary status appears to be the most important factor in determ ining pregnancy outcome. In contrast to earlier concerns about the norm ality of breast milk, breast milk composition of cystic fibrosis m others is norm al, and they can successfully breast feed their infants. Introduction significant symptoms, ameliorating the nutritional deficiencies, controlling bacterial respiratory infections, and preserving p ulm onary fu n ctio n, have succeeded in extending the median survival of th ese p a tie n ts to young adulthood. R ecently available data for the U nited States indicate that fifty percent of these patients now survive to the age of 19 (figure l ). 23 This tre n d is expected to continue and to result in an increasing num ber of cystic fibrosis patients surviving to their second, third, and fourth decades. Since many patients may be interested in establishing their own families, family and genetic counseling issues become a special concern. This m anuscript reviews five im portant aspects related to sexual d e v elo p m en t and rep ro d u ctio n in the cystic fibrosis patient: (1) delayed puberty, (2) ste rility in m ales, (3) red u c e d fertility in females, (4) increased risk of m atern al and fetal/neonatal m ortality, and (5) breast milk quality /85/ $01.20 Institute for Clinical Science, Inc. The autosom al recessive disease, cystic fibrosis, is the most frequent of the severe inherited diseases in Caucasians with an incidence of 1 in 1600 to 1 in The m ajor clinical findings com monly occurring in childhood in cystic fibrosis are m alabsorptive disease associated w ith exocrine pancreatic malfunction and recurrent bacterial pulmonary infection associated w ith progressive o b stru ctiv e lung disease. In earlier d ecades, m ost p a tie n ts d ied before reaching reproductive m aturity. However, although the underlying m olecular defect in cystic fibrosis rem ains u n know n, early diagnosis coupled w ith medical treatm ent aim ed at its clinically * Send all correspondence to: Thomas W. Seale, P h.d., Laboratory of Bioorganic Chemistry, Bldg. 4, Room 212, National Institutes of Health, Bethesda, M D
2 REPRODUCTIVE PROBLEMS IN CYSTIC FIBROSIS > 70 ^ U 30 tc Ul 2 0 a. 10 o F i g u r e 1. Longitudinal survival curve for cystic fibrosis patients in the United States for the years Adapted from M atthews and Drotar (1984). D elayed Puberty Delay in the m aturation of the hypothalam ic-p itu itary -g o n ad al axis occurs frequently in patients w ith chronic illness or m alnutrition. 7,30 Thus, it is not surprising that the onset and progession of sexual developm ent in patients with cystic fibrosis is often delayed in a m anner dependent on their underlying nutritional and pulm onary statu s. 24,36' 37 Moshang and Holsclaw investigated the clinical score at the tim e of m enarche in 63 girls with cystic fibrosis. 25 Their mean age at achieving m enarche was 14.5 years (versus 12.9 years in normal females) and varied with the severity of the illness. A m enorrheic girls w ith cystic fibrosis, m ean age 14 years, w ere significantly sicker and smaller than those achieving m enarche. Cross-sectional studies of cystic fibrosis patients have established that a chronological delay occurs in the attainm ent of pu b ertal levels of reproductive endocrine horm ones. 31 Prepubertal boys with cystic fibrosis who are m ost im paired in height, weight, and skeletal maturation also have m easurable abnorm alities of LH R H*-releasable gonadotrophin secre * Leutinizing hormone-releasing hormone. tion. 32 D espite continued im pairm ent of w eight in crease, p u b e rta l p a tie n ts do attain norm al gonadotrophin secretory responses to LHRH* administration and are sim ilar to subjects w ith constitutionally delayed adolescent developm ent in reproductive endocrine physiology. Subse q u en t to this delay, cystic fibrosis patients do reach norm al sexual m aturity. Sterility in Males It was noted in early studies of cystic fibrosis patients who survived to adulthood th at th ey w ere often in fe rtile. 35 A lthough w om en w ith cystic fibrosis w ere able to conceive and carry th e ir infants to term in a num ber of instances, males appeared to be unable to im pregnate th eir m ates. In seeking an u n d e r standing of the basis of this male infertility, two stu d ies exam ining 33 m ales w ith classic cystic fibrosis (ages 2=17 years) found that all of them produced semen which was azoospermic It is now the general clinical view that essentially all male cystic fibrosis patients are sterile (except for the rare individuals who rem ain fertile15). Generally, th eir semen volume is significantly reduced, has a lower ph, and an altered chemical composition com pared to that produced by norm al individuals. 515 To visualize b etter the nature of the anatom ical defects w hich appear to underlie azoosperm ia in males w ith cystic fibrosis, th e proxim al ductal stru c tures of the male reproductive tract will be review ed (figure 2). 16 Sem iniferous tubules of the testis em pty into the epithelially lined netw ork of the rete testis. E m erging from the rete testis, the convoluted tubule of the ductus epididymis forms the body and tail of the epididymis and finally becomes the vas (ductus) deferens. T he epididym is is a single elongated duct, the tortuosity of which can be appreciated w hen one considers its usual coiled len g th of 5 cm w hen extended is actually a tube 4-5 m long.
3 154 SEALE, FLUX, AND RENNERT F i g u r e 2. Schem atic draw ing o f th e hum an sperm conducting network. Figure is reproduced from the Textbook o f Human A natom y, 2nd edition, edited by W. J. Hamilton with the kind permission of the C.V. M osby Company. T he epididym is is the principal storage area for spermatozoa. The transit tim e is a b o u t tw o w eek s, d u rin g w hich th e sperm und erg o es a n d ro g e n -d e p e n d e n t m aturation. The head of the epididym is appears to be particularly active in fluid reabsorption. F a ilu re of th e a d u lt cy stic fibrosis patient to reproduce is prim arily due to a lack of an anatomically intact ductal sys tem for conducting sperm atozoa from the te s te s. It is g e n e ra lly fo u n d th a t th e external genitalia and prostate are nor m al on physical exam ination S p er m atogenesis is active, although a signifi cant nu m b er of sperm may b e m alform ed in som e in d iv id u a ls K aplan e t a l 15 w e re th e first to d e s c rib e an ato m ic lesions in the reproductive tract of males who died of cystic fibrosis. The vas def e re n s was a b s e n t in 1 0 of 1 0 p a tie n ts coming to autopsy and 7 of 7 com ing to surgery. In a significant fraction, the epi didymis was also absent. Landing et al 19 w ere unable to d etect the vas deferens in 31 of 32 patients from whom autopsy m aterial was available (13 of whom w ere = one year of age). T he epididym is was a tro p h ic o r fib ro tic, o ften w ith foci of dilatation of the efferent ductules, in the same n u m b er of patients. The sole nor m al fin d in g was in an in d iv id u a l for whom the diagnosis of cystic fibrosis was n o t d e fin ite ly e s ta b lis h e d. No sim ilar lesions w ere found in 108 of 109 male children dying of other diseases. O ther in v e stig a to rs h av e also fo u n d m arked abnorm alities in the structure of the epi didymis and vas deferens in very young infants w ith cystic fibrosis. 27,40 Although som e in fan ts a n d y o u n g c h ild re n may retain a norm al stru ctu re of the vas def erens and epididym is, 27,40 no adults with d o c u m e n te d cystic fibrosis a p p e a r to do so. Two m echanism s have been proposed to account for the structural abnorm ali ties of th e epididym is and vas deferens: (1 ) a developm ental anomaly occurring in the fetus during differentiation of these structures from the Wolffian d u c t, 15,19,40 and (2 ) a p ro ce ss o f a tro p h y ow ing to obstruction of these ductal structures by viscous s e c re tio n s. 6,1 9,2 7 T his q u e stio n has not yet been resolved, and it may be that both processes occur in some indi viduals. It is established that portions of norm al ducts do occur in some p rep u bertal m ales. 27,40 Also, left and right duc tal system s are not necessarily affected in the same m anner or to a sim ilar ex ten t. 40 Distal portions of th e vas deferens may be m ore fre q u e n tly affected w hen the effects are heterogeneous w ithin an indi vidual. 40 D uctal dilatation in the epidid ym is has also b e e n id e n tifie d in som e young infants and has b een in terp reted as an early indicator of m ucus inspissation w hich p rec e d e s po stn atal atrophy and subsequent fibrosis of these ductal elem ents. 27
4 REPRODUCTIVE PROBLEMS IN CYSTIC FIBROSIS 155 Azoosperm ia is found in eight to 26 percent of normal males (i.e., without cystic fibrosis) of couples being evaluated for infertility, b u t sp erm atogenesis is absent in a significant fraction. 14,22 Stern et al38 have recently proposed that semen analysis m ight be a diagnostic test for cystic fibrosis in adolescents and young adults w hose clinical p re se n ta tio n for cystic fibrosis is atypical. They suggest that, in azoospermia in those with only m inim al findings consistent w ith cystic fibrosis, scrotal exploration and testicular biopsy should be perform ed to establish w h e th e r or not th e azoosperm ia is of obstructive origin. The validity of this proposal has been challenged by Knight and H endry 17 who point out the common association of obstructive azoosperm ia and chronic respiratory disease. 12,13,43 It remains to be established w hether or not semen analysis with be useful for determ ining th a t an in d ividual w ith o u t the classic cystic fibrosis phenotype actually carries the genetic defect. Reduced Fertility and Risk of Pregnancy in Fem ale Patients It is generally held that women with cystic fibrosis have reduced fertility. 23,35 W hile subjective clinical experience supports such an assum ption, th e re exist scanty objective data. However, in keeping w ith this view, m enstrual irregularities occur in over half of th ese young w om en. 26 Two m echanism s have been proposed to account for reduced fertility in these patients; but, in the absence of m ore thorough stu d ies, th ese rep o rts m ust be considered as only suggestive. Q ualitative histological exam ination of the female reproductive tract suggested an increase in intracellular m ucins in cervical cells and an increased secretion of extracellular m ucins in cystic fibrosis fem ales of various ag es. 28 C ontrol females had sim ilar findings in some individuals b u t th ey o ccu rre d less frequently. C opious m ucin secretio n has been postulated to reduce sperm p e n e tration and th ereb y reducing fertilization. In contrast, other investigators have reported that cervical mucus was scant in women with cystic fibrosis; however, they suggested that cervical mucus from these women was qualitatively altered in w ater and electrolyte com position and speculated that this m ight im pede sperm m otility. 18 The advisability of pregnancy in cystic fibrosis continues to be a subject of m edical d eb ate. M atern al m ortality associated w ith pregnancy may be high and th ere is an increased incidence of spontaneous abortion, prem aturity and stillbirths. 3,10,20 Cohen et al3 have reviewed the outcome of 129 pregnancies in 100 women with cystic fibrosis. Ninety-seven of the 129 pregnancies were completed, providing 8 6 viable infants. Stillbirths (six percent), neonatal deaths (five p e r cent), and prem aturity (16 percent) were higher than in controls. One infant had cystic fibrosis. No m aternal deaths occurred during pregnancy. Although 15 of 84 women died within six months post partum, this death rate was similar to the m ortality found for age-m atched n o n pregnant cystic fibrosis patients. It appears th a t w om en w ith cystic fibrosis fall into two groups with regard to pregnancy. 4,29 In the first group, the overall m atern al condition is little affected and fetal outcome is good. In the second group, pregnancy appears to be associated with a worsening of the m othe r s clinical condition w hich n ev er retu rn s to th e p reg rav id state. Babies born to this latter group appear more frequently to be small for gestational age or born p re te rm. 29 P regravid n u tritio n a l status and pulm onary status are im portant for both m aternal and fetal outcome. W om en w ith m ild pulm onary disease and with intact pancreatic function seem to have a b etter outcome than those with significant or severe pulm onary disease.
5 156 SEALE, FLUX, AND RENNERT In asthm atics, too, the condition of patients with mild disease was generally unaffected by pregnancy b u t the condition of m ore severely affected patients generally w orsened during pregnancy. 9 In women with emphysema, pulmonary function also w o rsen ed d u rin g p re g nancy. 8 Thus, the advisability of p reg nancy in w om en w ith cystic fibrosis should be considered on the basis of individual m edical and psychosocial circum stances. B reast Milk Composition in Cystic Fibrosis The breast is considered to be a m odified sweat gland. As such there has been concern th a t b reast m ilk from w om en w ith cystic fibrosis m ight contain e le vated sodium levels reflecting that found in th e ir eccrin e sw eat. 39 B ecause the neonatal kidney has low functional capacity for sodium m anagem ent, new borns are vulnerable to life-threatening h y p ernatremia. The ability of these women to breast feed was particularly questioned following a brief report which described a m o th er w ith cystic fibrosis w hose breast milk contained a high sodium concen tratio n. 42 M ore recently, the breast milk of several women with cystic fibrosis has been studied ,42 In each of the cases, these affected women secreted breast milk w ith a norm al sodium concentration and nu rsed th eir infants effectively. In addition, a trivial explanation for the elevated sodium concentration in breast milk of one m other has been provided. 2 The emphasis of these prior studies was on th e sodium c o n te n t of the milk, and little data currently exist for th e m acro-organic co n stitu en ts of this breast milk. In the breast milk and colostrum of two women, protein, lactose, fat, and immunoglobulin levels were found to be normal or near norm al. 33 Thus, it appears that th e com position of major constituents of breast milk are acceptable for consum ption by infants. Care m ust be taken by physicians in individual cases where the m other s nutritional status is com prom ised. Conclusion D e sp ite th e rep ro d u c tiv e problem s associated with cystic fibrosis, a recent study of 30 m arried couples, in whom one m em b er had cystic fibrosis, in d i cated that the m ajority had successful sexual relationships. 21 Five out of 30 couples had serious sexual problem s which could be a ttrib u te d to cystic fibrosis. O bstructive pulm onary disease of w hatever origin can have a significant effect on sexual perform ance. 1 Sum m ary Male cystic fibrosis patients are usually sterile because of obstructive azoospermia but should have a semen analysis as young adults to establish the occurrence of sterility in individual cases. W omen with cystic fibrosis whose clinical status is good and who have good respiratory function appear to have no severe exacerbation of th eir sym ptom s w ith p reg nancy and have norm al term infants. Breast feeding by these m others appears to present no special risks to the neonate. Acknowledgm ents This m anuscript was prepared w ith sabbatical leave support to T.W.S. from the University of Oklahoma Health Sciences Center and a senior research fello w sh ip from th e Intram ural C ystic F ibrosis R esearch Program o f the N ational In stitu tes of Health (NIADDK). R eferences 1. A g l e, D. P. and B a u m, G. L.: Psychological aspects of chronic obstructive pulmonary disease. Med. Clin. N. Amer. 61: , A l p e r t, S. E. and C o r m i e r, A. D.: Normal electrolyte and protein content in milk from mothers with cystic fibrosis: An explanation for the initial report of elevated milk sodium concentration. J. Pediat. 102;77-8 0, 1983.
6 REPRODUCTIVE PROBLEMS IN CYSTIC FIBROSIS C o h e n, L. F., d i S a n t A g n e s e, P. A., and F r i e d - l a n d e r, J. : C ystic fibrosis and pregnancy. A national survey. Lancet 2: , C o r k e y, C. W., N e w t h, C. J., C o r e y, M., and L e v i s i o n, H. : Pregnancy in cystic fibrosis: A better prognosis in patients with pancreatic function? Am. J. O bstet. Gynecol. 140: , D e n n i n g, C. R., S o m m e r s, S. C., and Q u i g l e y, H. J.: Infertility in male patients with cystic fibrosis. Pediatrics 41:7-1 7, d i S a n t A g n e s e, P. A. : Fertility and the young adult w ith cystic fibrosis. N. E ngl. J. M ed. 279: , D r e i z e n, S., S p i r a k i s, C. N., and S t o n e, R. E.: A comparison of skeletal growth and maturation in undernourished and w ell nourished girls before and after menarche. J. Pediat. 70: , G a z i o g l u, K., K a l t r e i d e r, N. L., R o s e n, M., and Yu, P. N.: Pulmonary function during pregnancy in normal wom en and in patients with cardiopulm onary d isease. Thorax 2 5 : , G l u c k, J. C. and G l u c k, P. A.: The effects of pregnancy on asthma: A prospective study. Ann. Allergy 37: , G r a n d, R. J., T a l a m o, R. C., d i S a n t A g n e s e, P. A., and S c h w a r t z, R. H.: Pregnancy in cystic fibrosis of the pancrease. J. Am. Med. Assoc. 195: , H a m o s h, M., B i t a n a n, J., and W o o d, D. L.: Human milk in cystic fibrosis (CF): Composition and enzyme content. Pediat. Res. /6:164a, H a n d e l s m a n, D. J., C o n w a y, A. J., B o y l a n, L. M., and T u r t l e, J. R.: Young s syndrome. Obstructive azoospermai and chronic sinopulmonary infections. N. Engl. J. Med. 310:3-9, H e n d r y, W. F.: The long term results of surgery for ob stru ctive azoosperm ia. Brit. J. Urol. 53: , J o h a n s o n, C.-J.: Clinical studies on sterile couples with special reference to the diagnosis, etiology and prognosis of infertility. Acta Obstet. Gynaecol. Scand. 36 (Suppl.):l-168, K a p l a n, E., S h w a c h m a n, H., P e r l m u t t e r, A. D., R u l e, A., K h a w, K. T., and H o l s c l a w, D. S.: Reproductive failure in males with cystic fibrosis. N. Engl. J. Med. 279:6 5-69, K e l l y, D. E., W o o d, R. L., and E n d e r s, A. C. : Bailey s Textbook of Microscopic Anatomy. 18th edition. Baltimore, Williams and Wilkins, 1984, pp K n i g h t, R. K. and H e n d r y, W. E.: Obstructive azoospermia and respiratory disease. Lancet 2:152, K o p i t o, L. E., K o s a s k y, H. J., and S h w a c h m a n, H.: Water and electrolytes in cervical mucus from patients with cystic fibrosis. Fertil. Steril. 24: , L a n d i n g, B. H., W e l l s, T. R., and W a n g, C.-I.: Abnormality of the epididymis and vas deferens in cystic fibrosis. Arch. Pathol. 88: , L a r s e n, J. W.: Cystic fibrosis and pregnancy. Obstet. Gynaecol. 39: , L e v i n e, S. B. and S t e r n, R. C.: Sexual function in cystic fibrosis. Relationship to overall health status and pulmonary disease severity in 30 married patients. Chest 81: , L i p s h u l t z, L. I.: Subfertility. Current Urologic Therapy. Kauffman, J. J., ed. Philadelphia, W.B. Saunders, 1980, pp M a t t h e w s, L. W. and D r o t a r, D. : Cystic fibrosis a challenging long-term chronic disease. Pediat. Clin. N. Amer. 32: , M i t c h e l l - H i g g s, P., M e a r n s, J., and B a t t e n, J. C.: Cystic fibrosis in adolescents and adults. Quart. J. Med. 45: , M o s h a n g, T. and H o l s c l a w, D. S., J r.: Menarchal determinants in cystic fibrosis. Am. J. Dis. Child. 134: , N e i n s t e i n, L. S., S t e w a r t, D., W a n g, C.-I., and J o h n s o n, I.: Menstrual dysfunction in cystic fibrosis. J. A doles. H ealth Care 4 : , O p p e n h e i m e r, E. H. and E s t e r l y, J. R.: Observations on cystic fibrosis of the pancreas. IV. Developmental changes in the male genital system. J. Pediat. 75: , O p p e n h e i m e r, E. H. and E s t e r l y, J. R.: Observations on cystic fibrosis of the pancreas. VI. The uterine cervix. J. Pediat. 77: , P a l m e r, J., D i l l o n - B a k e r, C., T e c k l i n, J. S., W o l f s o n, B., R o s e n b e r g, B., B u r r o u g h s, B., H o l s c l a w, D. S., S c a l i n, T. F., H u a n g, N. N., and S e w e l l, E. M.: Pregnancy in patients with cystic fibrosis. Annals Int. M ed. 99: , P i r n s t o n e, B. : Endocrine function in proteincalorie malnutrition. Clin. Endocrinology 5:79 95, R e i t e r, E. O., S t e r n, R. C., and R o o t, A. W.: The endocrine system in cystic fibrosis. I. Basal gonadotropin and sex steroid levels. Am. J. Dis. Child. 135: , R e i t e r, E. O., S t e r n, R. C., and R o o t, A. W.: The reproductive endocrine system in cystic fibrosis. 2. Changes in gonadotrophins and sex steroids following LHRH. Clin. Endocrinology 26: , S e a l e, T. W., F l u x, M., R e n n e r t, O. M., S h e f f m a n, M. L., and S w e n d e r, P. 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7 158 SEALE, FLUX, AND RENNERT T u c k e r, A. S., P r i n i a n o, F. P., and M a t t h e w s, L. W.: Course of cystic fibrosis in 95 patients. J. Pediat. 89: , S t e r n, R. C., B o a t, T. F., and D o e r s h u k, C. F.: Obstructive azoospermia as a diagnostic criterion for the cystic fibrosis syndrome. Lancet 1: , T a l a m o, R. C., R o s e n s t e i n, B. J., and B e r n i n - g e r, R. W.: Cystic fibrosis. The Metabolic Basis of Inherited D isease. 5th edition. Stanbury, J. B., W yngaarden, J. B., Fredrickson, D. S., Goldstein, J. L., and Brown, M. S., eds. New York, McGraw-Hill Book Company, 1983, pp V a l m a n, H. B. and F r a n c e, N. E.: The vas deferens in cystic fibrosis. Lancet 1: , W e l c h, M. J., P h e l p s, B. L., O s h e r, A. B.: Breast feeding by a mother with cystic fibrosis. Pediatrics 67: , W h i t e l a w, A. and B u t t e r f i e l d, A.: High breast milk sodium in cystic fibrosis. Lancet 2:1288, Y o u n g, D.: Surgical treatment of male infertility. J. Reprod. Fertility 23: , 1970.
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