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Pii: s0015-0282(00)01615-0

VOL. 74, NO. 6, DECEMBER 2000Copyright 2000 American Society for Reproductive MedicinePublished by Elsevier Science Inc.
Printed on acid-free paper in U.S.A.
Chronic cough and infertility: a report of
two cases

Laurie McLean, M.D.,a and Paul Claman M.D., F.R.C.S.(C)b University of Ottawa and Ottawa Hospital, Ottawa, Ontario, Canada Objective: To report two cases of infertility caused by primary ciliary dyskinesia in patients who presented
with an associated complaint of a chronic cough.
Design: Case report.
Setting: University teaching hospital.
Patient(s): Two patients presenting with unexplained infertility and an associated history of long-term
chronic cough.
Intervention(s): Patients underwent a nasal mucosal biopsy by an otolaryngologist. Electron microscopy
(EM) examination of biopsy specimens was performed.
Main Outcome Measure(s): Diagnosis and appropriate treatment for functional tubal factor infertility.
Result(s): Both patients were diagnosed with primary ciliary dyskinesia based on EM of the nasal biopsy
specimens. Given this diagnosis, they immediately underwent IVF-ET. Both patients became pregnant with
their first IVF-ET cycle.
Conclusion(s): Other investigators have shown that almost 20% of patients with a chronic cough will have
EM evidence of ciliary dyskinesia. Patients presenting with idiopathic infertility and an associated unex-
plained chronic cough should be referred for nasal biopsy with EM evaluation to rule out primary ciliary
dyskinesia. Infertility in these cases, which is due to a functional tubal factor, is best treated with IVF-ET
rather than superovulation and intrauterine insemination treatments. (Fertil Steril௡ 2000;74:1251–3. 2000 by
American Society for Reproductive Medicine.)
Key Words: Ciliary dyskinesia, ciliary dysfunction, immotile cilia syndrome, Kartagener’s syndrome,
dynein arms, infertility
ectasis, chronic sinusitis, dextrocardia, and function of the fallopian tube is well estab- male factor infertility. The ultrastructure of the lished. Early research hypothesized that by cilia in KS has been shown to consist of ab- combining ciliary beat frequency and myo- normalities of the DAs. Initially it was felt that salpingeal contraction, the fallopian tube re- the structural abnormalities of the cilia ren- trieves the ovulated ovum, moves the sperm dered the cell totally immotile. However, sub- Received March 28, 2000;accepted August 1, 2000.
from uterus to distal oviduct, and subse- sequent work has determined that cilia with quently transports the resultant embryo from ultrastructural abnormalities may be dyskinetic distal oviduct into the uterine cavity.
rather than totally immotile. Primary ciliary 737 Parkdale Avenue, Suite505, Ottawa, Ontario, dyskinesia (PCD) is the term now used for a The ultrastructure of the cilium consists of group of syndromes associated with immotile nine pairs of microtubular doublets surround- or dyskinetic cilia, of which KS represents a ing two tubules that are enclosed in a central Otolaryngology,University of Ottawa.
(DAs) contain ATPase activity that provides To date, the bulk of research pertaining to the energy for the doublets to slide over one cilia and infertility has focused on women with another—this mechanochemical coupling is KS, but there is little reported about infertile believed to be the source of the ciliary beat.
Perhaps the best described condition in which cases of women presenting with infertility who the cilia do not function properly is Kartagen- have significant histories of chronic sinusitis 0015-0282/00/$20.00PII S0015-0282(00)01615-0 er’s syndrome (KS), characterized by bronchi- fertility; this syndrome continues to bear his name. Follow- A 28-year-old woman was referred to the Fertility Centre ing the advent of the electron microscope, Afzelius and at the Ottawa Hospital in 1996 with a 5-year history of colleagues (1, 2) examined the cilia of the sperm and respi- primary infertility. Ovulatory function was normal. Her part- ratory tract in men with clinical KS and discovered an ner’s semen analysis was normal (according to WHO crite- abnormality of the cilia ultrastructure. In the respiratory ria). Laparoscopy and hysterosalpingography were normal.
mucosa, the absence of the DA leads to an absence of Her medical history was significant for recurrent sinusitis, mucociliary clearance and subsequent chronic sinusitis, re- recurrent pneumonia, chronic bronchitis, and bronchiectasis.
current pneumonia, and bronchiectasis. Halbert et al. (3) She underwent several cycles of clomiphene citrate treat- examined the function and structure of cilia in the fallopian ment followed by six cycles of rFSH superovulation and tube of an infertile woman with KS. Using a laser light- intrauterine insemination cycles without a pregnancy occur- scattering system as well as EM, they measured the ciliary ring. Because of the history of chronic sinusitis and chronic beat frequency, ciliary topography, and ciliary density of the upper respiratory tract infections, the patient was referred to nasal and tubal mucosa. EM demonstrated similarities among an otolaryngologist for evaluation and nasal biopsy. With the the nasal and tubal ciliated cells including abnormal struc- use of electron microscopy (EM), the cilia of the nasal ture of the DA and an absence of the central microtubules.
mucosa were examined and found to have an absence of Although there was motility of the cilia in the fallopian inner DA and inconsistent outer DA. These findings were tube, it was dyskinetic. They concluded that ciliary dykinesia consistent with PCD. The patient has an ongoing singleton was the only identifiable explanation for the patient’s ongo- intrauterine pregnancy after her first IVF-ET treatment cycle.
ing infertility and that the structure of the cilia of the nasalmucosa mirrored that of the fallopian tube. Although the absence of DA remains the most prevalent abnormality of A 33-year-old woman presented with a 4-year history of the cilia, at least 20 different defects have now been de- infertility. Her only pregnancy that occurred independent of scribed affecting various components of these complex or- therapy ended in a left salpingectomy for ectopic pregnancy.
ganelles. These abnormalities do not always render the cilia The patient’s partner had a normal semen analysis (WHO).
totally immotile, but rather often the cilia exhibit decreased motility or uncoordinated motility (4). In our two cases, the Diagnostic laparoscopy performed before the ectopic couples had no identifiable cause for infertility other than pregnancy revealed normal pelvic anatomy except for min- PCD in the woman. Medical history was significant for imal (rAFS-1) endometriosis without any pelvic adhesions.
chronic sinusitis, chronic cough, and recurrent respiratory The fimbriated ends of both fallopian tubes were normal and tract infections in both women. Of patients with PCD, only patent. Hysterosalpingography before the ectopic pregnancy 50% have KS; however, 100% have cough and nearly 100% was normal. Subsequent to the ectopic pregnancy, a second have chronic sinusitis. In the general population of infertile laparoscopy with laser vaporization of minimal (rAFS-1) couples, the prevalence of PCD is approximately 1 in endometriosis was performed. Except for the absent left 40,000. Superovulation with intrauterine insemination would fallopian tube, findings were identical to the first laparos- not facilitate pregnancy in women with PCD because the copy. The remaining fallopian tube appeared completely oviduct, although patent, is not functional because the ab- normal and patent. Her medical history was significant for normal cilia are unable to transport gametes and embryos.
recurrent otitis media and chronic sinusitis requiring sinus sur- However, IVF-ET treatment for infertile women with PCD is gery as a child. There was also a history of recurrent otitis efficacious because it bypasses the functionally abnormal media and bronchiectasis for which she had undergone a oviduct. In both our cases the woman became pregnant with flexible fiberoptic bronchoscopy 10 years before. Findings on prior bronchoscopy included large thick mucous plugs in We propose that all women with a chronic cough or the left and right main-stem bronchi. No biopsies were taken chronic sinusitis and associated infertility be investigated for at the time. We referred the patient for otolaryngology eval- PCD. Van der Baan et al. (4) compared cilia ultrastructure and activity from patients with KS to cilia from both healthy Two biopsies of the mucosa of the middle turbinate were individuals and a group of patients with chronic respiratory examined using EM. The results were consistent with PCD.
tract infections. He found that 18% of patients with chronic The patient became pregnant with her first IVF-ET treatment upper respiratory tract infections had findings consistent cycle but unfortunately underwent a right salpingectomy for with PCD. Although we would be testing five women for one true positive result, the nasal biopsy is simple, quick,and accurate and involves minimal pain and complica- DISCUSSION
tions. Conversely, superovulation failures are time con- In 1933, Kartagener described four patients with chronic suming, expensive, and frustrating. If one woman in five sinusitis, bronchiectasis, situs inversus, and male factor in- with chronic cough and infertility can be identified as 1252 McLean and Claman
having PCD, then that woman can avoid ineffective super- 2. Afzelius BA, Camner P, Mossberg B. On the function of cilia in the female reproductive tract. Fertil Steril 1978;29:72– 4.
ovulation trials and proceed directly to IVF-ET with a good 3. Halbert SA, Patton DL, Zarutskie PW, Soules MR. Function and struc- ture of cilia in the Fallopian tube of an infertile woman with Kartagener’sSyndrome. Hum Reprod 1997;12:55– 8.
4. Van der Baan S, Veerman AJP, Bezemer PD, Feenstra L. Primary References
ciliary dyskinesia: quantitative investigations of the ciliary ultrastruc- 1. Afzelius BA, Eliasson K. Male and female infertility problems in the ture with statistical analysis. Ann Otol Rhinol Laryngol 1987;96: immotile cilia syndrome. Eur J Respir Dis 1983;64(Suppl):144 –7.


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