Review

Sexual and reproductive health in cystic fibrosis:

a life-course perspective
Katherine B Frayman, Susan M Sawyer

Lancet Respir Med 2015; Adolescents and adults with cystic fibrosis now approach developmental milestones, including sexual and
3: 70–86 reproductive ones, at a similar time to their healthy peers. Yet, their sexual and reproductive health (SRH) is
Published Online profoundly affected by their disease, and their SRH decisions can substantially affect their health. Navigation of
December 17, 2014
SRH milestones in the context of cystic fibrosis needs education, guidance, and access to SRH services. In this
http://dx.doi.org/10.1016/
S2213-2600(14)70231-0 Review, we discuss scientific knowledge of SRH in patients with cystic fibrosis across the life course and clinical
Department of Respiratory
practices for SRH within cystic fibrosis care. We identify crucial gaps in SRH education of patients and their
Medicine (K B Frayman MBBS), access to resources and then present a model of care for provision of developmentally appropriate SRH education
and Centre for Adolescent and care within cystic fibrosis services across the life course. This model emphasises the central importance of the
Health (Prof S M Sawyer MD), cystic fibrosis team and service links to primary and specialist SRH care.
Royal Children’s Hospital,
Melbourne, VIC, Australia;
Murdoch Children’s Research Introduction have resulted in many young adults carrying a heavy
Institute, Melbourne, VIC, Cystic fibrosis has long been regarded as a multisystem, burden of care, with uncertain effects on their SRH. Typical
Australia (K B Frayman,
life-limiting disorder of childhood, but it is now equally developmental milestones in education and employment,
Prof S M Sawyer); and
Department of Paediatrics, established as a chronic illness of adulthood. In many SRH, and cystic fibrosis are outlined in figure 1.
University of Melbourne, parts of the world, children with the disease have a Young people with cystic fibrosis encounter the same
Melbourne, VIC, Australia predicted life expectancy of 50–60 years, and now as SRH challenges as their healthy peers. Additionally, they
(Prof S M Sawyer)
many adults as children are living with cystic fibrosis.1 face challenges that are unique to people with chronic
Correspondence to: The importance of sexual and reproductive health (SRH) illnesses, and to cystic fibrosis in particular. Both their
Prof S M Sawyer, Centre for
Adolescent Health, Royal
in the lives of people with cystic fibrosis therefore has, social and sexual experiences and the potential implications
Children’s Hospital, Parkville, and will continue to, change greatly. of these behaviours are affected by living with the disease,
VIC 3052, Australia These improvements in health have occurred alongside its associated complications, and their health-care needs.
susan.sawyer@rch.org.au
evolving social and sexual contexts, and broad scientific In this context, previous scientific literature about SRH
See Online for appendix advances. Typical sexual and reproductive milestones have education and outcomes in people with cystic fibrosis
markedly shifted; the age at first sexual activity is earlier risks being outdated. We review the scientific knowledge
than in previous generations and first marriage and of SRH in cystic fibrosis across the life course and then
parenthood occur substantially later.2 Opportunities for describe present clinical practices, expanding the
parenting and options relating to contraception, assisted historical focus on pregnancy and male infertility to
fertility, and obstetric care have expanded, with different incorporate broad aspects of SRH (panel 1). We conclude
ethical considerations. However, advances in treatment by presenting a model of care that, compared with present
ad-hoc approaches, is expected to deliver more acceptable
and appropriate SRH education and care to children,
Key messages adolescents, and adults with cystic fibrosis.
• Young people growing up with cystic fibrosis face the same developmental challenges
as their healthy peers, including those relating to sexuality and reproduction. SRH and development
• The historical focus of sexual and reproductive health (SRH) in cystic fibrosis has been Puberty
on pregnancy and male infertility. A wide range of SRH concerns is now appreciated to Historically, onset of puberty in young people with cystic
be relevant. fibrosis was delayed, with a lag of roughly 2 years from
• Across the life course, SRH needs of people with cystic fibrosis are unmet. normal timing of menarche (a common surrogate
• Patients need their cystic fibrosis service to actively address their SRH across the life marker of pubertal timing) or attainment of pubertal
course. peak height velocity. A summary of the changing age of
• Parents need access to timely SRH education to support them to educate their children. onset of puberty and factors affecting pubertal
• Provision of contraception and management of pregnancy cannot be addressed development in children and adolescents with cystic
without a strong understanding of the health status of individual patients. fibrosis is included in the appendix. Findings from
• The literature suggests that ages exist by which discussion of specific SRH topics with studies in Poland continue to show substantial
parents and patients should occur. discrepancies in growth, physical stature, and menarchal
• We have provided a model of care as a framework to address SRH within cystic fibrosis age compared with population norms.3–6 However,
services across the life course. Led by cystic fibrosis physicians, this model describes analysis of cystic fibrosis registry data from western
roles and responsibilities for the cystic fibrosis specialist team, primary care providers, Europe and North America shows far less effect than the
and specialist sexual and reproductive health providers, showing the importance of Polish studies, with delay in pubertal onset of only
communication between these groups. 0–6 months, albeit with reduced peak height velocity.7,8
Such delays have been regarded as a physiological

70 www.thelancet.com/respiratory Vol 3 January 2015

 Review

Infancy Early Late Early Late Young Adulthood Ageing

(0−1 childhood childhood adolescence adolescence adulthood (25+ years)
years) (1−4 years) (5−9 years) (10−14 years) (15−19 years) (20−24 years)

Education
and Pre-school Primary school Secondary school Tertiary education, training and employment
employment

Sexual and
reproductive Gender identity Puberty Sexual debut Cohabitation Parenthood Menopause
health

Cystic fibrosis-related liver disease

Pancreatic enzymes
Cystic Cystic fibrosis-related diabetes •Transplantation
Transplantation
Airway clearance
fibrosis Long-term venous access •End-of-life
End-of-lifecare
care
Antibiotics
Percutaneous gastrostomy

Figure 1: Developmental milestones

This timeline provides a schematic indication of the typical ages of some of the key developmental milestones across the life course in the domains of education and
employment, sexual and reproductive health, and cystic fibrosis care.

response to malnutrition, persistent inflammation, and
progressive pulmonary disease. As the health of children
with cystic fibrosis improves, central actions of the cystic
fibrosis transmembrane conductance regulator (CFTR)
protein, expressed in the hypothalamus, have been raised
as an additional explanation.9
Menstruation
After menarche, women with cystic fibrosis are expected
to have normal menstrual cycles and sex hormone
concentrations. Although episodes of secondary
amenorrhoea can accompany deteriorations in health,
systematic exploration of the frequency of anovulation
and amenorrhoea, which have implications for bone
health, fertility, and contraception, is missing from the
scientific literature,9,10 and no research exists about the
experience of menopause in cystic fibrosis.
Sexual debut
Young people with cystic fibrosis engage in the same
sexual behaviours as their healthy peers. In 1995, Sawyer
and colleagues11 found no difference between adult
Australian women with cystic fibrosis and controls
(healthy age-matched people without CF) in the age of
onset of sexual intercourse, the proportion who were
sexually active, and marital status, although women with
the disease were significantly less likely to use
contraception. In 2005, 96% of adult Australian men with
cystic fibrosis reported ever having been sexually active,
with a mean age at first intercourse of 17·9 years (SD 3·5,
range 10–32).12 In Poland, 68% of young adult women
with cystic fibrosis reported having been sexually active,
with a mean age at first intercourse of 19·2 (SD 1·56) years,
similar to population norms.5
Only two studies13,14 have explored sexual activity in
adolescents with cystic fibrosis compared with control
populations. In 1990, Cromer and colleagues13 documented
that 43% of adolescents with cystic fibrosis were sexually
active, despite pubertal delay, compared with 60% of
controls. In 1998, Britto and colleagues14 showed that
although adolescents with cystic fibrosis were older (mean
age 15·7 years) at first sexual activity than matched
controls (14·6 years; p=0·237), they were equally likely to
engage in risky sexual behaviours. 42% of those with the
disease had not used barrier protection at last intercourse
(control 46·2%; p=0·71), 19% had not used any form of
contraception (including condoms) at last intercourse
(control 13·3%; p=0·05), and 47% had had three or more
sexual partners (control 44·4%; p=0·81).
Panel 1: Sexual and reproductive health domains to address
with patients with cystic fibrosis
General sexual and reproductive health domains
• Pubertal development and timing of menarche
• Prevention of sexually transmitted infections and use of
barrier protection
• Immunisation (human papillomavirus and hepatitis B virus)
• Contraception*
• Pap smears
• Reproductive decision making*
• Menopause
Cystic fibrosis-specific sexual and reproductive health
domains
• Urinary incontinence
• Genital candidosis
• Fertility (male and female)
• Assessment of fertility status (semen analysis)
• Genetic and prepregnancy counselling
• Access to assisted reproductive technologies
• Pregnancy
*Typical behaviours with considerations specific to cystic fibrosis.

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 Review
For a young person with a chronic illness, the risks of
unsafe sexual activity are amplified.15 Sexual debut now
usually occurs during adolescence in high-income
countries. In a large predominantly European sample,
29% of boys and 23% of girls were sexually active before
age 15 years,16 and in the USA, more than 90% of young
adults reported sexual debut during adolescence.17 For a
young person with cystic fibrosis, who faces the future
prospect of solid organ transplantation and associated
immunosuppression, the implications of an unplanned
pregnancy or sexually transmitted infection (STI) are
particularly substantial, providing a strong impetus for
preventive intervention.
STIs
Remarkably little scientific literature exists regarding
STIs in cystic fibrosis. In a study18 of Australian men
with cystic fibrosis, participants reported a lifetime
prevalence of STIs of 5%. People with cystic fibrosis
would be expected to have a normal response to some
STIs (eg, chlamydia, the most common STI).19
However, hepatitis B and C infections risk a poorer
prognosis than in people without cystic fibrosis,
particular in the setting of concomitant cystic fibrosis-
related liver disease.
STIs can jeopardise future lung transplantation.
Chronic infection with hepatitis B, hepatitis C, or HIV
are exclusion criteria for lung transplantation,20 and
latent human papillomavirus (HPV) and herpes simplex
virus infections can pose substantial long-term risks with
immunosuppression.21 In a retrospective study of
166 Australian female lung-transplant recipients,22 the
incidence of cervical abnormalities was five-times higher
than in the general population. Population studies of
men report increased prevalence of HPV-related cancers
in general.23 These data suggest the importance of
primary prevention with HPV immunisation for both
boys and girls in early adolescence, regular surveillance
(Pap smears) in women, and an emphasis on barrier
protection in prevention of STIs.
Contraception
Women with cystic fibrosis have access to the usual
range of contraception, including combined hormonal
contraceptives (combined oral contraceptive pill and
vaginal ring), long-acting reversible contraceptives such
as progestogen-only drugs and intrauterine devices
(IUDs), and barrier methods.24 The interplay of disease-
specific risk factors, including liver disease, cholelithiasis,
cystic fibrosis-related diabetes, osteoporosis, and totally
implantable vascular access devices complicates contra-
ception decisions. Yet, scientific literature to guide the
choice of appropriate contraceptive drugs for women with
cystic fibrosis is scarce.
Combined hormonal contraceptives are absolutely
contraindicated in pulmonary hypertension and decomp-
ensated cirrhosis.24–26 Standard preparations of the
72
combined oral contraceptive pill are associated with a two
to three-times increased risk of venous thrombo-
embolism,24 which is of particular importance for patients
with totally implantable vascular access devices,
associated with a 5–14% risk of venous thrombo-
embolism.27 Liver enzyme-inducing drugs, including
rifampicin and rifabutin, can interfere with the
effectiveness of the combined oral contraceptive pill, and
so barrier contraception is recommended during and
28 days after their use. Non-liver enzyme-inducing
antibiotics are no longer regarded as a concern for adverse
drug interactions with hormonal contraceptives,24,25 but
malabsorption of oral drugs has been raised as a potential
risk.26 Progestogen-only drugs, including depot medroxy-
progesterone acetate intramuscular injections, etono-
gestrel implants, and levonorgestrel IUDs, are relatively
contraindicated in decompensated cirrhosis. Con-
comitant use of etonogestrel implants and liver enzyme-
inducing drugs is a concern, and depot med
roxy-progesterone acetetate is associated with accelerated
but potentially reversible loss of bone mineral density.24
IUDs (both copper and levonorgestrel) are effective,
reversible, and longlasting (copper IUD, 10 years;
levonorgestrel IUD, 5 years). Although previously
reserved for multiparous women, these devices are
increasingly used safely in adolescents and nulliparous
women.24,25
The survival disadvantage of women with cystic
fibrosis, which becomes particularly apparent from
adolescence, has prompted questions about the effect of
endogenous and exogenous sex hormones on disease
progression, an area that warrants more research. In a
retrospective analysis of women attending a single
cystic fibrosis centre in the UK between 1981 and 2010,
Kernan and colleagues28 showed no difference in clinical
outcome measures between 57 women exposed to oral
contraceptives and matched controls, or between 3 year
periods of consecutive exposure and non-exposure in
the same patients. Chotirmall and colleagues29 showed
that in-vitro exposure of Pseudomonas aeruginosa to
oestradiol was associated with mucoid colony formation
and suggested that in menstruating women with cystic
fibrosis, oestradiol levels correlated with respiratory
exacerbations. They also raised questions about whether
respiratory exacerbations might occur less frequently in
women taking the oral contraceptive pill than in those
not taking it.29
In view of the IUD safety profile compared with
traditional forms of hormonal contraception, such as the
oral contraceptive pill and progestogen-based subdermal
implants, the IUD is an appropriate early choice for
many young women with cystic fibrosis. Although most
women access contraceptive advice from their family
doctors,30,31 these complexities reinforce the need for
active engagement of the cystic fibrosis team about
contraception, and consideration of subspecialist referral
if appropriate.
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Urinary incontinence
Urinary incontinence is prevalent in adolescents and
adults with cystic fibrosis, but, perhaps not unexpectedly,
under-reported to health-care professionals and, in many
cases, not disclosed even to parents.32–34 Interference
with physical activity (including physical education
classes at school) and airway clearance has been
reported, with common triggers being coughing,
physical activity, huffing, spirometry, and laughing.32–39
Existing studies do not use consistent definitions of
urinary incontinence prevalence, severity, or fre-
quency.32–39 The effect of urinary incontinence on men
with cystic fibrosis and potential emotional distress are
incompletely explored. A study40 of 12 women with cystic
fibrosis suggests that pelvic floor strengthening exercises
are effective at reducing leakage in the short term.
Research using age-matched controls is needed to
further quantify the incidence of urinary incontinence
in both sexes, together with the effect of preventive
interventions and treatment.
Other sexual health issues
Women with cystic fibrosis report an increased
prevalence of genital candidosis.41 Symptoms are
associated with antibiotic use;11,41 cystic fibrosis-related
diabetes, immunosuppression, and corticosteroid use
are additional risk factors.42 Men with cystic fibrosis
are also expected to be at increased risk of genital
candidosis. Despite accessible treatment, this topic
has received little attention in the scientific literature.
An increased incidence of testicular cancer in men
with cystic fibrosis has been reported.43 As the
prevalence of cystic fibrosis-related diabetes and its
microvascular complications increase, erectile
dysfunction might also occur.
Male infertility
Male infertility is secondary to congenital bilateral
absence of the vas deferens. Roughly 98% of men with
cystic fibrosis have obstructive azoospermia, with low
seminal volume, pH, and fructose concentration, and
anatomical and functional abnormalities of the
epididymis and seminal vesicles.44,45 CFTR is expressed
in the male reproductive tract, and CFTR gene mutations
are associated with congenital bilateral absence of the
vas deferens in men without phenotypic features of
cystic fibrosis.44,45 The precise mechanisms by which
CFTR mutations result in congenital bilateral absence of
the vas deferens are poorly understood, although the
distal epididymis and vas deferens seem particularly
sensitive to CFTR dysfunction.44 Mullerian duct
derivatives are unaffected, and congenital bilateral
absence of the vas deferens secondary to CFTR
mutations is not associated with renal tract anomalies.45
CFTR has also been suggested to have a role in
spermatogenesis, and dysfunctional bicarbonate
transport has been suggested to impair sperm
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Review
capacitation;46 however, many men with congenital
bilateral absence of the vas deferens are able to father
children using assisted reproductive technologies.44
CFTR mutation screening and genetic counselling
are recommended.
Female fertility
Since 1994, the North American Cystic Fibrosis
Foundation has reported about 140 pregnancies per year
in women with cystic fibrosis in the USA and Canada,
with 3–4% estimated to become pregnant per year.9,47
Most pregnancies are conceived spontaneously. As a
result, menstruating women, including those with severe
lung disease, should be assumed to be fertile. Case
reports describe spontaneous pregnancies in women
with predicted forced expiratory volume in 1 s (FEV1) as
low as 17%.48
Although fertility has long been regarded as reduced in
women with cystic fibrosis, this assumption continues to
be unquantified. CFTR is expressed in the cervix,
endometrium, fallopian tubes, and hypothalamus.
Abnormally tenacious cervical mucus without normal
cyclical variation has been described, which potentially
acts as a mechanical barrier to conception.9,49 Defects in
regulation of uterine fluid and bicarbonate secretion
could result in impaired sperm capacitation and
potentially decrease fertility.46
Parenthood
For the adult with CF, reproductive decision making
involves confronting many disease-specific challenges.
These challenges include uncertainty about fertility
status or known male infertility, access to and outcome of
assisted reproductive technologies, the effect of
pregnancy and parenting on health, the risk of cystic
fibrosis in offspring, and the practical, emotional, and
ethical considerations of raising children while facing
increasing morbidity and reduced life expectancy.50
A substantial proportion of adults with cystic fibrosis
are married or in long-term relationships, and are
increasingly choosing to become parents. A surprising
proportion of unplanned pregnancies have been
reported—from 26% of women with CF in one study30
to 50% in another.51 Findings from one study11 showed
that more than half of adult Australian women with
cystic fibrosis wanted to have children in the near
future. 22% had tried to conceive, 67% of whom were
successful. Similar attitudes were evident in Scotland,
where 26% of female and 6% of male participants
(median age 24 years, range 19–31) were parents, with
most (72% of women and 85% of men) reporting that
having children was important.52 Investigators of a large
cross-sectional cohort study53 from the UK cystic fibrosis
database in 2001 documented that 1·3% of partners of
men and 5·7% of women with cystic fibrosis of
reproductive age had been pregnant, although only 1%
of men and 0·5% of women had sought fertility
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treatment. Studies suggest that increasing numbers of
adults with cystic fibrosis are pursuing or wish to
pursue parenthood5,12—eg, in Australasia, 22% of men
at five cystic fibrosis centres were fathers, and 85% of
those who were not fathers wanted to have children in
the future.18
Assisted reproductive technology
In men with congenital bilateral absence of the vas
deferens, sperm are retrieved from the caput of the
epididymis via either percutaneous or microsurgical
epididymal sperm aspiration, or from the testis directly
via percutaneous or open biopsy. Harvested oocytes are
fertilised via intracytoplasmic sperm injection, with
success rates in men with cystic fibrosis similar to those
in men with obstructive azoospermia of other causes.54,55
Retrospective studies of assisted reproductive tech-
nologies in men with cystic fibrosis from the USA,56
France,57 and Australia54 report pregnancy rates of
60–65%. An increased risk of neonatal adverse outcomes
has been associated with assisted reproductive
technologies in general, and an increased risk of genetic
malformations with intracytoplasmic sperm injection
specifically.58 An alternative parenting option for men
with cystic fibrosis is artificial insemination with donor
sperm. Fostering and adoption are options in some
countries. The extent of remarriage also provides
opportunities for step-parenting.
Women with cystic fibrosis have access to established
in-vitro fertilisation techniques. Although studies of
assisted conception in women with cystic fibrosis are
scarce,59–61 the recognised risks, specifically multiple
gestation and ovarian hyperstimulation syndrome, are of
particular concern.62,63 For both men and women with
cystic fibrosis, preconception genetic screening of
partners is indicated, with subsequent consideration of
preimplantation genetic diagnosis.
Pregnancy
Despite the increased respiratory, cardiovascular, and
metabolic demands of pregnancy, many women with
cystic fibrosis deliver healthy infants with little effect on
their own health. Women who become pregnant have
better pulmonary function and nutritional status with
fewer complications of cystic fibrosis than those who do
not conceive.64,65 These women also undertake more
treatment for cystic fibrosis, have more attendance at
outpatient appointments, and, in keeping with
population-wide trends, are older than those who do not
become pregnant.53,64,65
However, pregnancies have been reported in
adolescents with cystic fibrosis and women with severe
respiratory compromise, including those awaiting lung
transplantation.60,61,66 The reproductive decisions of
women with cystic fibrosis have not been systematically
explored, and no comparisons with healthy women exist.
Many questions are raised by reported rates of unplanned
74
pregnancy of 26–50% in women with cystic fibrosis in
the UK30,51 and Australia,11 and not-infrequent reports of
termination of pregnancy, for maternal medical and
psychological reasons.47,59,65–68
Findings from large epidemiological studies comparing
women with cystic fibrosis who have been pregnant with
never-pregnant controls with cystic fibrosis show that
pregnancy has no sustained negative effect on maternal
physical health.59,64,65 In one cross-sectional study65 of
680 women enrolled in the North American Cystic
Fibrosis Foundation registry matched with 3327 controls,
pregnancy was positively associated with 10 year survival,
even in those with severe respiratory compromise (FEV1
<40%) and cystic fibrosis-related diabetes. However,
transient decreases in pulmonary function, increased
diagnoses of insulin-dependent diabetes, and increased
need for treatment, including admission to hospital, are
well described.59,64,66,69,70 Analysis of 119 women and
1190 controls from the Epidemiological Study of Cystic
Fibrosis71 suggests that pregnancy is associated with
increased treatment for exacerbations, and low health-
related quality-of-life scores, but a trend towards
increased survival.
However, for some women with cystic fibrosis,
pregnancy poses substantial risk.47 Low, and perhaps
more importantly, unstable pulmonary function is asso-
ciated with poorer maternal and neonatal outcomes than
in women with high or stable pulmonary function.47 Poor
nutrition at baseline and difficulty with weight gain
during pregnancy are also poor prognostic factors.61,70,72,73
Pulmonary hypertension, cor pulmonale, and respiratory
failure are absolute contraindications to pregnancy. A
predicted FEV1 of more than 60–70% is recommended,
but successful pregnancies have been described in
women with substantially lower lung function.47 Liver
disease and infection with Burkholderia cepacia are
relative contraindications.47
Offspring of women with cystic fibrosis are largely
healthy. Prematurity is associated with maternal medical
compromise, and semielective delivery of infants with
birthweights appropriate for their gestational age is
described.61,67 Infants have an increased risk of cystic
fibrosis and of their mother dying during their childhood.
All pregnancies in women with cystic fibrosis are
deemed high risk. Safe, successful pregnancies need
multidisciplinary care from specialised cystic fibrosis,
obstetric, anaesthetic, and possibly neonatal services.
Practice recommendations, with emphasis on careful pre-
pregnancy planning, are described in the European Cystic
Fibrosis Society consensus guidelines for the management
of pregnancy,47 and summarised in panel 2. Genetic and
psychological counselling for both the patient and her
partner are recommended, with attention to the emotional
and practical aspects of pregnancy and raising a child.
Maternal physical health should be optimised in
anticipation of conception, and attention to cystic fibrosis
care maintained throughout pregnancy and the post-
www.thelancet.com/respiratory Vol 3 January 2015

partum period. Areas of particular concern include airway
clearance techniques, maintenance of nutrition, screening
for diabetes, and antimicrobial choice.47 Breastfeeding is
encouraged for as long as the nutritional status of mother
and infant are stable. The prevalence of postnatal
depression in women with cystic fibrosis is unknown.47
Pregnancy in recipients of lung transplants is regarded
as high risk for both mother and fetus. In a case series74 of
ten women, more than 50% of the women had premature
infants and 40% died after a mean survival of
26 (range 18–38) months post partum. This finding is
supported by data from the US National Transplantation
Pregnancy Registry, which shows that 48% of 11 recipients
of lung transplants who became pregnant lost graft
function within 2 years, and neonatal complications were
reported in 71% of recipients.75 Recommendations are to
wait for a period of stable health of at least 2 years after
transplantation before conception.47
Present clinical practices
SRH education
Education of parents regarding cystic fibrosis-related SRH
varies. European guidelines on early management of cystic
fibrosis emphasise that families should be educated from
the time of diagnosis “so that they develop progressively an
understanding of cystic fibrosis care and what changes to
expect as their child grows”.76 However, no specific reference
is made to infertility or to how parents should address SRH
in the context of their child’s cystic fibrosis as he or she
matures. In some cystic fibrosis centres, parents receive
information regarding male infertility from their son’s
cystic fibrosis clinician around the time of diagnosis;77
however, this practice seems far from universal.
Parental knowledge of SRH in cystic fibrosis has been
explored in five studies,5,77–80 only one of which included
parents of young children77 (age 6–19 years; tables 1 and
2). In this study at a cystic fibrosis centre in Australia,
99% of parents were aware of their son’s reduced fertility,
including 86% who were aware of probable infertility,
having been informed by the cystic fibrosis team at
around the time of diagnosis. In small studies in both
the UK78 and USA,79 only 50% of parents understood that
their adolescent sons with cystic fibrosis were likely to be
infertile. The only study5 of cystic fibrosis-related SRH
knowledge of parents of adolescent and young adult
women, done in Poland in 2009, documented poor
parental understanding, including misconceptions
regarding fertility and the potential effect of pregnancy
on their daughter’s health.
Parents want to be involved in the SRH education of
their children with cystic fibrosis, but identify an
absence of knowledge and confidence as substantial
barriers to this.77 They consistently identify their child’s
cystic fibrosis team as the preferred source of cystic-
fibrosis related information for themselves, yet mostly
do not get information on SRH from this team. At one
Australian centre where all parents were informed of
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Review
Panel 2: Management considerations for pregnancy in women with cystic fibrosis
Before pregnancy
Counselling and pregnancy planning
• Genetic; medical; psychological; practical
Health optimisation
• Lung function; aerobic capacity; infection management;* respiratory physiotherapy
and airway clearance; postural and pelvic floor muscles; nutritional status (eg, folic
acid and vitamins A and D); glycaemic control (eg, oral glucose tolerance test)
During pregnancy
Health maintenance
• Frequent clinical review (monthly, then every 2 weeks during third trimester)
Care coordination
• Communication between cystic fibrosis team and obstetric service
Specific considerations
• Medications;† respiratory physiotherapy and airway clearance; urinary incontinence;
gastro-oesophageal reflux; constipation; hypoxia; ventilatory failure
Nutritional management (recommended weight gain ≥11 kg)‡
During childbirth
Planning
• Anaesthetic review needed in context of respiratory health (planning meeting
recommended at roughly 26 weeks’ gestation); probable need for peripheral venous
access; review cystic fibrosis drugs and respiratory physiotherapy
Labour
• Preference for vaginal delivery; caesarean section with regional anaesthesia if
maternal or fetal compromise; analgesia choice; respiratory physiotherapy and airway
clearance needed
Delivery location
• Obstetric high-dependency unit
After pregnancy
Health maintenance
• Respiratory physiotherapy might need to be started in the immediate post-partum period;
more frequent medical review to support usual cystic fibrosis care and monitor weight
Care coordination
Psychological concerns
• Monitor for postnatal depression
Breastfeeding
• Review all drugs;† monitor maternal nutrition and weight
Contraceptive advice
*Conception during acute exacerbations is not advised. †The following anti-infective drugs are of concern during pregnancy,
delivery, or breastfeeding. First trimester: intravenous aminoglycosides (once-daily dosing recommended if needed); inhaled
aminoglycosides (likely to be safe); clarithromycin; rifamycins; trimethoprim; carbapenemens; metronidazole; vancomycin;
teicoplanin; fluconazole; itraconazole; posaconazole; voriconazole; aciclovir; valaciclovir; ganciclovir. Second and third trimesters:
intravenous aminoglycosides; fluoroquinolones; rifamycins; sulphonamides; tetracyclines; carbapenems; colistin;
chloramphenicol; metronidazole; vancomycin; teicoplanin; fluconazole; itraconazole; posaconazole; voriconazole; ganciclovir. At
delivery: sulphonamides; tetracyclines; chloramphenicol. Breastfeeding: fluoroquinolones; azithromycin; roxithromycin;
clarithromycin; chloramphenicol; metronidazole; fluconazole; itraconazole; posaconazole; voriconazole; amphotericin;
ganciclovir. Other drugs of potential concern during pregnancy: ursodeoxycholic acid (first trimester) and systemic corticoster-
oids. ‡Enteral (and occasionally parenteral) feeding might need to be considered. Continuous feeds might be preferred. Enteral
feeding needs monitoring of blood glucose concentrations and risk of aspiration. Adapted from Edenborough and colleagues.47
male infertility at around the time of diagnosis, fewer
than one in five had subsequent discussions of SRH
with their son’s cystic fibrosis clinician.77 At the same
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Participants Male fertility Female Knowledge Genetics Knowledge of Timing of first Source of most cystic Proportion of parents
knowledge fertility of effect of knowledge effect on education fibrosis-related SRH who want more
knowledge pregnancy sexual about male information information
activity infertility
Hames et al, 20 parents of Effect on Female Potential for Risk of cystic People with Not explored Not explored 15%
1991, UK78 22 patients (73% reproductive patients can health fibrosis in child cystic fibrosis
male); age range organs: 35%; become problems: of parent with can have
11–20 years effect on fertility: pregnant: 95% 30% cystic fibrosis: normal sex
50% 10%; parents of lives: 95%
a child with
cystic fibrosis
are both
carriers: 100%
Sawyer et al, 10 parents of Infertility: 50%; .. .. Not explored Not explored At son’s diagnosis Not explored Not explored
1998, USA79 adolescent male reduced fertility: (80% at diagnosis
patients; mean 10% (varied in infancy, 20% at
age 16 years (SD understanding of diagnosis age
1; range 14–17) cause: two parents 12 years)
thought infertility
was a side-effect
of drugs)
Nixon et al, 52 mothers of .. Not explored Not explored Not explored Not explored Ever discussed Cystic fibrosis doctor: 96%
2003, adolescent female female sexual 42%; books and
Australia80 patients; median health with their magazines: 38%; other
age 15 years daughter’s cystic cystic fibrosis team
(range 12–19) fibrosis doctor: member: 23%; family
22% doctor: 21%; school and
teacher: 13%; parent of
other children with
cystic fibrosis: 12%;
other friend: 8%;
internet: 2%
Frayman et al, 148 parents (76% Reduced fertility: .. .. Not explored Not explored Around time of Sought additional 82%; information about
2008, of eligible 99%, including son’s diagnosis: information: 67%; ART: 55%; semen analysis
Australia77 parents) from nearly always median age discussed SRH with and establishment of
84 families (82% being infertile: 2 months cystic fibrosis specialist fertility status: 46%; age-
of eligible 84%; male (range 0–72); after learning of appropriate information
families) of male patients can father informed by infertility: 19%; for adolescent boys: 46%;
patients; mean children using cystic fibrosis discussed with other pathophysiology of
age 12·7 years ART: 96% team: 83% (cystic health-care infertility: 45%; how to
(range 6–19) fibrosis specialist: professional: 4% inform son about
56%; other team possible fertility issues:
member: 8%; 43%; how to cope with
written son’s possible fertility
information from issues: 37%; general SRH
cystic fibrosis information: 35%; how
team: 19%) to decide what to tell
their sons: 32%
Korzeniewska 64 parents of Normal fertility: Normal Risk of Afraid of risk of Not explored Not explored Parent of other children Not explored
et al, 2009, female patients; 44%; reduced fertility: 58%; substantial having a child with cystic fibrosis:
Poland5 mean age fertility: 2%; nearly reduced deterioration with cystic 58%; papers or
20·94 years always infertile: fertility 23%; in health: fibrosis: 9% magazines: 50%;
(SD 1·5; range 38%; always always infertile: 53% internet: 20%; cystic
16–24); response infertile: 5%; 6%; unsure: fibrosis doctor: 16%;
rate for all female unsure: 13% 13% popular scientific
patients older publication: 9%
than age 16 years:
51%, but 72% for
female patients
aged 16–24 years

ART=assisted reproductive technology. SRH=sexual and reproductive health. “Not explored” refers to a topic that could have been explored, but was not, and middle dots show when the topic was not applicable.

Table 1: Cystic fibrosis-related SRH knowledge and education of parents

centre, fewer than one in four parents had ever had obtained any SRH information at all from the cystic
discussed SRH with their daughter’s cystic fibrosis fibrosis service.5
team,80 and in Poland, only 15% of parents of older Beyond discussions at diagnosis, parents generally
adolescents and young adult women (age 16–24 years) instigate discussions with cystic fibrosis teams about

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 Review

Ideal timing for Preferred information Ideal age for son to Ideal age for son or Ideal source of Parents’ attitude to Parents’ attitude to their own
initial parental sources for parents learn of infertility daughter to have son’s initial cystic fibrosis specialist’s involvement in cystic fibrosis-
education first SRH discussion information initial discussion of related SRH education of their
with health-care about male infertility with son son or daughter
professional infertility
Hames 1991, UK78 Not explored Not explored Not explored Not explored Not explored Not explored Not explored
Sawyer et al, Not explored Not explored Not reported Mean age 13·9 years Not explored Present: 10%; would have Sufficient knowledge to discuss
1998, USA79 (SD 2·6; range liked to have been present: with their son: 10%; comfortable
10–18) 50% to discuss with their son: 30%
Madge et al, Not explored Not explored Mean age 13·5 years Not reported Cystic fibrosis Discussions should occur Not reported
1999, UK81* (range 10–18); when team and parents: during outpatient visit:
child mature enough: 78%; parents only: 62%; unsure: 24%
22%; older than age 18%
16 years: 10%
Nixon et al, 2003, Mean age Not explored ·· Mean age 12·2 years ·· ·· Not explored
Australia80 9·4 years† (SD 2·3);† before age
14 years: 92%
Frayman et al, Around time of Written information: Should “definitely Not reported Parents (alone or Want to be informed of Comfortable to discuss with their
2008, Australia77 diagnosis: almost 65%; cystic fibrosis know” by mean age together with specialist’s discussions: son: 92%; comfortable to discuss
75%; within specialist: 50%; cystic 15 years cystic fibrosis 58%; specialist should first with their son: 85%; satisfied
2 years of fibrosis team: 45%; specialist): 95% obtain parental consent: with present level of knowledge:
diagnosis: 10% internet: 19%; support 21%; specialist should only 30%; do not know enough to
group: 3%; family discuss infertility if asked inform their son first: 27%; would
doctor: 2%; parent of by parent or patient: 4%; have liked more information:
other child with cystic parents do not need to be 42%; parental confidence
fibrosis: 1%; other: 4%‡ informed: 18% decreased as son’s age increased
Korzeniewska Not explored Not explored ·· After menarche: ·· ·· Never discussed with their
et al, 2009, 43%; age daughter: 68%; initiated
Poland5 12–14 years: 38%† conversations: 20%

SRH=sexual and reproductive health. “Not explored” refers to a topic that could have been explored, but was not; “not reported” refers to one that was discussed but the statistic not reported; and middle dots
show when the topic was not applicable. *Study participants: 91 parents (74% mothers). †Parents of female adolescents, about preferences for education about female SRH. ‡Parents preferred to receive written
information, but the cystic fibrosis specialist was their preferred source of more specific information.

Table 2: Parent preferences about cystic fibrosis-related SRH education

SRH. Parents describe several barriers to such dis-
cussions, including concerns regarding privacy, embarr-
assment (of the parent, their child, and their doctor),
concerns regarding the appropriateness of having these
discussions with their child present, little time in the
clinic, concerns that other cystic fibrosis issues demand
more immediate attention, and difficulty in initiation of
these conversations.77,80 Health-care professionals’ own
reports of the SRH education that they provide to
parents of boys with cystic fibrosis are consistent with
parents’ experiences.82 Two-thirds of the 32 cystic
fibrosis clinicians questioned in a 2001 US study82
reported that they routinely informed parents of their
son’s probable infertility soon after diagnosis. Half of
these would only address SRH again if parents
specifically asked. One in five reported that they first
discuss infertility with parents when their sons are
peripubertal, and one in eight reported not discussing
SRH with parents at all.
The understanding of the SRH education of young
people with cystic fibrosis is predominantly derived
from parent reports, a study of health-care professionals’
practices, and older adolescents’ and adults’
retrospective accounts of their early education. 43% of
parents in an Australian study77 were sure that their
sons (who ranged in age from 9 to 19 years, with a
median age of 16 years) had been informed of probable
infertility. These parents reported that their sons first
learnt about their probable infertility at a median age of
11 years, most often from their parents (76%), although
17% believed that their sons first learnt of probable
infertility from their own reading. Only six parents
reported that their son’s cystic fibrosis specialist had
been involved in initial SRH discussions, generally
after the subject had already been discussed by the
parent. 20% of parents were unsure of their son’s
knowledge, and 37% believed that their son was not
aware of probable infertility. At the same cystic fibrosis
centre, adolescent female patients identified their
parents as their predominant source of SRH
information. Only 13% of girls (who ranged in age from
12 to 19 years, with a median age of 15 years) had ever
discussed SRH with their cystic fibrosis specialist,
citing difficulty with the initiation of the discussion and
embarrassment as barriers to such conversations.80
Similarly, cystic fibrosis clinicians describe difficulties
educating young people about SRH. Clinicians in the
one study82 of health-care professional attitudes and
practices reported routinely discussing infertility with
adolescent boys at a mean age of 15·2 years, although
they identified 13·8 years as the most appropriate age to
start such discussions. The information that they

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 Review
discussed varied: only half of the clinicians reported that
they reassured boys that cystic fibrosis does not affect
sexual function, and fewer than 20% reported discussing
reproductive options. Clinicians identified several
barriers to discussion of SRH with adolescents,
including embarrassment, little time or difficulty finding
the right time, difficulty discussing bad news,
insufficient training, and competing priorities to address
in cystic fibrosis care. 50% of clinicians reported that
they either informed or sought consent from parents
before initiating such conversations.82
Findings from studies exploring the knowledge of
older adolescents and adults with cystic fibrosis show
further deficits in the timing and source of SRH
education. Adults with cystic fibrosis consistently report
learning about SRH, particularly male infertility, later
than they would have liked and from less than ideal
sources (eg, from peers with cystic fibrosis). In a study18
of 264 adult men from five Australasian cystic fibrosis
centres, only 43% had learnt of their probable infertility
from their preferred source (eg, cystic fibrosis clinicians
or parents). This learning was at a mean of 17·4 years,
substantially later than their preferred age of 14·0 years.
Their age at initial education varied by information
source—three-quarters of those informed by their
parents were younger than 16 years of age at the time,
which was younger than those informed by health-care
professionals. Similar trends are evident in studies of
men from the UK and North America, and in studies of
women. At a regional cystic fibrosis centre in the UK,
women with cystic fibrosis reported receiving their first
SRH advice at an average age of 16·0 years (range
11–27), substantially later than their preferred age of
13·7 years (range 11–18).30 They identified their family
doctor (25%) and parents (21%) as their major sources
of initial SRH information, with only 17% of participants
receiving the information from their cystic fibrosis
clinic. Clearly, substantial numbers of adults with cystic
fibrosis have never discussed SRH with their cystic
fibrosis team, and many of those who have, including
85% of men and 76% of women in a study52 from four
Scottish cystic fibrosis centres, report that they were
unable to obtain all of the information that they needed
from their cystic fibrosis team. Retrospective studies of
adult men suggest that the emotional response to
infertility is less in those who first learn in adolescence,
with the effect increasing over time.12,18
Perhaps unsurprisingly, substantial deficits exist in
the SRH knowledge of both male and female
adolescents and adults with cystic fibrosis (tables 3 and
4). Men are generally aware that cystic fibrosis can
affect their fertility, but consistently underestimate the
prevalence of infertility. The literature describes sub-
stantial confusion; the difference between impotence
and infertility is often unclear, particularly to adolescent
boys, and the need for barrier protection from STIs is
often not appreciated by either boys or men. Almost
78
one in three adult men at a single cystic fibrosis centre
in Australia, where knowledge of reduced fertility was
almost universal, assumed that they did not need to
use condoms.12 This misconception was significantly
more common for men who had first learnt of
infertility from their health-care professional than for
those who had been told by their parents. Similarly,
findings suggest that some women with cystic fibrosis
are confused regarding fertility status and the potential
for pregnancy.5,11
SRH care
The European Cystic Fibrosis Society’s standards of
care89 states that “good general health care information
needs to be communicated to all patients who are
sexually active”, specifically emphasising the importance
of expert advice about contraception, including barrier
protection to avoid STIs, and the need to address cystic
fibrosis-specific SRH topics. Nevertheless, integration of
SRH into routine practice within cystic fibrosis services
varies greatly.
Historically, sexually active women with cystic
fibrosis have been less likely to use contraception than
their healthy peers; many have never discussed their
contraceptive choices with their cystic fibrosis team.11,52
In the only North American study90 documenting
contraceptive use, the proportion of the 69 females
with cystic fibrosis using abstinence or natural family
planning was substantially higher than population
norms (17% vs 1%). In a UK study of 42 women
attending a regional cystic fibrosis centre, Gatiss and
colleagues30 documented pregnancies in 31% of
participants, of which 26% were unplanned. Most
study participants obtained their contraceptive advice
from their family doctor (50%), with 17% attending
family planning clinics, and 10% receiving advice from
their cystic fibrosis team.30 Most had not received any
advice regarding contraception in the context of cystic
fibrosis. Findings from a large UK study of 150 women
(92% response rate) were similar, with one in five not
using contraception. Of the 60% that were using
contraception, over half had received contraceptive
advice from their family doctor, with 20% receiving
counselling from their cystic fibrosis team.31 A high
proportion of unplanned pregnancies and therapeutic
termination of pregnancy in women with cystic
fibrosis coupled with the health risks of pregnancy in
those with severe lung disease and the potential
benefits of prepregnancy counselling, including
genetic counselling, suggest the importance of
integration of SRH care into cystic fibrosis care.47,51,67
Genetic counselling and testing before pregnancy
provide options for prenatal diagnosis of cystic fibrosis
if indicated. Early disclosure of pregnancy also
supports prenatal diagnosis.
Despite the high prevalence of genital candidosis in
people with cystic fibrosis, Webb and Woolnough42 have
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 Review

Participants Male fertility Female fertility Knowledge of Genetics Knowledge of Age at first Source of most cystic Proportion of
knowledge knowledge effect of knowledge effect on education fibrosis-related SRH patients who
pregnancy sexual activity about male information want more
infertility information
Hames et al, 22 patients Effect on reproductive Female patients Potential for Correct risk of People with Not explored Younger than age 33%*
1991, UK78 (73% male); age organs: 27%; effect on can become health cystic fibrosis in cystic fibrosis 18 years: cystic fibrosis
range fertility: 86%; likely pregnant: 91% problems: 45% child of person can have clinic staff and parents
11–20 years infertility: 0% with cystic normal sex equally; older than age
fibrosis: 14%; lives: 86% 18 years: cystic fibrosis
parents of child clinic staff*
with cystic
fibrosis are both
carriers: 64%
Sawyer et al, 55 female Male patients are Fertility is reduced: Pregnancy Correct risk of Not explored ·· ·· ··
1995, patients; nearly always infertile 65%; nearly always worsens lung cystic fibrosis in
Australia11 median age or have reduced infertile: 4%; disease: 62%; offspring: 15%;
22 years (range fertility: 87%; unsure: fertility normal: pregnancy overestimated
18–50); 13% 9%; unsure: 22% improves lung risk: 31%;
response rate: disease: 2%; no unaware of
89% effect: 2%; importance of
unsure: 34% partner’s carrier
status: 15%;
unsure: 38%
Johannesson 14 adult female ·· Not reported Not reported Not reported Not reported ·· Information about Not reported
et al, 1998, patients sexual maturation:
Sweden83 (qualitative cystic fibrosis specialist:
study) 35%; information
about fertility
problems: cystic
fibrosis specialist: 14%;
Cystic Fibrosis
Association: 21%;
information about
overcoming fertility
difficulties:
gynaecologist or cystic
fibrosis specialist: 57%;
Cystic Fibrosis
Association: 36%
Sawyer et al, Ten adolescent Most male patients ·· ·· Not explored Confused Adolescents: Adolescents: health- Not explored
1998, USA79 male patients; are infertile: 60% of infertility with mean care provider: 83%;
mean age adolescents, 90% of impotence: 13·9 years parents: 17%; adults:
16 years (SD 1; adults; understand 40% of (SD 1·6); health-care provider:
range 14–17); correct explanation of adolescents, adults: mean 48%; parents: 17%
and 40 adult infertility: 17% of 20% of adults; 16·0 years
male patients; adolescents misunderstood (SD 4·7)
mean age need for
29 years (SD 9; protection
range 18–53) from STIs: 50%
of adolescents;
26% of adults
Fair et al, 136 patients Aware that male Not explored Not explored Not explored Not explored Under Initial source of Received adequate
2000, UK52 (60% male); patients are usually 16 years: 37%; information about information from
median age infertile: 98%† 16–19 years: male infertility: cystic health-care
24 years (range 20%; older fibrosis clinic: 41%, professional: male
19–31); than 19 years: parent: 26%, Cystic patients: 15%;
response rate: 26%; Fibrosis Trust leaflets: female patients:
70% unknown: 20%;† ever discussed 24%; wanted more
18%; learning SRH with health-care written
from parents professional: male information about
usually before patients: 57%, female fertility: 58%
16 years: 67%† patients: 74%; ever
discussed
contraception in cystic
fibrosis clinic: male
patients: 12%, female
patients: 15%
(Table 3 continues on next page)

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 Review

Participants Male fertility Female fertility Knowledge of Genetics Knowledge of Age at first Source of most cystic Proportion of
knowledge knowledge effect of knowledge effect on education fibrosis-related SRH patients who
pregnancy sexual activity about male information want more
infertility information
(Continued from previous page)
Rodgers et al, 18 male Unstated (all patients Not explored Not explored Not explored Not explored Median Cystic fibrosis team: Not explored
2000, UK84 patients; assumed aware) 17 years (range 33%; parents: 28%;
median age 13–24) written information:
25 years (range 11%; unexpectedly:
16–43); 28% (cystic fibrosis
response rate: patients: 17%; cystic
60% fibrosis textbook: 6%;
doctor: 6%)
Thickett et al, 72 male Rare for male patient Not explored Not explored Not explored Not explored Not explored Sexually experienced Not explored
2001, UK85 patients; mean to father a child: 57%; patients who never
age 24·6 years much less common received advice about
(range 16–43); than normal to father infertility or
response rate: a child: 25%; fertility contraception: 56%;
72% normal: 7%; eight received advice from
men had tried to cystic fibrosis
conceive without physician: 24% (of
success for 1–6 years those who received
advice)
Nixon et al, 55 adolescent ·· Not explored Not explored Not explored ·· ·· Parents: 60%; school Age younger than
2003, female patients; and teachers: 44%; 16 years: 34%; age
Australia80 median age books and magazines: older than 16 years:
15 years (range 38%; friends: 27%; 57%
12–19); cystic fibrosis doctor:
response rate: 24%; other cystic
96% fibrosis team member:
15%; family doctor:
9%; internet: 9%;
friend with cystic
fibrosis: 5%
Sawyer et al, 94 male Nearly always Not explored Not explored Not explored Confused Mean Cystic fibrosis clinic: 66%
2005, patients; mean infertile: 77%, fertility infertility with 16·4 years 55%; parents: 13%;
Australia12 age 30·5 years reduced: 16%, normal impotence: 9% (SD 4·1; range other cystic fibrosis
(SD 7·6; range fertility: 2%, unsure 7–31); younger patient or friend: 11%;
18–54); 4%; effect on male than 15 years: written material: 14%
response rate: fertility due to sperm 32%; learnt
75% transport issue: 76%, from preferred
effect on male fertility source: 53%
due to sperm
production issue:
13%, both 2%, unsure
10%
Houser et al, 51 patients Patients able to have Patients able to Not explored Risk of cystic Not explored Not explored Not explored Not explored
2008, USA86 (47% male); children: 96%; have children: fibrosis in
mean age reproduction more 96%; reproduction offspring if
21 years (range difficult for men than more difficult for partner not a
15–29) for women: 65%; women than for carrier: 59%; risk
unsure: 27%; aware of men: 8%; unsure: of cystic fibrosis
options for men 27% in offspring if
wanting to have partner a carrier:
children: 62%; aware 44%
of ART: 26%
Chotirmall 16 male Male fertility affected: ·· ·· Not explored Not explored Mean age Initial source of Had questions
et al, 2009, patients; mean 100%; correct when first information about about fertility but
UK87 age 24 years explanation for male discussing with male infertility: written were too
(SD 4·0; range infertility: 31%; able health-care material: 44%; ever embarrassed to
19–35); to explain infertility: professional discussed with health- ask: 44%
response rate: 56% 21·9 years care professional: 57%
32% (SD 2·6; range
18–26)
(Table 3 continues on next page)

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 Review

Participants Male fertility Female fertility Knowledge of Genetics Knowledge of Age at first Source of most cystic Proportion of
knowledge knowledge effect of knowledge effect on education fibrosis-related SRH patients who
pregnancy sexual activity about male information want more
infertility information
(Continued from previous page)
Gatiss et al, 42 female ·· Not explored Not explored Not explored Not explored Average age Sources of initial Not received
2009, UK30 patients; mean when first information: family enough advice:
age 29·7 years receiving doctor: 26%, parents: 14%; received no
(range 16–51); sexual health 21%, cystic fibrosis advice: 7%; not
response rate: advice 16 years clinic: 17%, friend: 10%, received specific
76% (range 11–27)‡ family planning clinic: advice about
10%, school: 7%; contraception:
current source of 62%; not
contraceptive advice: received any
family doctor: 50%, information
family planning clinic: about possible
17%, cystic fibrosis antibiotic
clinic: 9·5% interactions with
contraceptive
drugs: 57%
Korzeniewska 64 female Male fertility normal: Female fertility Possibility of Afraid of risk of Not reported ·· Popular scientific Not reported
et al, 2009, patients; 67%, male fertility normal: 66%, substantial having a child publication: 56%;
Poland5 response rate: reduced: 33%, male female fertility health with cystic other patient: 52%;
51% (72% for patients nearly always reduced: 33%, deterioration: fibrosis: 77% internet: 48%; papers
those aged or always infertile: female patients 67% and magazines: 48%;
16–24 years); 0%, aware of ART: 0%; always infertile: cystic fibrosis doctor:
mean age reasons for 2%, female 44%; friend: 19%;
20·94 years contraceptive use patients cannot parents: 17%; siblings:
(SD 1·5; range because of risk of: have children at 15%
16–24); unexpected all: 14%; reasons
pregnancy: 60%, STIs: for contraceptive
3%, both: 7%, no use because of
reason to use risk of:
contraception: 27%, unexpected
unsure: 2% pregnancy: 80%,
STIs: 5%, both:
11%, unsure: 3%
Popli et al, 37 male Nearly all male ·· ·· Worried that Not explored Adolescence: Cystic fibrosis clinician: Not explored
2009, UK88 patients; patients have fertility their child could 59%; older 40·5%; book,
response rate: issues: 65%; all male have cystic than 20 years: newsletter, or internet:
52% patients have fertility fibrosis: 65% 21% 27%; cystic fibrosis
issues: 11%; uncertain nurse, fertility
how many men specialist, or parents:
affected: 24%; able to 32%
describe exact nature
of fertility problem:
65%; aware of
availability of ART:
50%
Sawyer et al, 264 male Fertility affected: Not explored Not explored Not explored Not explored Mean age Cystic fibrosis clinic: 68%
2009, patients; 99%, nearly always 17·4 years 41%; parents: 20%;
Australia18 median age infertile: 75%, fertility (SD 2·5; range educational material:
30 years (range reduced: 18%, fertility 5–44); first 17%; friends or
17–56); normal: 2%, unsure: heard from patients: 8%; family
response rate: 5%; infertility due to parents: doctor: 3%;
65% sperm transport 16 years (74%), combination of
problem: 78%, first told by sources: 5%
infertility due to family doctor:
sperm production 20 years (67%);
problem: 10%, both: learnt from
2%, unsure: 11% preferred
source: 43%

ART=assisted reproductive technology. SRH=sexual and reproductive health. STI=sexually transmitted infection. “Not explored” refers to a topic that could have been explored, but was not; “not reported” refers
to one that was discussed but the statistic not reported; and middle dots show when the topic was not applicable. *Information about cystic fibrosis, not specific to SRH. Participants particularly wanted
additional information about employment and the future. †Data relates to male patients only. ‡Data relates to female patients only.

Table 3: Cystic fibrosis-related SRH knowledge and education of patients

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 Review

Ideal age to learn Ideal source of initial information about Ideal age for initial discussion Preferred sources of cystic fibrosis- Ideal age for semen
of male infertility male infertility with health-care professional related SRH information analysis
Hames et al, Not explored Not explored Not explored <13 years of age: parents and clinical staff; Not explored
1991, UK78* ≥13 years of age: medical staff alone;
<18 years of age: wanted open discussions
in patient groups and organised social
events
Johannesson ·· ·· 13–14 years Cystic fibrosis doctor; discussion groups ··
et al, 1998, with other patients; specialist
Sweden83† gynaecologist working closely with cystic
fibrosis team (first visit at age 16–17 years)
Sawyer et al, Mean 14·2 years Health-care provider: 30%; parents: 20%; no Not explored Not explored Not explored
1998, USA79‡ (SD 2·6) preference: 50%
Fair, et al, 2000, Not explored Not explored <16 years of age: 56% male Cystic fibrosis doctor: 56% of male Not explored
UK52 patients, 32% female patients; age patients; cystic fibrosis nurse: 70% of
16–19 years: 33% male patients, female patients
46% female patients; age 20–24
years: 11% male patients, 16%
female patients
Rodgers et al, Mean 13 years Cystic fibrosis team: 78%; parents: 80% of those Not explored Discussions to be initiated by the cystic When in a long-term
2000, UK84 (range 8–16) initially told by their parents; all patients fibrosis centre, supported by written relationship or at time
wanted discussions to be initiated by the cystic information, and repeated periodically of initial infertility
fibrosis centre discussions
Thickett et al, Not explored Not explored Not explored Adult cystic fibrosis physician: 71%; adult Not explored
2001, UK85 cystic fibrosis nurse: 24%
Nixon, et al, ·· ·· Mean 13·2 years (SD 1·8) Regarded cystic fibrosis team as important ··
2003, Australia80† source of information: 87% (would ask:
37%; would be interested if it was
discussed: 35%; too embarrassed to
discuss: 19%)
Sawyer et al, Mean 14·4 years Cystic fibrosis clinic: 49%; parents: 29%; written Not explored Cystic fibrosis team; specialist reproductive Age 17–18 years: 73%;
2005, Australia12 (SD 2·8; range material: 5%; combination: 15% experts; written information age 19–20 years: 22%;
6–24) older than 20 years: 5%
Chotirmall et al, Mean age 16·9 Written material: 69% Not explored Not explored Mean age 18·9 years
2009, UK87 (SD 2·2; range (SD 2·5; range 16–25)
12–21)
Gatiss et al, ·· ·· Mean 13·7 years (range 11–18) Not explored ··
2009, UK30†
Korzeniewska ·· ·· 12–14 years Mother: 78%; cystic fibrosis doctor: 75%; ··
et al, 2009, friends: 23%; siblings: 19%; other cystic
Poland5† fibrosis patients: 9%; other health-care
professional: 4·7%; parents: 4·7%; wanted
special educational seminars: 93%
Popli et al, 2009, All men told at Not explored Not explored If patients needed fertility treatment: Not explored
UK88 >20 years of age fertility specialist: 51%; cystic fibrosis
felt that should physician: 21%; family doctor: 13·5%
have been told
younger
Sawyer et al, Mean 14 years Cystic fibrosis clinician: 36%, parents: 34%, Not reported Not reported Younger than age
2009, Australia18 (95% CI 14–15) combination: 21%, did not want to find out 20 years: 81%;
from friends, patients, family doctor, or written unnecessary: 8%
information alone; preferred source younger
than age 16 years: parents > cystic fibrosis
clinician > combination, preferred source older
than age 16 years: cystic fibrosis clinician

SRH=sexual and reproductive health. “Not explored” refers to a topic that could have been explored, but was not; “not reported” refers to one that was discussed but the statistic not reported; and middle dots
show when the topic was not applicable. *Preferred sources of information about cystic fibrosis, not specific to SRH. Information from Cystic Fibrosis Trust thought to be the most valued and popular existing
information source. †Data relates to female participants only. ‡Education preferences of adult male study participants only reported.

Table 4: Patient preferences about cystic fibrosis-related SRH education

suggested that it is usually diagnosed by the patient or enquire about symptoms of candidosis, and provide
their family doctor rather than by the cystic fibrosis team. education, diagnosis, and management as needed.
The frequency of cystic fibrosis clinic visits provides an Only a small proportion of men have the opportunity
opportunity for cystic fibrosis clinicians to regularly to confirm their fertility status at an appropriate time.

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 Review

Infancy Early Late Early Late Young Adulthood

(0−1 years) childhood childhood adolescence adolescence adulthood (25+ yr)
(1−4 years) (5−9 years) (10−14 years) (15−19 years) (20−24 years)

SRH care of patients by primary health-care services

Linkages with Immunisation (eg, HPV) Contraception Pap smears Men’s health services
primary care Candidosis treatment STI prevention
services and treatment

SRH education of parents by the cystic fibrosis service

Male infertility Urinary incontinence Contraception
Genital candidosis STI prevention
Pubertal development Reproductive options
Male infertility
Female fertility

SRH education of patients by the cystic fibrosis service

Direct roles for
Urinary incontinence Male infertility Reproductive options Genetic counselling
the cystic
Female fertility Pre-pregnancy counselling
fibrosis service
Contraception
STI prevention

SRH care delivery by the cystic fibrosis service

Urinary incontinence Pubertal assessment Contraception* Optimise preconception health
Candidosis treatment Semen analysis*

Specialist SRH services (linked to the cystic fibrosis service)

Adolescent medicine Gynaecology Genetic counselling Infertility assessment
Linkages with
Endocrinology Andrology and ART services
tertiary care
services Obstetrics

Figure 2: A model of care for delivery of SRH education and services to patients with cystic fibrosis, and their parents, across the life course
This model shows the typical ages and the broad content domains to address, and emphasises the interdependent roles of the specialist cystic fibrosis service in relation to primary care and specialist
SRH services. ART=assisted reproductive technology. HPV=human papillomavirus. SRH=sexual and reproductive health. STI=sexually transmitted infection. *Services to be universally offered that
might or might not be provided by the cystic fibrosis service itself.

Findings from studies from the USA,79 the UK,84,85 and
Australasia12,18 show that a quarter to a half of participants
underwent semen analysis in adulthood, although most
of those who had not undergone analysis wanted to.
Adult men have identified late adolescence (age
17–20 years) as the most appropriate time for semen
analysis to be offered.12,18,79,84,85
Recommended clinical practice
In this Review, we strongly suggest that present ad-hoc
approaches to SRH within cystic fibrosis care are
inadequate, resulting in large gaps in SRH knowledge
and less than ideal SRH outcomes. Yet the scientific
literature is clear—to maintain physical health and
promote psychological wellbeing, young people with
cystic fibrosis need information about normative sexual
development and age-appropriate preventive health
measures, and cystic fibrosis-specific SRH information.
Consensus exists between patients, parents, and
health-care professionals about the appropriate age
and developmental stage to deliver particular SRH
information. Similar consensus exists about so-called
educational deadlines—ie, the age by which particular
information should be delivered. Specifically, parents
of male patients need to be informed of probable
infertility at around the time of diagnosis, all parents
need to understand the effect of cystic fibrosis on SRH
before their child reaches puberty, and physicians
should have an initial conversation about SRH with
patients in early adolescence. Male patients should be
aware of infertility by 15 years of age, semen analysis
should be offered by 17–20 years of age, and women
considering pregnancy should receive medical,
psychological, and genetic counselling before con-
ception. Men considering fathering a child should also
receive genetic and psychological counselling.
The onus is on the cystic fibrosis physician to
proactively create opportunities within routine cons-
ultations that first help equip parents, and then patients,
to understand and safely manage their SRH. Although

www.thelancet.com/respiratory Vol 3 January 2015 83

 Review
Search strategy and selection criteria
We reviewed the scientific literature using the databases
Medline, Embase, PsycInfo, PubMed, and the Cochrane
Library, and by manually searching references. The MeSH
medical subject headings and search strategy are summarised
in the appendix. We restricted the search to reports published
in English between Jan 1, 1990 and Sept 30, 2013. Reports
relating to physiology, genetics, and reproductive
technologies were further restricted to being published
between Jan 1, 2000 and Sept 30, 2013. Reproductive
decision making of cystic fibrosis carriers was beyond the
scope of this Review.
the maturity and behaviours of individuals naturally
varies, if physicians wait for a specific trigger or direct
request before addressing SRH, information will be
provided too late—if at all. Although an annual cystic
fibrosis review might be appropriate to check that
educational deadlines have been met, the most
appropriate setting for SRH discussions is routine
appointments.
Figure 2 shows a model that describes the SRH education
and care that need to be delivered to both patients and
parents by the cystic fibrosis team. It also describes the
service linkages that are essential for optimum delivery of
SRH care within a cystic fibrosis service. In the first decade
of life, the focus is on parents, starting at around the time
of diagnosis and culminating in the late primary school
years to coincide with the beginning of school-based sex
education (figure 1). The goal of these discussions is to
ensure that parents are sufficiently informed and
empowered to take the lead in addressing cystic fibrosis-
specific SRH topics with their children at home. In the
second decade of life, the focus shifts to patients, who will
now benefit from specific discussion about SRH by health-
care professionals. Opportunities for confidential con-
sultations with adolescents need to be created. Initial
discussions need to be followed by repeated conversations
throughout adolescence and into adulthood, with
increasingly specific information provided by the medical
team; contraception, barrier protection for STI prevention,
urinary incontinence, candidosis, and fertility should be
routinely discussed with all adolescents, and semen
analysis should be offered to male patients from late
adolescence. In adulthood, these discussions need to be
coupled with repeated opportunities to explore the practical
aspects of reproductive decision making, including pre-
conception counselling and early referral for management
of infertility.
With the exception of medicine, undergraduate
training of the disciplines represented within cystic
fibrosis teams does not consistently include SRH. It is
similarly absent from many postgraduate courses,
including medicine. Many health-care professionals
struggle to discuss sensitive topics such as SRH,
84
especially with adolescents who are easily embarrassed.
The model of care described in figure 2 does not
prescribe who is responsible for delivery of SRH care
within the cystic fibrosis team, and individual members
of multidisciplinary teams are expected to contribute to
different aspects of SRH education as appropriate. An
example is the role of physiotherapists in prevention and
treatment of urinary incontinence. However, we argue
that cystic fibrosis physicians need to carry the main
responsibility for routine SRH discussions with parents
and then patients, and for fostering a culture of care that
is inclusive of SRH being a routine focus of discussion
within multidisciplinary cystic fibrosis teams. Education
of cystic fibrosis teams about SRH is likely to promote
this inclusion of SRH within routine CF care.
The model of care also shows the importance of
service linkages and care coordination. Communication
between the cystic fibrosis team and family doctors is
crucial because these doctors routinely provide access-
ible SRH care, including preventive health-care
measures such as immunisations and Pap smears.
Service linkages are equally crucial between cystic
fibrosis centres and specialist SRH providers, inclu-
ding those with experience in adolescent medicine,
gynaecology, andrology, infertility management,
assisted reproductive technologies, genetic couns-
elling, and obstetrics. Fostering of relations between
each cystic fibrosis service and a small number of
specialists will help build the necessary understanding
of cystic fibrosis and promote timely access to
specialist skills.
SRH behaviours emerge across the life course. Young
people with cystic fibrosis now approach the
developmental milestones of adolescence and early
adulthood at a similar time to their healthy peers. Yet,
ultimately, their life chances remain profoundly
affected by their disease course, and their SRH deci-
sions can have a substantial, and often predictable,
effect on their health. As children pass through
adolescence into adulthood, increasing age is accom-
panied by a growing burden of disease. At the same
time, cognitive maturation results in an increased
capacity for patients to appreciate the implications of
cystic fibrosis. In the context of such dynamic changes
to sexual and cognitive maturation, SRH behaviours,
and disease burden, young people and parents need
information and support to safely and successfully
navigate early SRH milestones. To overcome later SRH
hurdles, patients need access to primary care and
specialist services, careful planning, and psychosocial
support. As cystic fibrosis clinicians, we need to take
responsibility for fostering an environment in which
our patients can make safe and informed decisions,
where SRH is routinely discussed with appropriately
trained staff, and where primary and specialist SRH
care is coordinated by clinicians with specialist
knowledge of cystic fibrosis.
www.thelancet.com/respiratory Vol 3 January 2015

Contributors
SMS conceptualised the framework for the Review. KBF led the scientific
literature searches in collaboration with SMS. KBF and SMS equally
interpreted the scientific literature and wrote the Review. SMS led the
development of the model of care.
Declarations of interest
We declare no competing interests.
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