Evidence for sexual transmission of genital herpes in children

Abstract

Genital herpes in a prepubertal child presents a child protection clinician with a difficult problem: how likely is it that transmission occurred as a consequence of sexual abuse? Published guidelines on the management of sexually transmitted infections in children provide varying recommendations and refer to a limited literature.
To review the evidence for the likelihood of sexual transmission in a child with proven genital herpes.
Structured literature search for reports of series of children presenting with genital herpes where an assessment for possible sexual transmission or child sexual abuse had been made.
Five suitable papers were identified. Although just over half of reported cases of genital herpes in children had evidence suggestive of a sexual mode of transmission, the quality of assessment of possible sexual abuse was too weak to enable any reliable estimation of its likelihood. Sexual transmission is reported more commonly in older children (aged > or =5 years), in children presenting with genital lesions alone and where type 2 herpes simplex virus is isolated.
Child protection clinicians should be aware of the weakness of the evidence on the likelihood of sexual transmission of genital herpes in prepubertal children. The US guidance that child sexual abuse is "suspicious" reflects the evidence better than the UK guidance that it is "probable". A larger, more up-to-date, methodologically sound, population based study is required.

Full text

ORIGINAL ARTICLE
Evidence for sexual transmission of genital herpes in children
Richard Reading, Yifan Rannan-Eliya
...................................................................................................................................
See end of article for
authors’ affiliations
........................
Correspondence to:
Dr Richard Reading, School
of Medicine, Health Policy
and Practice, University of
East Anglia, Norwich NR4
7TJ, UK; r.reading@uea.ac.
uk
Accepted22November2006
Published Online First
21 February 2007
........................
Arch Dis Child 2007;92:608–613. doi: 10.1136/adc.2005.086835
Introduction: Genital herpes in a prepubertal child presents a child protection clinician with a difficult
problem: how likely is it that transmission occurred as a consequence of sexual abuse? Published guidelines
on the management of sexually transmitted infections in children provide varying recommendations and refer
to a limited literature.
Objective: To review the evidence for the likelihood of sexual transmission in a child with proven genital
herpes.
Methods: Structured literature search for reports of series of children presenting with genital herpes where an
assessment for possible sexual transmission or child sexual abuse had been made.
Results: Five suitable papers were identified. Although just over half of reported cases of genital herpes in
children had evidence suggestive of a sexual mode of transmission, the quality of assessment of possible
sexual abuse was too weak to enable any reliable estimation of its likelihood. Sexual transmission is reported
more commonly in older children (aged >5 years), in children presenting with genital lesions alone and
where type 2 herpes simplex virus is isolated.
Conclusions: Child protection clinicians should be aware of the weakness of the evidence on the likelihood of
sexual transmission of genital herpes in prepubertal children. The US guidance that child sexual abuse is
‘‘suspicious’’ reflects the evidence better than the UK guidance that it is ‘‘probable’’. A larger, more up-to-
date, methodologically sound, population based study is required.
G
enital herpes in a child not sufficiently mature to engage
in consensual sexual activity, proven with culture of
herpes simplex virus (HSV), raises the question of
whether sexual abuse may have been the mode of transmission.
In most cases some form of multidisciplinary child protection
investigation will be required. An essential medical contribu-
tion is to advise on the likelihood that the infection is sexually
transmitted or whether transmission is possible by other
means.
There is little evidence on which to base such advice. Culture
and typing of the virus is important as rarely other genital
lesions can be mistaken for herpes simplex. HSV type 2 in
adults is strongly suggestive of sexual transmission, but we do
not know whether this also holds true in children, and in the
UK the majority of genital herpes infections are type 1 anyway.
1
Published guidelines on the management of sexually
transmitted infections in children in the United Kingdom
stress sexual abuse is a ‘‘probable’’ mode of transmission for
genital herpes,
2
that is, an intermediate risk for sexual abuse
between ‘‘possible’’ and ‘‘highly probable’’. However, this
recommendation is derived from an earlier publication from
the Royal College of Physicians in which there is inconsistency
between the summary conclusion that sexual transmission is
‘‘probable’’ and the text which describes uncertainty in
knowledge about modes of transmission.
3
In the US, guidance
from the American Academy of Pediatrics
45
and the Centers for
Disease Control and Prevention
6
both state that sexual
transmission is ‘‘suspicious’’ and describe other possible modes.
The primary evidence is rarely cited and where it is, seems to
depend largely on a single paper from 1968 reporting six cases.
7
We have searched for and reviewed the evidence for the
likelihood that transmission has occurred through sexual abuse
for a child with proven genital herpes.
METHODS
Studies were identified in early 2004 and updated in November
2005. Medline (1966–2005), CINAHL (1982–2005) and Embase
(1980–2005) were the primary databases searched. Search
terms included combinations of herpes simplex, genital, child,
sex*, transmi*, abuse, incest, and rape. Using the search terms
(herpes simplex), child*, and genital, yielded 265 records. Using
(sex* transmi*), child*, and herpes yielded 210 records. Using
(child abuse) and (genital herpes) yielded 24 records. Using
genital and herpes and (child* or sex*) and (abuse or incest or
rape) yielded 97 records. Using herpes and child* and genital
yielded 380 records. In order to identify possible studies missed
by our primary searches, we searched the social science
database ASSIA (1975–2005) and the ISI Web of Science
database using combinations of the above terms. We examined
additional papers referenced by articles identified by the search
strategy. No further relevant papers or studies were identified.
Papers were deemed suitable for review if they described
children under 18 years of age presenting with genital herpes
simplex where the population included prepubertal children
and in whom an assessment for either sexual abuse or sexual
transmission had taken place. We included cohort studies, case-
control studies, cross-sectional incidence studies and case
series. Data on cases could be collected prospectively or
retrospectively, as long as there was an attempt at complete
ascertainment from a population over a time period, and a
description of the population was given. In addition, we
reviewed papers describing series of children presenting with
suspected child sexual abuse in whom genital herpes infection
had been considered either clinically or by viral culture. We
excluded single case reports and reports of multiple cases in
which there was no evidence that all cases presenting over a
period of time had been ascertained.
We assessed the quality of included papers in terms of the
thoroughnessandreliability of the diagnosisof HSV and in terms of
the standards for evaluating the mode of transmission. Indicators
of high quality HSV diagnosis included viral culture and typing on
all cases. Less good, but still adequate was paired type specific sera.
Poor quality was indicated by cytology only or no confirmatory
investigation and less than complete investigation in all potential
608
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Table 1 Evidence of genital herpes among series of children assessed for child sexual abuse
Paper Study group Setting Study type Ages of children Mode of HSV identification Mode of CSA* ascertainment No. identified with HSV and type
Rimsza and 311 children Paediatric department Retrospective 0–18 years Not clear, possibly only Clinical history, genital 2 with ‘‘signs of HSV’’,
Niggemann, 1982
8
assessed for CSA and CSA referral chart review clinical examination. No exam and social enquiry no details of HSV
over a 3.5 year centre, Phoenix, of cases identified details of virological taken, but all children culture or typing
period AZ, USA prospectively investigations given were assumed to have
been sexually abused
Grant, 1984
9
157 children Child protection Prospective 0–16 years Viral culture not carried Clinical history, genital 1 child with HSV (not
presenting with centre, Winnipeg, observational out routinely, only if exam and social enquiry. typed) and no age stated
possible CSA to Canada study clinically indicated Good quality but showed no evidence of
a child protection ascertainment of CSA CSA
centre over
18 months
De Jong, 1986
10
532 children Paediatric Prospective ,14 years Viral culture if clinically Clinical history, genital 1 child with HSV (type
assessed for CSA department and CSA observational indicated, and only carried exam and social enquiry 2), age of child not stated
over a 4 year period referral centre, study out on 3 cases taken, but all children
Philadelphia, PA, were assumed to have
USA been sexually abused
De Villiers et al, 227 children Child abuse clinic, Prospective All ages (124/227 All children had viral Clinical history and No cases of HSV isolated
1992
11
attending a child Johannesburg, South observational ,10 years) culture. This is the only social enquiry
abuse clinic over 1 Africa study study in this group where
year, 96.5% with all cases had a viral culture
alleged CSA
Gardner, 1992
12
209 sexually abused Child sexual abuse Case control study Ages 2–14 years Unclear. Extensive Clinical history, genital 1 girl aged over 10 years
girls attending a unit in Perth, Australia with prospective (160/209 (10 bacteriological work-up but exam and social enquiry from sexually abused
child sexual abuse ascertainment of years) no details given on criteria group (type not reported)
unit over 2 years and all cases or methods of viral
108 non-abused presenting to unit identification
controls having
elective operations
Ingram et al, 1992
13
1538 children Child sexual abuse Prospective Ages 1–12 years Viral culture of ‘‘all Clinical history, genital 2 girls. One aged 4 years
attending a child assessment centre, observational (,90% (10 suspicious papules or exam and social enquiry (HSV type 2) gave no
sexual abuse department of study years) ulcers’’. Number of history of CSA, one aged .
assessment centre paediatrics, Raleigh, children who had viral 7 years (HSV type 2) gave
over 10.5 years NC, USA culture is not reported history of CSA
Yordan and 288 girls attending Regional paediatric Prospective Up to 18 years Viral culture of ‘‘any History from referrer and 1 girl aged 17 years (type
Yordan, 1992
14
paediatric sexual sexual abuse clinic, observational (184/288 (10 genital ulcer’’. Number of child, genital exam and not specified) with a
abuse clinic over 3 Hartford, CT, USA study years) children with viral culture social enquiry 4 year history of
years 5 months is not reported but all had intrafamilial sexual abuse
an extensive
bacteriological work-up
Siegel et al, 1995
15
855 children Child abuse centre, Prospective 3 weeks to 18 Clinical examination only. Clinical history, genital No cases of HSV
assessed for CSA paediatric department, observational years (no. (10 It is not clear whether viral exam and social enquiry suspected
over a 1 year period Cincinnati, OH, USA study years not clear culture would have been
(704 girls, 151 boys) but mean age = 7 carried out but no cases
years) had clinical signs
*CSA, child sexual abuse; social enquiry indicates some form of multidisciplinary child protection investigation.
Genital herpes in children 609
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cases.
1
Quality indicators for the assessment of mode of
transmission were less easy to define. There is no gold standard
for identifying child sexual abuse. We considered that reason-
able standards should include a sensitive history, clinical
genital examination, some form of social care assessment
which may include information gathering and interviewing
child and parent, and a multidisciplinary review of all this
evidence. We assessed whether three components of this
process (namely history, examination and social enquiry) were
carried out and on what proportion of eligible cases. However, it
was not possible to assess the depth, thoroughness or
consistency of this process from the descriptions given in
papers.
One author carried out the searches for abstracts, reviewed
the abstracts and identified potential papers (YRE for the initial
search, RR for the updated search). Both authors read the
papers and selected papers for inclusion and exclusion by
consensus. Disagreement was resolved by discussion.
Assessment of quality was carried out initially by RR and
agreed by discussion. Pre-agreed forms to score abstracts for
eligibility and papers for quality were not used in view of the
variable (and generally poor) quality of the evidence.
RESULTS
Of the abstracts retrieved, 13 papers were suitable to be
included in the review. Of these, eight papers included series of
children presenting consecutively for child protection assess-
ments.
8–15
One of these included comparative data from non-
abused controls.
12
The other five were series of children with
genital herpes infections presenting consecutively either to
paediatric departments in hospitals or sexually transmitted
infection clinics.
7 16–19
Series of children presenting for child protection
assessments
The results of the eight papers are shown in table 1. The overall
results suggest genital herpes is very uncommon in children
being evaluated for sexual abuse (8/4117 children). In two of
these eight cases no evidence for sexual abuse was found. The
other six cases were from clinic populations in whom it was
either explicitly stated or assumed that all children had been
sexually abused. Hence, these data do not help address the
likelihood of sexual transmission in cases of genital herpes
because the numerator is heavily biased towards children who
have been sexually abused.
Only the study by De Villiers et al routinely cultured samples
from all cases for herpes virus. As the others cultured only
when clinically indicated, and in some cases not at all, cases
may have been missed. Most of the studies included adolescent
children who may have been consensually sexually active as
well as being abused. The clinical details and ages of the
individual cases were often not described. Thus, although the
prevalence of genital herpes in children who have been sexually
abused is low, this may be over- or under-estimated by the data
presented here.
Our search strategy only identified papers where herpes had
either been looked for or found. We are aware of other studies
where sexually transmitted infections were sought among
children being assessed for child sexual abuse but where no
mention of herpes was made.
20–22
Series of children presenting with genital herpes
We identified five studies of series of children presenting
consecutively over a defined period with genital herpes (or who
were part of larger clinical populations which would be reliably
expected to include all children with genital herpes) in whom
enquiries had been made about possible child sexual abuse
(table 2). AS two of these studies were from sexually
transmitted infection clinics in India covering highly deprived
populations including large groups of young adolescent boys
involved in prostitution, it may not be appropriate to generalise
the results to different populations. The other series are all
small and old with poor quality diagnosis of sexual abuse. We
identified one further paper from Chile which appeared to
report on around 90 cases of children with genital herpes.
However, as there was no information on mode of transmission
and our attempts at contacting the authors were unsuccessful,
this paper has been excluded from the review.
23
Among the studies included, details of the type of history, the
quality of physical examination, standards for assessing
physical findings, and the extent and nature of further social
investigations are scanty. It is clear that these were not
investigated systematically in any of the studies. There is no
information on which types of sexual contact (ie, genital–
genital, oral–genital, hand–genital or anal contact) were
considered. The description of the physical findings which
were taken to indicate abuse would not be seen as adequate or
appropriate now (eg, ‘‘hymen was noted to be perforated’’
7
).
The paper by Kaplan et al
16
has the most thorough and
consistent reported assessments. We have provided a descrip-
tion of each study in table 3.
The reported modes of transmission from these five studies is
described in the right hand columns of table 2. Because of the
heterogeneity of populations, the age of the studies and the
generally poor quality of methods, we have not included a
summary meta-analysis. Extreme caution should be used in
interpreting these results, but with this caveat, sexual
transmission has been reported more commonly when HSV
type 2 has been isolated, in older age groups and when only
genital lesions occur. Where both oral and genital lesions occur,
especially if in a younger child, the suggestion is that either
autoinoculation occurs in the context of a primary infection, or
that intimate child care such as nappy changing by an infected
adult occurs.
DISCUSSION
This review confirms the association of genital herpes in
children with sexual contact. While a diagnosis of sexual abuse
cannot be made on one finding alone, any case of genital herpes
should usually result in a multidisciplinary child protection
investigation. As part of this process, the child protection
clinician will inevitably be asked about the likelihood of sexual
transmission. In adults, genital herpes is thought to be
transmitted sexually in almost all cases, either by an oro-
genital or a genito-genital route.
1
However, in adults genital
herpes is common, sexual activity nearly ubiquitous, and
difficult questions about how the infection was contracted
can legitimately be answered by the fact that herpes can be
clinically asymptomatic in either partner for long periods. In
contrast, among children genital herpes is rare, there may be
frequent non-abusive contact with children’s genitalia by
adults during child care, and there is the theoretical possibility
of autoinoculation from an oral lesion during a primary attack.
Furthermore, clinically apparent genital herpes in a child may
be the result of a primary attack years previously which may or
may not have been sexually transmitted.
In this review, we have shown two main findings. First,
genital herpes is rarely reported among children being assessed
for possible, probable or known sexual abuse. However, few
studies universally tested for herpes simplex, so we have no
way of knowing how common asymptomatic infection may be.
In a review of the transmission of infection after sexual abuse,
Hammerschlag called for a large study using sensitive methods
of virus identification and non-abused controls.
24
610 Reading, Rannan-Eliya
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Table 2 Studies evaluating sexual transmission in series of children identified with genital herpes simplex
Paper Study group Setting Study type
Ages of
children
Mode of HSV
identification
Mode of CSA
ascertainment
No. of
cases
with
HSV*
HSV type* Age range*
Co-occurrence of
other herpetic
lesions*
HSV1 HSV2
,5
years
5–9
years
>10
years
Genital
lesions
alone
Oral and
genital
lesions
Nahmias et al, All children presenting Hospital Retrospective 3–12 years Cytology, viral Clinical history and 6 (4) 2 (0) 4 (4) 1 (0) 4 (3) 1 (1) 3 (3) 3 (1)
1968
7
over a 3 year period paediatric cross-sectional culture and viral clinical examination.
with genital herpes – department, study typing Poor quality
6 cases in total Atlanta, GA assessment of CSA
USA
Kaplan et al, All children with culture Children’s Retrospective 0–12 years Viral culture Clinical history, 6 (4) 5 (3) 1 (1) 2 (0) 3 (3) 1 (1) 4 (4) 2 (0)
1984
16
proven genital herpes hospital cross-sectional and typing clinical examination,
over a 9 year period – 6 Philadelphia, study and social enquiry
cases in total. Case PA, USA in some cases only.
ascertainment from lab Exclusion of CSA by
reports only – possible clinical history alone
cases without viral in other cases
culture may have been
missed
Taieb et al, All 50 children presenting Paediatric Prospective 11 months Viral culture and Clinical history alone. 3 (1) 2 (1) 1 (0) 2 (0) 0 1 (1) 1 (1) 2 (0)
1987
17
with a primary herpes dermatology cohort study to 11 years viral typing Poor quality assessment
infection over a 10 year department, of CSA. Main focus of
period Bordeaux, paper was epidemiology
France and virology of primary
herpes infections, brief
details only for cases
with genital lesions
Pandhi et al, 58 children attending a STD clinic, Retrospective 0–14 years Cytology (Tzanck Clinical history. Not typed 0 0 4 (2) Not reported
1995
18
sexually transmitted New Delhi, cross-sectional smear), no Assessment of sexual
infection clinic over India study virology. transmission of low
18 months. Highly Cytology has reliability. Although 2/4
disadvantaged low sensitivity cases with HSV gave no
population, many for identifying history of sexual contact,
involved in herpes the authors imply that
prostitution sexual contact was likely
Pandhi et al, 127 children attending STD clinic, Retrospective 0–14 years Cytology (Tzanck Clinical history. Not typed 2 (2) 3 (3) 6 (6) Not reported
2003.
19
Note, a sexually transmitted New Delhi, cross-sectional smear), no Assessment of sexual
different infection clinic over India study virology. transmission of low
authors, 6 years. Highly Cytology has reliability
setting and disadvantaged population, low sensitivity
study group many living in poorly for identifying
to paper managed children’s homes herpes
described with high prevalence of
above homosexual abuse
*Number thought due to child sexual abuse in brackets.
CSA, child sexual abuse.
Genital herpes in children 611
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Second, among groups of children identified with genital
herpes, it is suggested that sexual transmission occurs in just
over half the cases (table 2). However, this evidence is weak.
The series are all small. The reliability of ascertainment of
sexual abuse was variable and would not be accepted by current
standards. In some studies only clinical history was taken and
no reference was made to multidisciplinary social enquiries,
while in others there seems an assumption that sexual
transmission occurred unless there was convincing evidence
otherwise. It is possible that there has been publication bias in
favour of studies reporting an association between childhood
genital herpes and sexual abuse. Therefore, the overall figure
for the likelihood of sexual transmission could be either over-
or underestimated.
The poor quality of this evidence means it is not possible to
estimate the likelihood of sexual transmission in children
presenting with genital herpes. This is a much weaker evidence
base than that available for gonorrhoea for example, where
larger series and a better understanding of the natural history
of the disease mean we can be more certain it is sexually
transmitted. The US guidance in this respect, reflects the
evidence more reliably, where gonorrhoea is described as
‘‘highly suspicious’’ of sexual abuse, while genital herpes is
‘‘suspicious’’.
4–6
We propose that the current UK recommenda-
tion should be changed to ‘‘possible abuse’’.
When genital herpes occurs in children, we support the view
that a multi-agency enquiry is required to exclude sexual abuse
in the absence of another credible explanation. Both clinically
and for research purposes, herpes should be included in any
situation where a sexually transmitted infection screen is
carried out in children. Although this may be considered over-
investigation clinically, a carefully conducted study of genital
examination and genital viral culture in any child presenting
with a primary herpes infection elsewhere would help answer
many questions about the frequency of autoinoculation,
asymptomatic infection and incidental isolation of the virus.
A larger, methodologically robust and more up-to-date study of
children presenting with genital herpes is required in order to
be more certain of the implications in a child who is not mature
enough to engage in consensual sexual relations. In the
meantime this review provides doctors with the evidence on
which to base their judgment.
Table 3 Details of studies reporting investigation of cause in series of children with genital herpes
Paper Review
Nahmias et al,1968
7
This is the most quoted study; 6 children with genital herpes, with relatively poor reference standards for the identification of abuse, formed
the retrospective cohort. Four had type 2 infections, one based on serology results. Of these, 1 had been sexually exposed, 1 molested, and 2
had a perforated hymen (1 also isolated herpes from the mouth). One with type 1 herpes had gingivostomatitis and genital lesions, with no
history of venereal contact, and an intact hymen. A 3 year old boy with type 1 genital infection but no concurrent oral lesions, had had
gingivostomatitis previously and had herpes virus cultured from the mouth. It is unclear whether a history of abuse was considered. In view of
the age of the study it is unclear how well evidence of sexual abuse was collected.
Kaplan et al, 1984
16
Records of children with culture-positive genital herpes (under 13 years, excluding neonates) were reviewed to determine how acquisition
was documented and whether sexual abuse had been investigated. Four out of 6 children had evidence of abuse (three on clinical history,
one after social enquiry), two had infection suggestive of autoinoculation (sexual abuse excluded on clinical history in these two). The study
cohort is small and fairly old, but reference standards for herpes virus identification were good. Child protection assessments were variable:
in some cases detailed multidisciplinary social enquiries were carried out, in other cases only clinical history and examination were
undertaken. Nevertheless, evidence was presented to show that the possibility of sexual transmission had been considered by clinicians in
each case and some justification was provided for the decisions on how extensively to pursue this.
Taieb et al, 1987
17
50 children with culture-positive primary herpes infections were studied. Of these, 3 had genital herpes. One 44 month old girl had type 1
herpes isolated from genital, orolabial and cutaneous lesions, but the source of infection was unknown. A 25 month old had type 2 herpes
isolated from orolabial and genital lesions. It was suggested the probable source of infection was from a sibling with gingivostomatitis. The
3rd case was that of an 11 year old girl with type 1 genital herpes. Although the authors suspected venereal transmission, genital
examination was not performed and the history was inconclusive. Overall, the reference standards were poor and evidence for sexual abuse
was not consistently investigated.
Pandhi et al,1995
18
58 children under 14 years age reporting to the dermatology and sexually transmitted diseases department of a Delhi hospital over a 20
month period formed the retrospective cohort. Reference standards for documenting infection were moderate (Tzanck smear identifies
multinuclear giant cells, but this does not have a high sensitivity). Reference standards for the possibility of sexual abuse were moderate, and
depended on clinical history alone. 4 boys, all aged 11–14 years, had genital herpes, 2/2 gave a history of sexual contact. All these boys
were sexually mature and from an extremely disadvantaged background with a high prevalence of prostitution involving young boys. This
combination of factors suggests the findings may not be transferable to children typically seen in developed nations such as the UK and could
only be transferred to the small group of children involved in prostitution who, by definition, would be sexually abused.
Pandhi et al,2003
19
127 children (under 14 years) who attended the sexually transmitted infection (STI) clinic of a tertiary hospital in India over 6 years, formed
the retrospective cohort. Reference standards for documenting infection were moderate (Tzanck smear identifies multinuclear giant cells, but
this does not have a high sensitivity). Reference standards for the possibility of sexual abuse were moderate, based on clinical assessment
alone. 11 had genital herpes with documented sexual transmission (7 girls after abuse, 2 boys after sodomy, 2 boys after voluntary
heterosexual contact). The cohort was highly disadvantaged; over 60% were illiterate, over 70% were from low socioeconomic backgrounds
and 17% were from remand homes. Syphilis was the most common infection, seen in 25%, followed by 14% with genital warts. There was a
high incidence (70%) of homosexual abuse in the boys presenting with STIs. As with the previous study from India, this combination of factors
suggests these findings may not be transferable to children typically seen in developed nations such as the UK. There is no overlap with the
previous study (different authors, clinic and population) despite similarities of author names, city and layout of report.
What is already known about this topic
N
Genital herpes in a child raises the question of sexual
abuse.
N
The likelihood of sexual transmission in children is
unclear.
N
Published guidelines are inconsistent.
What this study adds
N
Available evidence is too weak to allow an estimation of
the likelihood of sexual transmission.
N
Sexual transmission has been reported more commonly
in children over 5 years of age where genital lesions
alone occur and where type 2 herpes simplex virus is
isolated.
612 Reading, Rannan-Eliya
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ACKNOWLEDGEMENTS
We are grateful to Dr Jose´ Cristo´bal Paniagua Marrero for translating
the Chilean article. We are indebted to Dr Alison Kemp who has
provided many helpful comments and advice on earlier drafts of this
paper.
Authors’ affiliations
.......................
Richard Reading, School of Medicine, Health Policy and Practice,
University of East Anglia, Norwich, UK
Yifan Rannan-Eliya, University Hospital of Wales, Cardiff, UK
Competing interests: None.
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