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676740

research-article2016
URO0010.1177/2051415816676740Journal of Clinical UrologyAyres et al.

NCRAS 2017 Supplement

Journal of Clinical Urology

Trends in incidence, mortality and


2017, Vol. 10(1S) 19­–23
© British Association of
Urological Surgeons 2017
treatment of penile cancer before and Reprints and permissions:
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after centralisation of penile cancer DOI: 10.1177/2051415816676740


https://doi.org/10.1177/2051415816676740
journals.sagepub.com/home/uro

services in England (1990–2009)

BE Ayres1, M Iles2, L Hounsome2, S McPhail2, R Persad3,


J Verne2 and NA Watkin1 on behalf of the National Cancer
Intelligence Network

Abstract
Objective: Penile cancer services were centralised in England in 2002. Has this had an impact on treatments for penile
cancer and survival?
Patients and methods: All cases of penile cancer from 1990 to 2009 were identified from national cancer registry
data. Mortality data were obtained from the Office for National Statistics and survival data were extracted from a
national population-based database, the Cancer Information System. Socioeconomic deprivation was calculated using a
national income deprivation score and surgical treatments were obtained from Hospital Episode Statistics (HES) data.
Results: The number of penile cancer cases recorded rose from 300 to 400 per year during the early period of
centralisation. There was a significant rise in the age-standardised incidence of penile cancer from 1.2 per 100,000 to 1.4
per 100,000 during this period. Mortality remained stable at 0.3 per 100,000. One-year and five-year relative survival
remained stable after centralisation at 88% and 72% respectively. The incidence and mortality of penile cancer was
significantly higher in the most deprived quintile of the population. Following centralisation, the number of total penile
amputations was low at 11% but only 39% of men were recorded as having lymph node surgery, although this may reflect
poor compliance with coding rather than true practice.
Conclusions: The incidence of penile cancer in England is rising, but mortality and survival remains stable. Incidence and
mortality is higher in more deprived areas, and greater public awareness of this disease and its risk factors are needed.
By 2009, rates of penile amputation were low but potentially the proportion of lymph-node surgery remained low. This
may change with the uptake of inguinal sentinel lymph-node sampling.

Keywords
Centralisation, deprivation, epidemiology, incidence, mortality, penile cancer, penile cancer surgery, survival

Date received: 8 January 2016; accepted: 4 September 2016

Introduction
Penile cancer is rare, with an incidence <1 per 100,000 in 1Department of Urology, St George’s Hospital, UK
Europe and North America.1 Centralisation was recom- 2National Cancer Intelligence Network, Public Health England, UK
mended in England in 2002 by the National Institute for 3Bristol Urological Institute, UK

Clinical Excellence.2 Each penile cancer supranetwork


Corresponding author:
should have a referral population of at least 4 million with Benjamin Ayres, Department of Urology, St George’s Hospital,
a minimum of 25 new cases of penile cancer managed Blackshaw Road, Tooting, London SW170QT, UK.
each year. Centralisation has resulted in greater use of Email: beayres@hotmail.com
20 Journal of Clinical Urology 10(1S)

penile-preserving surgery with reconstruction, attempting


to preserve penile form and function as much as possible.3
In addition, inguinal sentinel lymph-node sampling has
been introduced,4,5 after pioneering work from Amsterdam.6
This technique significantly reduces the morbidity of
inguinal node surgery whilst providing accurate staging
information. The aim of this study was to use routine data
sources to assess epidemiological and operative trends
during the early years of penile cancer centralisation in
England.

Patients and methods


All cases of penile cancer (International Classification of
Diseases, tenth revision (ICD)-10 C60) and penile intraep-
Figure 1.  Age-standardised incidence and mortality rates
ithelial neoplasia (PeIN) (ICD-10 D074) diagnosed in of penile cancer and penile intraepithelial neoplasia (PeIN) in
England between 1990 and 2009 were extracted from the England, 1990–2009.
National Cancer Data Repository (NCDR).
Survival data were extracted from the Cancer
Information System (CIS) 1990–2009, an online data sys- recorded as it does not have a specific OPCS code. These
tem now superseded by CancerData. The survival reported limitations must be carefully considered when interpreting
here is all-cause relative survival. This method accounts the results below, and in particular make it difficult to draw
for age, gender and socioeconomic background and pre- any strong conclusions from the treatment data due to lack of
sents survival as a percentage of the expected survival detailed codes for the procedures performed. A central audit
rates for that cohort (i.e. a relative survival of 50% is dou- repository for penile cancer, as currently exists for other uro-
ble the background mortality rate). logical tumour types/procedures but not for penile cancer,
Disease-specific mortality was obtained from the would potentially provide more robust data and allow
Office for National Statistics (ONS) for 1995–2009, count- stronger conclusions.
ing all cases for which penile cancer was recorded as the
underlying cause of death. Penile cancer treatments were Results
identified from Hospital Episode Statistics (HES) data from
2005 to 2009, using the Office of Population Censuses and Incidence
Surveys (OPCS) codes listed below. Total amputation of There has been an increase in the incidence of penile can-
penis (OPCS code N261) is recorded. Unfortunately, penile- cer in England since centralisation of penile cancer man-
preserving surgery was not accurately coded as it could be agement to supranetwork centres (Figure 1). Prior to the
coded as partial amputation (OPCS N262, N268–N269) year 2000 the number of penile cancer cases recorded per
or excision of lesion of penis (OPCS N271–N273, year in England was 300. This rose to around 400 in 2009.
N278–N279). Lymph node surgery was coded as either There was a significant increase in the age-standardised
block dissection of lymph nodes (T851–T859) or biopsy or incidence rate of penile cancer when comparing the years
excision of lymph nodes (T871–T879). Unfortunately, cod- 2001–2003 with 2004–2006, 2002–2004 with 2005–2007
ing for whether procedures were inguinal (Z616) or pelvic and 2003–2005 with 2006–2008 (p < 0.05), rising from 1.2
(O141) was extremely poor. Data on radiotherapy and cases per 100,000 to 1.4 per 100,000. This rise mainly
chemotherapy were not available for this time period. occurred in the 60- to 69-year-old age group. There has
Socioeconomic deprivation was defined using the also been a significant increase in the incidence of PeIN
income deprivation score of the Department of Communities over these non-overlapping three-year periods (p < 0.05)
and Local Government Indices of Deprivation.7 Rates rising from 0.3 per 100,000 to 0.5 per 100,000. This rise
were age-standardised using the 1976 European standard has been seen across all age groups. The incidence of
population. penile cancer is significantly higher in the most deprived
This study was limited by the limitations of the databases quintile of population compared to the least deprived (p <
used. All data collection was prospective, but our data extrac- 0.05) (Figure 2).
tion was retrospective. CIS survival data do not record the
cause of death. ONS mortality data are complete, including
Mortality and survival
the cause of death, but are anonymous. Recording of staging
and treatment data in NCDR and CIS is poor. Treatment data Age-standardised mortality rates have remained fairly
from HES are dependent on the accuracy of hospital coding, constant since centralisation at around 0.3 per 100,000
and unfortunately penile-preserving surgery is not accurately (Figure 1). Mortality rates for the most deprived quintile of
Ayres et al. 21

Table 1.  Number of total amputations for penile cancer


recorded in England per year, 2005–2009.

Year Number

2005 41

2006 55

2007 40

2008 34

2009 45

Total 215

Figure 2.  Age-standardised incidence and mortality rates of


penile cancer in England by deprivation quintile, 2003–2007.

Figure 4.  Percentage of patients having total amputation for


penile cancer in England, per deprivation quintile, 2005–2009.
Overall total amputation rate on the whole cohort was 11%.

Men in the most deprived quintile had a significantly


Figure 3.  Relative survival rates for penile cancer in England. higher total amputation rate, 13.9% (p < 0.05), compared to
One-year relative survival, 1990–2010. Five-year relative
the other quintiles (Figure 4). There was no significant differ-
survival, 1990–2006.
ence between deprivation quintiles for partial amputation.
According to HES data, lymph-node surgery, either
population are significantly higher than the least deprived biopsy/excision or block dissection, was performed in 794
(Figure 2). One- and five-year relative survival has men (39%) overall. This proportion was higher in men
remained fairly stable pre- and post-centralisation, having total amputation (65%) and partial amputation
although we only have five-year survival data for the very (48%). Rates of lymph-node surgery did not increase dur-
beginning of the centralisation period (Figure 3). One-year ing 2005–2009 and the first and only time that lymph-node
relative survival was 86% from 1990 to 1992 and 88% biopsy/excision was used more frequently than block dis-
from 2005 to 2007. Five-year relative survival was 70% section was in 2009 (Figure 5). Unfortunately, coding for
from 1990 to 1992 and 72% from 2001 to 2003. whether lymph-node procedures were inguinal (Z616) or
pelvic (O141) was extremely poor and perhaps reflects
poor compliance with coding in general for lymph-node
Penile and nodal surgery surgery.
Between 2005 and 2009, 2030 penile cancers were regis-
tered and 1760 (87%) had surgery. There is no OPCS code
Discussion
for glansectomy and some cases were coded as other oper-
ations of penis. Total amputation was performed in 215 The incidence of penile cancer in England has been rising.
patients, 11% of the total. A total of 836 men (41%) had a This has been observed in other studies8,9 and in other
partial amputation and 669 (33%) had excision of penile countries, such as Australia9 and Denmark.10 However,
lesion. The number of total amputations was similar year this is not the case in all developed countries, with the inci-
on year from 2005 to 2009 (Table 1). dence being fairly stable over the same time period in the
22 Journal of Clinical Urology 10(1S)

disease is more advanced at presentation too, although as


previously stated staging data do not reliably exist in
national databases to assess this further.
The data on penile surgery are limited since there is no
code for glansectomy. The number of radical penectomies
appears to have remained stable from 2005 to 2009 at
about 40–50 cases per year, 11% of the total number of
recorded penile cancer operations. It is difficult to draw
any other conclusions on primary penile cancer treatments
received and proportion of penile-preserving surgery due
to the lack of specific codes. Only 39% of patients are
recorded as having lymph-node surgery, with a similar
proportion having the surgery each year from 2005 to
Figure 5.  Number of cases of lymph-node biopsy/excision vs 2009. The proportion of men having lymph-node surgery
block dissection of lymph nodes in England, 2005–2009. following radical penectomy was higher at 65%. This sug-
gests case selection, with men with more advanced disease
United States.9 There are several possible causes behind having lymph-node surgery. Inguinal sentinel lymph-node
this rise in incidence in England. Infection with human sampling was introduced as a technique for nodal staging
papilloma virus (HPV) is a known risk factor for penile in penile cancer following centralisation of penile cancer
cancer and it is found in about 40%–45% of penile cancers services in England.4,5 It is associated with a significantly
and 80%–100% of cases of PeIN.11 Rising rates of HPV lower morbidity than full groin dissection at 7.6%.5 This
infection12 may therefore partly explain the rise in inci- may explain the rise in lymph-node biopsy/excision in
dence of penile cancer and PeIN. Another factor is that 2009, when the technique was starting to become available
infant circumcision reduces the risk of developing penile in penile cancer centres. However, again it is difficult to
cancer and rates of infant circumcision in England have draw strict conclusions from this as the low number of pro-
been falling.13,14 An additional reason for the large rise in cedures may be due to poor compliance with coding rather
cases of PeIN is better detection and awareness of the con- than observation being the preferred approach to impalpa-
dition; centralisation of penile cancer services has had an ble inguinal nodes, especially since coding for whether
impact on this and may also have improved reporting of lymph-node procedures were inguinal or pelvic was
penile cancer cases to national databases. extremely poor. A central audit repository for penile can-
Despite the rise in penile cancer incidence throughout the cer, as currently exists for other urological tumour types/
2000s, the mortality and survival rates remained stable. procedures but not for penile cancer, would potentially
Whilst it is disappointing that centralisation has not had an provide more robust data and allow stronger conclusions
impact on survival, one-year survival is unlikely to be sig- with respect to current treatment strategies and allow
nificantly changed as this represents advanced disease at bench-marking which is not possible with HES data due to
presentation and there have been few advances in the effec- the lack of codes for penile-preserving surgery.
tiveness of chemotherapy in penile cancer. The five-year sur-
vival figures in this study represent only the very early period Conclusion
of centralisation. Evidence has been presented that shows at
least a 7% improvement in five-year survival in penile can- During the early years of centralisation of penile cancer ser-
cer in one region of England since centralisation.15 vices the incidence of penile cancer rose and mortality and
This study highlights the impact of deprivation on the survival remained static. The incidence, mortality and rate
incidence, mortality and resulting surgical options for of total penile amputation was higher in more deprived
penile cancer. In England, the healthcare system is free and areas, and more work needs to be done in promoting aware-
easy to access, and therefore these differences are unlikely ness of this disease and its associated risk factors. Total
to be due to inequalities in healthcare access. However, penile amputation rates were low at 11%. However, the rate
they may reflect differences in public awareness of the of lymph-node surgery was potentially low at 39%, although
condition, embarrassment and willingness to seek medical this may reflect problems with coding. If a true figure, the
advice early. It may also be that risk factors for penile can- rate should rise following the introduction of inguinal senti-
cer are more prevalent in areas of higher deprivation. nel lymph-node sampling in several penile cancer centres.
Smoking is a risk factor and is significantly higher in lower
socioeconomic groups.16 High-risk HPV has a higher rate Conflicting interests
in women from deprived areas.17 The higher mortality rate The JCU editorial board has commissioned this review for the
and higher rate of total penile amputation amongst the JCU NCRAS supplement. The Authors declare that there is no
most deprived quintile of the population suggest that the conflict of interest.
Ayres et al. 23

Funding the long-term outcome of 500 inguinal basins assessed at a


single institution. Eur Urol 2013; 63: 657–663.
This research received no specific grant from any funding agency
6. Horenblas S, Jansen L, Meinhardt W, et al. Detection of
in the public, commercial, or not-for-profit sectors.
occult metastasis in squamous cell carcinoma of the penis
using a dynamic sentinel node procedure. J Urol 2000; 163:
Ethical approval 100–104.
Not applicable. 7. Department of Communities and Local Government.
English indices of deprivation, https://www.gov.uk/gov-
Informed consent ernment/statistics/english-indices-of-deprivation-2015
(accessed 16 December 2015).
Not applicable. 8. Arya M, Li R, Pegler K, et al. Long-term trends in inci-
dence, survival and mortality of primary penile cancer in
Guarantor England. Cancer Causes Control 2013; 24: 2169–2176.
BA. 9. Sewell J, Ranasinghe W, De Silva D, et al. Trends in penile
cancer: A comparative study between Australia, England
and Wales, and the US. Springerplus 2015; 4: 420.
Contributorship
10. Baldur-Felskov B, Hannibal CG, Munk C, et al. Increased
BEA, MI, RP and NAW researched literature and conceived the incidence of penile cancer and high-grade penile intraepi-
study. BEA, MI, LH, SM and JV were involved in data acquisi- thelial neoplasia in Denmark 1978–2008: A nationwide
tion and analysis. BEA wrote the first draft of the manuscript. All population-based study. Cancer Causes Control 2012; 23:
authors reviewed and edited the manuscript and approved the 273–280.
final version of the manuscript. 11. Gross G and Pfister H. Role of human papillomavirus in
penile cancer, penile intraepithelial squamous cell neopla-
Acknowledgements sias and in genital warts. Med Microbiol Immunol 2004;
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for their support for this work. 12. Desai S, Chapman R, Jit M, et al. Prevalence of human pap-
illomavirus antibodies in males and females in England. Sex
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