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Cancer Epidemiology 43 (2016) 76–86

Contents lists available at ScienceDirect

Cancer Epidemiology
The International Journal of Cancer Epidemiology, Detection, and Prevention

journal homepage: www.cancerepidemiology.net

Data quality at the Singapore Cancer Registry: An overview of


comparability, completeness, validity and timeliness
Janice Wing Mei Funga,* , Sandra Bee Lay Lima , Huili Zhenga , William Ying Tat Hoa ,
Bee Guat Leea , Khuan Yew Chowa , Hin Peng Leeb
a
National Registry of Diseases Office, Singapore Cancer Registry, Health Promotion Board, 3 Second Hospital Avenue, Singapore 168937, Singapore
b
Saw Swee Hock School of Public Health, National University of Singapore, 12 Science Drive 2 #10-01 Singapore 117549, Singapore

A R T I C L E I N F O A B S T R A C T

Article history: Aim: To provide a comprehensive evaluation of the quality of the data at the Singapore Cancer Registry
Received 4 March 2016 (SCR).
Received in revised form 21 June 2016 Methods: Quantitative and semi-quantitative methods were used to assess the comparability,
Accepted 23 June 2016
completeness, accuracy and timeliness of data for the period of 1968–2013, with focus on the period
Available online 9 July 2016
2008–2012.
Results: The SCR coding and classification systems follow international standards. The overall
Keywords:
completeness was estimated at 98.1% using the flow method and 97.5% using the capture-recapture
Cancer registry
Data quality
method, for the period of 2008–2012. For the same period, 91.9% of the cases were morphologically
Neoplasms verified (site-specific range: 40.4–100%) with 1.1% DCO cases. The under-reporting in 2011 and 2012 due
Comparability to timely publication was estimated at 0.03% and 0.51% respectively.
Completeness Conclusion: This review shows that the processes in place at the SCR yields data which are internationally
Validity comparable, relatively complete, valid, and timely, allowing for greater confidence in the use of quality
Accuracy data in the areas of cancer prevention, treatment and control.
Timeliness ã 2016 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
2. Material . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
Sources of notification .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
3. Methods . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
3.1. Comparability . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
3.2. Completeness . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
3.3. Validity . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
3.4. Timeliness . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
4. Results . . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
4.1. Comparability . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
4.2. Completeness . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
4.3. Validity . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
4.4. Timeliness . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
5. Discussion . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
6. Conclusion . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
Conflict of interest . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
Authorship contribution . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
References . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85

* Corresponding author.
E-mail addresses: janice_fung@hpb.gov.sg, wingmei.fung@gmail.com
(J.W.M. Fung).

http://dx.doi.org/10.1016/j.canep.2016.06.006
1877-7821/ã 2016 Elsevier Ltd. All rights reserved.
J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86 77

1. Introduction performed manually by a team of nine registry staff and a visiting


consultant pathologist [13]. Retrospectively, a separate team of
Established in 1968, the Singapore Cancer Registry (SCR) is a staff perform annual audits on the data collected to ensure that the
population-based national registry with a repository of informa- level of data accuracy is at least 95%.
tion on borderline, in-situ and malignant tumours and benign Mortality data of all patients are obtained from the National
neoplasms which were diagnosed or treated in Singapore, with Death Registry on a two-monthly basis via secured file transfer
data collected by all available sources nation-wide [1]. Singapore is channels. The certification of death is virtually complete in
a multi-ethnic country with the Chinese, the Malays and the Singapore [13].
Indians being the three main ethnic groups in its resident
population, which includes Singapore citizens and permanent 3. Methods
residents. Residents comprised 94.5% of the total population in
1980, 81.2% in 2000, and 71.2% in 2013 due to a large influx of 3.1. Comparability
foreign workers in the past decades [2,3]. The SCR registers all
cases of cancer diagnosed in Singapore, but for this study, the Comparability is the extent of which coding and collection
incidence rates pertain only to Singapore’s resident population. practices adhere to international guidelines [14]. In this study,
The registry data is used for international and national bench- comparability is examined by reviewing the registry’s standards,
marking, guiding policy direction and in research [4]. The high definition and practices in incidence date and basis of diagnosis,
quality of data is hence critical for accurate decision making [5,6]. topography and morphology, coding of multiple primaries, and
The reporting of neoplasms has been mandatory since 2009, staging [15].
when the Ministry of Health enacted the National Registry of
Diseases (NRD) Act [7] to provide statutory regulations on 3.2. Completeness
reporting. All hospitals, laboratories, and healthcare institutions
in Singapore were required to report cancer cases [1,7,8]. Prior to Completeness is the extent to which all diagnosed cancer cases
this, cancer notifications were voluntary. in Singapore are captured in the registry database [10,14–16]. This
This study presents the first comprehensive evaluation of the allows us to determine whether incidence rates and survival
data quality of SCR in line with the evaluation guidelines published proportions reflect their true values. Taking reference from Parkin
by the International Agency for Research on Cancer (IARC) [9] and and Bray [10], we used the historic data approach (stability of
techniques covered by Bray and Parkin [10,11]. The quality of the incidence rates over time (1968–2013), shape of age-specific
data collected by the SCR will be assessed in the four indicative curves for selected cancers (2008–2012), and age-specific inci-
areas of comparability, completeness, validity and timeliness. dence rates of childhood cancer (2008–2012) compared with the
reference deciles for childhood cancer published in the Cancer
2. Material Incidence in Five Continents (CI5), Volume X [9]). Segi’s world
population was used for direct standardisation in calculating age-
Sources of notification standardised rates. Other semi-quantitative methods used include
the mortality/incidence (M:I) ratio (2008–2012) versus one minus
The sources of notification for the SCR had grown increasingly five years relative survival (2003–2012), and the number of
comprehensive since its establishment in 1968. Registrations were notifications per case (2008–2012) [10,15,17].
initially based on voluntary notifications received from clinicians Quantitative methods included the capture-recapture method
[12]. From 2001 onwards, the pool of sources was enlarged through (2008–2012) and the flow method for cases diagnosed in 2008 and
data obtained from pathology records, hospital discharge summa- followed up until 31 December, 2012. The capture-recapture
ries and death certificates [2]. This was enhanced by the enactment method assumes that all the notification sources are independent
of the NRD Act in 2009 which mandated medical professionals to of each other and all patients have the same probability of being
report all histologically verified and clinically diagnosed cancer captured in the Registry. However, these assumptions are likely to
incidents within three months from the date of diagnosis, using a be violated in cancer registration. The notification sources can be
structured notification form [1,8]. broadly classified into: clinical sources, pathological sources and
Modes of notification include usage of hardcopy forms or via an death certificates. When substantially two of three groups are
online national healthcare portal [4], with monthly tracking done dependent on each other, it is possible to correct for the
by registry staff. A secure electronic system also facilitates the dependency between the sources by pooling the two groups into
information transfer of the Hospital Inpatients Discharge Summary one broad group and compare it with the remainder group by a
(HIDS) listings. As a majority of cancer cases are diagnosed two-way capture-recapture method [18,19].
histologically, the SCR receives monthly pathology reports from all The flow method models the flow of individuals through the
public and private laboratories. Haematological, radiotherapy, and case ascertainment process from diagnosis to registration, taking
nuclear medicine information from treatment centres are also sent into account of the time since diagnosis [20]. Two datasets were
to the SCR on a regular basis. The workflow of the notification used to run the flow method: cases diagnosed in 2008 and cancer
process is illustrated in Fig. 1. cases who died in 2012. Using the flow method, we computed the
Patient data are collected using the unique national identity probability of patient being registered, missing or lost, and we
number issued to Singapore residents. For non-residents, their plotted the probability of patient being registered over the years
passport numbers or foreign identification numbers (FIN) are used since diagnosis.
[1]. These unique numbers minimize the risk of potential All statistical analysis were performed using Stata SE Version
duplication of records in the SCR database amidst multiple 13.
notification sources.
Data are captured via electronic transmission from hospitals to 3.3. Validity
the registry using the National Registry of Diseases System (NRDS)
since 2004, and additional information is collected manually from Validity refers to the accuracy of the data, and is defined by Bray
hardcopy medical records. During the data collection process, & Parkin as the proportion of cases in the registry with a given
verification of information for accuracy and completeness is characteristic which truly have this attribute [11]. The proportions of
78 J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86

Cancer notifications HIDS / Cancer listings Listings from Death


by physicians Pathology reports from HCIs e.g. NCC and registry / MHA
/nurses or listings other treatment centres

Match Patient’s Identification


number / Name against
existing records in NRDS

NO
New Primary?

YES

Create a new
Update existing case record in
records NRDS

need 1 NO
additional Notification from Wait for
Information? respective data Notification
YES source received?

YES
NO Abstract data at
EMR/NEHR/MRO
case record NO
to complete the
‘complete’?
registration.

YES

collect data at
Registration completed another HCI?
NO
YES

Legends: Go to 1
HCI Healthcare Institute
HIDS Hospital Inpatient Discharge Summary
MHA Ministry of Home Affairs
MRO Medical record office in hospital
NCC National Cancer Centre
NRDS National Registry of Diseases system
EMR Electronic Medical Records
NEHR National Electronic Health Records

Fig. 1. Workflow for cancer registration.

cases with morphological verification (MV%), death certificate- cancer site were coded according to International Classification of
only cases (DCO%), and cases with other and unspecified sites (O&U Diseases (ICD) 9th revision. Since 1993, the basis for coding has
%) were analysed. Taking reference from CI5, Volume X [9], SCR been changed to ICD-O-2 and subsequently to ICD-O-3 [23] from
data were compared with seven other regional registries which 2003 to present. The tumour morphology was coded according to
were selected based on geographical and ethnicity comparability, the Manual Of Tumor Nomenclature And Coding (MOTNAC) and
for the period 2003–2007. This allows for the assessment of ICD-O-2 in the early years and converted to ICD-O-3 [23] from
statistical differences using the detailed methods described in CI5, 2003 to present. For coding of haematopoietic and lymphoid
Volume VIII [22]. tissues, SCR follows the rules of the World Health Organisation
(WHO) Classification of Tumours [24], for cases from 2010 and
3.4. Timeliness forward. Fig. 2 gives a graphic overview of the international
standards that the SCR has been following for the classification and
Timeliness can be interpreted using the median time taken coding of neoplasms.
from diagnosis to registration and the time from registration to the The incidence date and basis of diagnosis has been recorded
reporting of incidence in SCR’s annual reports [14,15]. according to the IARC guidelines [25] since 2003. Prior to that, the
basis of diagnosis was determined based on a hierarchy of sources
4. Results with the date of histology examination accorded the highest
priority, to clinical confirmation [2]. The incidence date was based
4.1. Comparability on notifications by medical professionals.
The reporting of multiple primary tumours follows the IARC
The SCR registers incident cases of malignant and in-situ multiple primary rules [26]. A primary tumour or multiple primary
neoplasms. From 1968 to 1992, the topographical codes of the tumours at an organ or paired organ with the same morphology or
J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86 79

Fig. 2. The standards of classification and coding of neoplasms, Singapore, 1968–2013.

within the same morphology group is counted as one incidence. 4.2. Completeness
However, for data collection, the SCR also registers two tumours of
different laterality but of the same morphology in the same paired Annual trends in incidence rates of cancer did not display
organ, and two tumours at different sub-sites of the same organ of unusual or sudden systematic fluctuations for the period 1968–
the same morphology. The coding of morphology and recording of 2013 for all sites combined and top cancers (Fig. 3).
multiple primary cancers at the same organ or paired organ are The shapes of the age-specific incidence curves for males and
guided by the Multiple Primary and Histology Coding Rules Manual females in Singapore are typical for the major cancers, indicating
2007 from the Surveillance, Epidemiology, and End Results (SEER) no variability in completeness by age (Fig. 4). To retain similar
Program [27]. ethnic demographics, international comparisons were made with
The Registry follows the staging rules from the American Joint Eastern Asia and South Eastern Asia countries using data from
Committee on Cancer (AJCC) 6th edition [28] for cases diagnosed GLOBOCAN 2012 [31]. Countries with high quality national or
between 2003 and 2009. For cases diagnosed from 2010, the regional data were selected, namely Japan, Philippines, and
staging is assigned according to AJCC 7th edition [29]. Thailand for the year 2012, to compare with Singapore during
Classification and coding of cancers can be challenging. To the period of 2008–2012.
ensure accuracy and consistency, the SCR consults an in-house The age specific incidence rates for childhood cancer in
pathologist for reviewing of complex cases. The SCR also houses Singapore, 2008–2012, was compared with the upper and lower
two Certified Tumor Registrars (CTR) certified by the National deciles for childhood cancer published in CI5 Volume X [9]. The
Cancer Registrars Association (NCRA) [30], who ensure that the values were within range except for boys and girls aged 0–4 years
SCR coding practices adhere to international guidelines. which exceeded the upper limit of the reference interval (Table 1).

Annual trends in age-standardised incidence rates, Males Annual trends in age-standardised incidence rates for all sites
300.0 combined, and for Top 5 cancers, Females, 1968-2013, Singapore
300.0
Age-standardized rate (per 100,000 per year)

Age-standardized rate (per 100,000 per year)

250.0
250.0

200.0
All sites combined 200.0
All sites combined
Colo-rectum
150.0 Colo-rectum
150.0
Lung
Enactment of NRD Act Lung
Enactment of NRD Act
Prostate
100.0 100.0 Female Breast
Liver
Corpus uteri
Stomach
50.0 50.0 Ovary, etc

0.0 0.0
1968
1971
1974
1977
1980
1983
1986
1989
1992
1995
1998
2001
2004
2007
2010
2013
1968
1971
1974
1977
1980
1983
1986
1989
1992
1995
1998
2001
2004
2007
2010
2013

Year of diagnosis Year of diagnosis

Fig. 3. Annual trends in age-standardised incidence rates for all sites combined, for top cancers, Males and Females, 1968–2013, Singapore.
80 J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86

Colorectum, Male Colorectum, Female


500 400
AGE-SPECIFIC RATE (per 100,000 per year)

450

AGE-SPECIFIC RATE (per 100,000 per year)


350
400
300
350
300 250
Singapore (2008-2012)
250 200
200 Japan
150
150 Philippines
100
100 Thailand
50
50
0 0

0-14

15-39

40-44

45-49

50-54

55-59

60-64

65-69

70-74

75+
0-14

15-39

40-44

45-49

50-54

55-59

60-64

65-69

70-74

75+
AGE AGE
Thyroid, Females
Thyroid, Male 25

AGE-SPECIFIC RATE (per 100,000 per year)


25
AGE-SPECIFIC RATE (per 100,000 per year)

20
20 Singapore (2008-2012)

15 15
Japan

10 10
Philippines

5 5
Thailand

0 0
0-14

15-39

40-44

45-49

50-54

55-59

60-64

65-69

70-74

75+

0-14

15-39

40-44

45-49

50-54

55-59

60-64

65-69

70-74

75+
AGE AGE

Breast, Females
250
AGE-SPECIFIC RATE (per 100,000 per year)

200

150
Singapore (2008-2012)

100 Japan
Philippines
50
Thailand

0
0-14

15-39

40-44

45-49

50-54

55-59

60-64

65-69

70-74

75+

AGE

Fig. 4. Age-specific incidence curves for colorectal, thyroid and breast cancers, Singapore 2008–2012, compared with three Asian registries using data from GLOBOCAN 2012.

Table 1
Age-specific incidence rates per million of childhood cancers by gender, Singapore, 2008–2012.

Age Boys Reference1 Girls Reference1


0 4 27.6 <13.7 to >25.6 24.0 <11.3 to >23.2
5–9 11.8 <8.9 to >16.5 10.9 <7.0 to >12.7
10–14 16.3 <9.2 to >16.3 11.6 <7.9 to >14.9
1
The upper and lower deciles for childhood cancer incidence rates in CI5 Vol IX.
J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86 81

Males Females
1.0 1.0 Liver Oesophagus
Pancreas
Oesophagus Pancreas
Liver Lung Lung
0.8 0.8

Melanoma
0.6 0.6

M:I Rao
M:I Rao

All sites
0.4 Colorectum 0.4 Cervix uteri Colorectum
Melanoma Ovary, etc.
Lymphoma Lymphoma
Prostate Female
0.2 0.2 All sites
breast

Corpus uteri
0.0 0.0
0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0
1-survival 1-survival

Fig. 5. Mortality:Incidence ratios (2008–2012) versus 1 minus 5 yrs relative survival (2003–2012), Singapore.

The mortality/incidence (M:I) ratio is a comparison of mortality compared with those from clinical sources in a two-way capture-
statistics obtained from an independent source and the number of recapture method to estimate completeness for cases diagnosed in
new cancer cases in the same time period [10,14,32]. If the 2008–2012.
mortality data is reliable and accurate, with a steady trend of The overall completeness for the period 2008–2012 was
incidence and survival, the M:I ratio will be approximately 1 minus estimated to be 97.5% (Table 3). The lowest completeness was
5 years survival probability [10,33,34]. Any distortions in the M:I estimated for liver (83.5%), while the highest completeness was
ratio may suggest completeness issues [34]. estimated for lip, vermilion (100%). Liver cancer is highly fatal.
The mortality/incidence (M:I) ratios which had a strong Hence, due to strong negative dependency between pathological
coherence with 1-survival were pancreas, colorectum and lung sources and death certificates for liver cancer, its completeness was
cancers for males and females (Fig. 5). For prostate cancer and underestimated based on a two-way capture-recapture method.
breast, liver, oesophagus and melanoma cancer for females, the M:I The flow method estimates a completeness of registration of
ratio was higher than (1-survival), whereas lymphoma for males, 94.3% at one year and 98.1% at five years after cancer diagnosis for
corpus uteri and ovary cancer had a M:I ratio that was lower than all sites combined, for cancer cases diagnosed from 2008 till 2012
(1-survival). The M:I ratios for most cancer sites were similar to (Fig. 6).
those of the region, with the exception of oesophagus cancer which
had a M:I ratio higher than the region. 4.3. Validity
The average number of notifications per case for all sites
combined was 2.3 (Table 2). The site with the highest rate of Table 4 presents the age-standardised incidence rates (includ-
notifications per case was cervical uteri with 3.1 notifications per ing their standard errors) and the ratio of the observed value to the
case, compared to leukaemia with 1.4 notifications per case. A high expected value (O/E). The MV(%), DCO(%) and M:I(%) are also
number of notifications per case reduces the possibility of cancer shown as indicators of validity and completeness. For the period
diagnoses going unreported, thus increasing the completeness of 2003–2007, the proportion of MV cases for Singapore was 88.6% for
registry data [10]. males and 93.0% for females for all sites but non-melanoma skin,
Using the capture-recapture method for the period of 2008– and the proportion of DCO cases was 1.5% for males and 1.3% for
2012 and for all sites combined, the cases notified by clinicians and females (Table 4) The MV and DCO proportions observed in
pathologists formed the majority at 69.2%, followed by those Singapore was not significantly different from the region.
notified by pathologists only (17.1%) and clinicians only (9.4%). The Additionally, the O&U proportions were 2.3% for Singaporean
direction of dependency between each pair of sources is males and 2.0% for Singaporean females for the period 2003–2007
determined by comparing the true and estimated number of based on data from CI5-X [9].
cases. If there is positive dependence between two sources, the
capture-recapture method underestimates the true number of 4.4. Timeliness
cases, whereas negative dependence overestimates the true
number of cases [19,35]. While pathological sources and death The study shows that the timeliness of SCR data had improved
certificates were negatively dependent, there was positive significantly. The median time between diagnosis and registration
dependency between clinical sources and pathological sources. was halved from 160 days in 2005 to 76 days in 2013, and this trend
The strength of dependency between each pair of sources was was similar for both male and females (Fig. 7).
determined by evaluating the magnitude of under- or over- The incidence data reported in annual reports [8,36–40] appear
estimation of the true number of cases. The lower the magnitude, to be stable over time, with the number of cases diagnosed each
the weaker the dependency [35]. The dependency between year being consistently reported in the year of publication as well
pathological sources and death certificates was stronger than as subsequent years (Table 5). For example, the cancer incidence
other pairs as the over-estimated number of clinical cases was the for 2012 (12123 cases) was first reported in the 2008–2012 report
largest (data not shown). Hence, these cases were combined and which was published in 2014 [39]. This incidence for 2012 was
82 J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86

Table 2
Total number of cases, number of notifications per case, percentage of morphologically verified cases (MV%) and percentage of cases obtained from death certificate only (DCO
%), Singapore, 2008–2012.

ICD-9 ICD-O-31 Site Total No. of Cases No. of Notifications per case MV% DCO%
140 208 C00-C96 All sites 56697 2.3 91.9 1.1
140 C00 Lip 8 2.3 100.0 0.0
141 C01 C02 Tongue 294 2.4 100.0 0.0
142 C07-C08 Salivary gland 199 2.0 99.5 0.5
143 145 C03-C06 Mouth including gum, palate and floor of mouth 206 2.4 99.5 0.5
146 C09-10 Tonsil and Oropharynx 179 2.2 98.3 0.0
147 C11 Nasopharynx 1510 2.4 99.5 0.2
148 C12-C13 Hypopharynx 134 2.3 95.5 1.5
150 C15 Oesophagus 513 2.4 95.9 1.4
151 C16 Stomach 2502 2.3 97.0 0.8
152 C17 Small intestines 235 2.0 95.7 0.4
153 C18 Colon 5482 2.4 95.6 1.0
154 C19-C21 Rectosigmoid, Rectum and Anus 3309 2.5 97.7 0.3
155 C22 Liver and Intrahepatic ducts 2801 1.8 40.4 6.2
156 C23-C24 Gall bladder and Biliary ducts 561 2.1 81.6 1.1
157 C25 Pancreas 1417 2.2 76.4 3.2
158 C48 Retroperitoneum & Peritoneum 165 2.4 96.4 0.6
160 C30-C31 Nasal cavity, middle ear and accessory sinuses 166 2.2 99.4 0.6
161 C32 Larynx 375 2.3 97.6 0.3
162 C33-C34 Trachea, Bronchus and Lung 6503 2.4 86.0 2.3
163 C38.4 Pleura 82 2.4 95.1 0.0
164 C37 C38 excluding C38.4 Thymus, heart and mediastinum 249 2.0 98.0 0.8
170 C40-C41 Bones and articular cartilage 174 2.2 98.3 0.0
171 C47, C49 Connective and soft tissues 467 2.2 96.8 0.2
172 C43 Melanoma of skin 140 2.5 99.3 0.0
173 C44 Other neoplasms of Skin 2662 1.8 99.4 0.2
174 C50 (female) Female Breast 8507 2.4 99.4 0.2
175 C50 (male) Male Breast 29 1.9 96.6 0.0
180 C53 Cervix uteri 920 3.1 98.7 0.3
181 C58 Placenta 23 1.9 91.3 0.0
182 C54 Corpus uteri 1784 2.7 99.3 0.2
183 C56-C57 Ovary and other parts of female genital organs 1604 2.5 95.4 0.9
184 C51 C52 Vulva and Vagina 128 2.7 97.7 0.8
185 C61 Prostate 3321 2.5 96.5 0.2
186 C62 Testis 169 2.2 99.4 0.0
187 C60 & C63 Penis and other parts of male genital organs 107 2.6 100.0 0.0
188 C67 Bladder 926 2.3 98.1 0.4
189 C64-C66, C68 Kidney and other parts of Urinary organs 1497 2.3 87.5 1.7
190 C69 Eye 37 2.2 91.9 0.0
191 192 C70-C72 Brain, Spinal cord and parts of Central Nervous System 689 2.1 82.9 2.9
193 C73 Thyroid 1299 2.0 99.0 0.1
194 C74-C75 Adrenal gland, other endocrine glands and related structures 143 2.3 88.8 0.0
199 C80 Unspecified2 749 1.9 64.6 5.3
200, 202 C82-C85, C96 Non-Hodgkin's lymphoma 2002 2.2 100.0 0.0
201 C81 Hodgkin's disease 210 2.4 100.0 0.0
203 C88, C90 Multiple myeloma and immunoproliferative neoplasms 454 1.9 93.0 0.0
204 C91 Lymphoid leukaemia 455 2.3 95.6 0.4
205 C92 Myeloid leukaemia 1111 2.0 93.7 0.0
206 C93 Monocytic leukaemia 47 2.6 100.0 0.0
207 C94 Other leukaemia 114 1.4 69.3 0.0
208 C95 Leukaemia, unspecified 39 1.7 94.9 2.6
1
ICD-10 codes were used for C43, C82-95.
2
“Unspecified” include unknown primary sites.

updated in the 2009–2013 report which was published in 2015 In terms of completeness, the modified flow method gave
(12185 cases) [40]. The percentage difference of 0.51% therefore higher estimates than the capture-recapture method. The modified
shows a slight under-reporting for the 2012 cancer incidence. flow method is more appropriate for the SCR as it is able to adjust
for delayed registration [20] since the SCR collects data retrospec-
5. Discussion tively, but the results from both methods affirm the high level of
completeness of registration of around 97–98%.
This evaluation of the data quality of the SCR suggests a high A limitation of the capture-recapture method is its assumption
degree of comparability, completeness, validity and timeliness. The that all notification sources are independent of each other and all
quality of data was also recognized by the IARC in the GLOBOCAN patients have the same probability of being captured in the
2012 project where SCR’s data was conferred a data quality index of registry, which are likely to be violated in cancer registration
A1, indicating high quality national incidence and mortality data [18,41]. However, taking reference from Brenner [19] and Larsen
[31]. It meets the prerequisites of high quality data with its et al. [14], it is possible to correct for the dependency between the
mandatory reporting of neoplasms, unique personal identification sources by pooling the two groups into one broad group and
numbers and extensive access to sources of notification. compare it with the remainder group by a two-way capture-
J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86 83

Table 3
Capture/recapture estimation on combination of death certificates and pathological sources, Singapore, 2008–2012.

ICD-9 ICD-O-31 Site True Dependency between


Number
D: C versus C: D versus P: C versus Completeness (%)
P3 P4 D5
140 208 C00-C96 All sites 56697 + 97.5
140 C00 Lip 8 NA NA NA 100.0
141 C01 C02 Tongue 294 NA NA NA 99.1
142 C07-C08 Salivary gland 199 NA NA NA 97.7
143 145 C03-C06 Mouth including gum, palate and floor of mouth 206 NA NA NA 99.3
146 C09-10 Tonsil and Oropharynx 179 + + 97.8
147 C11 Nasopharynx 1510 NA NA NA 98.9
148 C12-C13 Hypopharynx 134 + + 98.1
150 C15 Oesophagus 513 + + 98.7
151 C16 Stomach 2502 + 98.4
152 C17 Small intestines 235 + + 93.0
153 C18 Colon 5482 + 98.7
154 C19-C21 Rectosigmoid, Rectum and Anus 3309 + 99.1
155 C22 Liver and Intrahepatic ducts 2801 + 83.5
156 C23-C24 Gall bladder and Biliary ducts 561 95.8
157 C25 Pancreas 1417 + 95.0
158 C48 Retroperitoneum & Peritoneum 165 + + + 97.6
160 C30-C31 Nasal cavity, middle ear and accessory sinuses 166 + + + 97.4
161 C32 Larynx 375 + 98.9
162 C33-C34 Trachea, Bronchus and Lung 6503 + 97.6
163 C38.4 Pleura 82 + + 98.2
164 C37 C38 excluding Thymus, heart and mediastinum 249 NA NA NA 94.0
C38.4
170 C40-C41 Bones and articular cartilage 174 NA NA NA 94.0
171 C49 Connective and soft tissues 467 NA NA NA 95.2
172 C43 Melanoma of skin 140 NA NA NA 98.3
173 C44 Other neoplasms of Skin 2662 + + 99.2
174 C50 (female) Female Breast 8507 + + 99.6
175 C50 (male) Male Breast 29 NA NA NA 95.9
180 C53 Cervix uteri 920 + 99.4
181 C58 Placenta 23 NA NA NA 84.1
182 C54 Corpus uteri 1784 + + 99.3
183 C56-C57 Ovary and other parts of female genital organs 1604 + 97.0
184 C51 C52 Vulva and Vagina 128 NA NA NA 99.0
185 C61 Prostate 3321 + 98.8
186 C62 Testis 169 + 97.2
187 C60, C63 Penis and other parts of male genital organs 107 NA NA NA 98.9
188 C67 Bladder 926 + + 98.3
189 C64-C66, C68 Kidney and other parts of Urinary organs 1497 + 96.9
190 C69 Eye 37 NA NA NA 97.5
191 192 C70-C72 Brain, Spinal cord and parts of Central Nervous System 689 + 91.5
193 C73 Thyroid 1299 + + 96.6
194 C74-C75 Adrenal gland, other endocrine glands and related 143 NA NA NA 94.5
structures
199 C80 Unspecified2 749 + + 89.0
200, 202 C82-C85, C96 Non-Hodgkin's lymphoma 2002 + 97.9
201 C81 Hodgkin's disease 210 NA NA NA 99.5
203 C88, C90 Immunoproliferative neoplasms and multiple myeloma 454 NA NA NA 91.2
204 C91 Lymphoid leukaemia 455 NA NA NA 94.2
205 C92 Myeloid leukaemia 1111 + + 92.2
206 C93 Monocytic leukaemia 47 99.4
207 C94 Other leukaemia 114 NA NA NA 53.8
208 C95 Leukaemia, unspecified 39 NA NA NA 67.5

Notes:
a. Cases from death certificate and pathology sources were combined and compared with those from clinical sources in a two-source capture-recapture analysis to estimate
completeness for all sites.
b. The dependency between death certificate and pathology sources was stronger than other pairs as the over-estimated number of clinical cases was the largest. There is also
a high proportion of sites in the same direction of negative dependency.
c. “NA” refers to “Not Applicable”. The dependency for these sites cannot be calculated as there were no cases from C + P + D.
1
ICD-10 codes were used for C43, C82-95.
2
“Unspecified” include unknown primary sites.
3
D: C versus P: between clinical and pathology sources for all death certificates.
4
C: D versus P: between death certificate and pathology sources for all clinical records.
5
P: C versus D: between clinical and death certificate sources for all pathology records.
84 J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86

recapture method. Nevertheless, overestimation can still occur due


to positive dependency between two sources and vice versa [19].
The flow method analysis was modelled after Montanaro’s
modified method [20] which was able to take into account delays
between the diagnosis date and registration, since the SCR does not
collect real-time data. A limitation is that the reliability of the
analysis depends on the quality of death data available.
The semi-quantitative evaluation of completeness displayed
relatively stable trends of annual incidence ASR over time and
typical shapes of the age-specific incidence curves. The childhood
cancer incidence rates were within the reference ranges except for
values for boys and girls aged 0–4 years where the incidence rates
were above the upper limits of the reference interval. This is likely
to be an incidental finding as data cleaning was performed to
ensure that there were no duplicate registrations or coding errors.
The M:I ratio was higher than (1-survival) for prostate cancer
and breast, liver, oesophagus and melanoma cancer for females
Fig. 6. Completeness of ascertainment according to time since diagnosis for all which may suggest incompleteness in incidence, whereas lym-
cancer sites combined, 2008–2012.
phoma for males, uterine and ovary cancer had a M:I ratio that was

Table 4
Singapore (2003–2007), regional comparison of incidence rates (ASRs), MV%, DCO% and M/I ratios.

MALE

SITE Cases ASR (se) O/E MV(%) DCO(%) M/I(%) ICD-10


Lip, oral cavity and pharynx 1770 16.6 (0.41) 1.23 98.8 0.4 46.0 C00 14
Oesophagus 335 3.6 (0.2) 1.08 96.4 0.9 97.9> C15
Stomach 1325 14 (0.39) 1.10 97.4 0.6 70.8 C16
Colon, rectum and anus 3890 40.3 (0.66) 1.12 97.1 0.7 44.3 C18 21
Liver 1663 17.4 (0.44) 1.11 39.7 4.6 91.9 C22
Pancreas 569 5.9 (0.25) 1.12 70.5 4.6 95.3 C25
Larynx 353 3.7 (0.2) 1.11 96.9 0.3 40.8 C32
Lung (incl. trachea) 3852 41.1 (0.67) 1.09 87.0 2.0 88.4 C33 34
Melanoma of skin 50 0.5 (0.07) 1.20 50.0< 0.0 52.0 C43
Prostate 2190 24.2 (0.52) 1.05 96.3 0.2 20.0 C61
Testis 119 1.3 (0.13) 1.08 98.3 0.0 5.0 C62
Kidney etc. 632 6.3 (0.26) 1.16 87.5 1.3 35.4 C64 66, C68
Bladder 637 7.1 (0.28) 1.11 98.1 0.3 26.5 C67
Brain, central nervous system 230 2.4 (0.17) 1.13 83.5 4.8 70.0 C70 72
Thyroid 215 2.1 (0.15) 1.19 98.6 0.0 12.1 C73
Lymphoma 1157 11.7 (0.36) 1.10 99.7 0.3 34.1 C81 88,C90
Leukaemia 537 6.4 (0.29) 0.97 99.3 0.7 51.6 C91 95
All sites but non melanoma skin 20963 219.9 (1.56) 1.11 88.6 1.5 60.2 C00 96bC44

Female

Site Cases ASR (se) O/E MV(%) DCO(%) M/I(%) ICD-10


Lip, oral cavity and pharynx 648 5.5 (0.22) 1.35 99.8 0.2 36.7 C00 14
Oesophagus 83 0.6 (0.07) 1.50 89.2 2.4 95.2> C15
Stomach 850 7.1 (0.25) 1.37 96.1 1.1 74.5 C16
Colon, rectum and anus 3363 28.8 (0.51) 1.34 95.3 1.1 44.6 C18 21
Liver 534 4.6 (0.21) 1.33 39.8 5.1 98.7 C22
Pancreas 466 4.0 (0.19) 1.33 57.9 8.2 98.1 C25
Larynx 33 0.3 (0.05) 1.33 90.9 3.0 42.4 C32
Lung (incl. trachea) 1898 16.3 (0.38) 1.33 83.3 3.2 83.2 C33 34
Melanoma of skin 57 0.5 (0.07) 1.40 100.0 0.0 47.4 C43
Breast 6717 57.8 (0.72) 1.33 99.0 0.3 23.6 C50
Cervix uteri 1013 8.9 (0.29) 1.30 99.5 0.2 38.6 C53
O&U part of uterus 1337 11.8 (0.33) 1.30 99.0 0.1 15.4 C54-55
Ovary 1003 9.1 (0.29) 1.29 94.1 1.4 47.5 C56
Kidney etc. 332 3.1 (0.18) 1.23 82.5 1.2 37.3 C64 66, C68
Bladder 206 1.9 (0.13) 1.37 98.1 0.0 34.5 C67
Brain, central nervous system 191 2.1 (0.16) 1.05 84.3 3.1 52.9 C70 72
Thyroid 650 5.9 (0.24) 1.25 99.4 0.2 11.4 C73
Lymphoma 841 7.8 (0.28) 1.21 99.3 0.7 35.9 C81 88,C90
Leukaemia 443 5.1 (0.26) 1.00 99.3 0.7 47.9 C91 95
All sites but non melanoma skin 21915 192 (1.34) 1.31 93.0 1.3 46.2 C00 96bC44

Notes:
a. Significantly lower (<) or higher (>) values are shown in bold.
b. SCR data were compared with Malaysia (Penang), Thailand (Bangkok), Philippines (Manila), China (Hong Kong), Japan (Osaka), Republic of Korea and India (New Delhi)
based on geographical and ethnicity comparability.
c. Data Source: CI5 X, International Agency for Research on Cancer (IARC), 2014.
d. Statistical tests performed were modelled after the detailed methods described in CI5-VIII, Comparability and quality of data chapter (page 72).
J.W.M. Fung et al. / Cancer Epidemiology 43 (2016) 76–86 85

Table 5
Number of registered cancer cases in Singapore from 2008 to 2012, comparing the incidence first published in the annual report to the incidence reported in the next annual
report.

Year of annual report publication

2010 2011 2012 2013 2014 2015 (09-13 report) % Difference


(04- (05- (06- (07- (08-12
08 report) 09 report) 10 report) 11 report) report)
Number of registered cancer cases by year 2008 10316 10316 0.00

2009 10568 10579 0.10


2010 11160 11144 0.14
2011 11525 11529 0.03
2012 12123 12185 0.51

between data timeliness and data completeness as both improved


over the years.
180.0
6. Conclusion
160.0

140.0 This review indicated that the SCR adheres to international


120.0
guidelines, has a high degree of completeness, accuracy and
timeliness. It should however be kept in mind that an efficient
Median days

100.0 national registry system is not the end goal; the eventual
80.0 Male objectives are to step up actions to prevent, control and improve
Female interventions for cancer care. This review allows for greater
60.0 confidence in the use of the quality data in the SCR for treatment
40.0 and research, as well as the evaluation of national programmes
such as the National Breast Cancer Screening Programme [43] and
20.0
the National Cervical Screening Programme [44], which in turn
0.0 impacts decision-making by the Singapore health authorities.
2005 2006 2007 2008 2009 2010 2011 2012 2013
Year Conflict of interest

Fig. 7. Median time between diagnosis and registration, Males and Females,
None declared.
Singapore 2005–2013.

Authorship contribution

Study concept and design: JWMF, SBLL. Data acquisition:


lower than (1-survival). Based on regional comparisons shown in WYTH, BGL. Quality control of data: SBLL. Data analysis and
Table 4, the M:I ratio for oesophageal cancer was higher than the interpretation: JWMF. Statistical analysis: HZ. Manuscript prepa-
region for both males and females. However, the results need to be ration: JWMF. Critical revision of the manuscript for important
interpreted with caution as under-reporting or over-reporting or a intellectual content: JWMF, SBLL, KYC, HPL.
lack of stability of incidence and mortality trends may distort the
results [10]. Additionally, this method may not be appropriate for References
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