42Gac Sanit. 2006;20(Supl 3):42-51 Accuracy of cancer death certificates in Spain: a summary of available information Beatriz Pérez-Gómeza / Nuria Aragonésa / Marina Pollána / Berta Suáreza / Virginia Lopea / Alicia Llácerb / Gonzalo López-Abentea aÁrea de Epidemiología Ambiental y Cáncer. Centro Nacional de Epidemiología. Instituto de Salud Carlos III. Madrid. España. bÁrea de Análisis Epidemiológico y Situación de Salud. Centro Nacional de Epidemiología. Instituto de Salud Carlos III. Madrid. España. (Validez de la certificación de la muerte por cáncer en España: resumen de la evidencia disponible) Correspondencia: Beatriz Pérez-Gómez. Área de Epidemiología Ambiental y Cáncer. Centro Nacional de Epidemiología. Instituto de Salud Carlos III. Sinesio Delgado, 6. 28029 Madrid. España. Correo electrónico: bperez@isciii.es Recibido: 25 de noviembre de 2005. Aceptado: 22 de febrero de 2006. Abstract Objectives: Differences in mortality rates within Europe might be partly due to the quality of mortality statistics. The present article summarizes the available data on the quality of can- cer death certification in Spain. A short description of the tem- poral distribution of the proportion of deaths due to ill-defined tumors in Spain –an indirect indicator of the quality of cancer death certification– is also provided. Methods: Relevant studies were identified from electronic da- tabases (MEDLINE, EMBASE, IME and IBECS) and from ma- nual searches of the references contained in the articles re- trieved. Quality data on death certificates for all tumors and for each specific cancer location were summarized, and all main cancer sites were classified according to their pooled accu- racy indicators. Trends for the percentage of deaths due to ill- defined tumors and conditions were studied for the period from 1980 to 2002. Results: In Spain, deaths from cancer as a whole and lea- ding cancer sites (lung, colon-rectum, prostate, stomach, pan- creas, female breast, uterus, brain, leukemia, lymphomas and myeloma) were well-certified. However, other frequent loca- tions, such as the larynx, esophagus and liver were overcer- tified, while deaths from bladder, kidney and ovarian cancer were undercertified. The percentage of deaths due to ill-de- fined tumors and causes was regularly higher in females and decreased in both sexes during the study period. However, the recent introduction of the International Classification of Di- seases (ICD)-10 has reversed this trend. Conclusions: Spanish death certificates can be considered as accurate and useful to estimate the burden of cancer, though certification of some frequent sites should be improved. The possible effect of the introduction of the ICD-10 requires ca- reful surveillance. Key words: Death certificates. Mortality. Cancer. Quality con- trol. Spain. Resumen Objetivos: Parte de las diferencias en tasas de mortalidad por cáncer entre países europeos podrían deberse a diferencias de calidad en las estadísticas de mortalidad. Nuestro objeti- vo es sintetizar la información cuantitativa que hay acerca de la calidad de los certificados de defunción de cáncer en Es- paña, y se añade una somera descripción de la evolución tem- poral de la proporción de defunciones por tumores mal defi- nidos, indicador indirecto de calidad. Métodos: Se identificaron los estudios relevantes mediante búsquedas en bases de datos electrónicas (MEDLINE, IME, EMBASE e IBECS), y posteriormente se añadieron referen- cias presentes en los artículos encontrados. Se extrajo la in- formación acerca de calidad de certificación para cáncer en conjunto y para las principales localizaciones tumorales, y se clasificaron los tumores según sus indicadores de calidad. Se estudió también la tendencia del porcentaje de muertes mal definidas o tumores mal definidos entre 1980-2002. Resultados: En España, el cáncer en conjunto y las princi- pales localizaciones –pulmón, colon-recto, próstata, estóma- go, páncreas, mama, útero, cerebro, leucemia, linfomas y mie- loma– están bien certificados. Sin embargo, otras localizaciones como laringe, hígado y esófago están sobrecertificadas, mien- tras que el cáncer de vejiga, riñón y ovario están infracertifi- cados. Los porcentajes de muertes por tumores o condicio- nes mal definidas, mayores en mujeres, han disminuido en el período estudiado, aunque la introducción de la CIE-10 ha invertido esta tendencia. Conclusiones: En general, los certificados de cáncer pue- den considerarse válidos y útiles para estimar el impacto del cáncer en España, aunque la certificación de algunas locali- zaciones importantes tendría que mejorar. Debería estudiar- se el posible efecto de la introducción de la CIE-10. Palabras clave: Certificados de defunción. Mortalidad. Cán- cer. Control de calidad. España. Background One of the most usual approaches to studying the situation of cancer worldwide is to analyse the geographic distribution of mortality rates and their trends. Informa- tion on the quality of cancer mortality data is thus es- sential for interpreting differences in mortality statistics. In Spain, mortality represents the only comprehen- sive and homogeneous source of information on can- cer for the whole country. The source of mortality sta- tistics is the medical death certificate (DC), a compulsory administrative document completed by the practitioner who certifies the death. This certificate is subsequently transcribed onto a second document, the Statistical Bu- lletin of Death (SBD), and both are sent to the Munici- pal Civil Registry. Usually, the Civil Registry forwards the SBDs to the regional offices of the National Statis- tic Institute (Instituto Nacional de Estadística [INE]) on a monthly basis, where all items except cause of death are digitally recorded. When the data have been duly screened to detect errors and ensure quality control, the underlying causes of death (Causa básica de defunción) are coded at the Regional Authority Mortality Registries by trained teams, applying common criteria in accor- dance with International Classification of Diseases (ICD) guidelines. National coding protocols have been esta- blished to guarantee homogeneity of data1, while spe- cific methods have also been implemented to validate accuracy systematically. Digital data files are then sent to the INE head office, which releases them once they have been rendered anonymous. Quantitative data that would enable to asses the qua- lity of cancer death certificates in Spain are relatively scarce. Several studies have addressed this topic, but all refer to areas of the country or to specific popula- tions, and some have been published in local epide- miological bulletins or in symposium proceedings, which are not easily accessible. In this paper, we sought to synthesize information derived from these studies and to complement such data with a short description of the temporal distribution of the proportion of deaths due to ill-defined tumours in Spain, as an indirect indicator of the quality of cancer death certification. Methods For review purposes, DC and SBD were deemed to be death certificates, as a very high concordance bet- ween both documents has been reported2. Studies into the quality of cancer death certification in Spain were identified through: 1) a MEDLINE and EMBASE search using broad search criteria (January 1966 to January 2006); 2) a similar search in Spanish bibliographical da- tabases, the Spanish Medical Index (Índice Médico Es- pañol [IME]), and IBECS; and 3) references in identi- fied papers. In two studies3,4, only abstracts of poster presentations at scientific meetings were published. In these cases, quality-indicator data presented in the pos- ter were specifically searched for. Studies were considered eligible if they reported quantitative estimates of the accuracy of death certifi- cates containing any mention of cancer. In these stu- dies, cancer death certificates were compared against a second source of information, mainly comprising cli- nical or anatomo-pathological reports (which were taken as the «gold standard»). Agreement between both sources was measured using detection and confirma- tion rates. According to Percy et al5, the detection rate (DR) or sensitivity for a specific site is defined as the propor- tion of hospital diagnoses (available clinical/anatomo- pathological information) with cancer of a certain site, with a death certificate where this disease is conside- red to be the basic cause of death, whereas the con- firmation rate (CR) or positive predictive value is the pro- portion of cancer deaths in which the underlying cause specified in the death certificate is confirmed by hos- pital diagnosis. DRs and CRs can be computed as: a) site-speci- fic cancer rates at three digits of the ICD, that is con- sidering an indicator per cancer-site; b) all-site three- digit rates, an overall indicator for cancer where the rates’ numerator contains all cancer cases (ICD-9 codes 140-208) in which the site specified in the death cer- tificate and clinical information agree; and c) all-tumour rates, also an overall indicator where the rates’ nu- merator includes all cases that just mention «cancer» in both the death certificate and gold standard, even though there might be site misclassification. These fi- gures are logically expected to be higher than overall comparisons at a three-digit level. A graphical sche- me that might help understand these concepts is shown in figure 1. Identified papers were classified into three main ca- tegories: I. Studies focusing on all-cause death certificates, which provide accurate detection and confirmation rates (fig. 1). II. Studies based solely on death certificates that mention cancer. These could be subdivided into two groups: a. Studies with an additional source of informa- tion on cg or bg (fig. 1) that allows them to esti- mate accurate detection and confirmation rates. In some cases, these data6 were not considered for the purpose of calculating site-specific can- cer rates, thereby leading to overestimated rates. 43 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 b. Studies without information on cancer deaths not certified as such, or on non-cancer cases erro- neously certified as cancer (cg or bg). This rules out the possibility of computing all-tumour or three-digit agreement detection rates, and means that site-specific detection rates and confirma- tion rates are likely to be overestimated (fig. 1). In some cases4,7,8, it was possible to find infor- mation on global false positives within the text of the paper. We used these data to calculate un- biased all-tumour confirmation rates. III. Necropsy-based studies. Since necropsies are relatively scarce in this country9, the main problem with these studies is external validity, as they tend to focus on very specific populations. Many of the detection and /or confirmation rates of- fered in the summary tables were directly taken from the selected studies, though, where possible, the tables were completed by computing DRs and CRs using data provided in the papers. In a second stage, a pooled CR and DR was cal- culated for each specific cancer location using data from all studies that had covered that location, and then all main cancer sites were classified according to Percy’s criteria, the bench-mark for these types of studies5. Fi- nally, as a complementary approach, we calculated the percentage of deaths due to ill-defined tumour versus all-tumour deaths and the percentage of deaths of ill- defined conditions versus all-cause deaths for the pe- riod 1980-2002, using whole country mortality figures supplied by the INE. Results Published studies on quality of cancer death certificates in Spain A total of 14 studies providing quantitative data on quality of cancer death certification in Spain were found. The main characteristics of these studies, their classi- fication according to the above criteria and, where avai- lable, all-tumour (ICD-9 codes 140-208) and all-site three- digit detection and confirmation rates are shown in table 1. In addition, figure 2 depicts the geographical loca- tion of the respective study populations. Six of these studies belonged to categories I and II(a)3,6,10-14, those furnishing the most accurate estima- tors, with detection rates ranging from 75.2-100% for all tumours as a whole and 64.8-100% for all-site three- digit rates. On average, confirmation rates were higher than detection rates, ranging from 91.5-99.3% for all- tumour and 68.2-80.8% for all-site three-digit rates. Another five studies were classified as category II(b)7,8,15-18. In general, they supplied data on all-tumour and all-site three-digit confirmation rates. Yet, with two exceptions4,8, these studies failed to consider global false positives when estimating three-digit confirmation rates, an approach that implies a certain overestimation of the agreement. Where possible, therefore, we calculated a 44 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 Site-specific detection rate = a / (a + cg + cs) Site-specific confirmation rate = a / (a + bg + bs) All-site three-digit detection rate = ∑a / ∑(a+ cg + cs) All-site three-digit confirmation rate = ∑a /∑ (a + bg + bs) All-tumour detection rate = a + bs + cs / a + bs + cs + cg All-tumour confirmation rate = a + bs + cs / a + bs + cs + bg = site-concordant cases = global false positive (corresponds to a non-cancer cause of death) = site false positive (corresponds to cancer at other location = global false negative (cancer case certified outside ICD cancer codes) = site false negative (cancer case certified as cancer at other location) = true negative cases a bg bs cg cs d DC/SBD + _ + a cg + cs – bg + bs d DC/SBD + _ + a + bs + cs cg – bg d Clinical/anatomo-pathological information Clinical/anatomo-pathological information a) Three-digit agreement rates b) All-tumour agreement rates Figure 1. Cross-tabulation of cause of death according to clinical diagnoses and medical death certificates and quality-indicator formulae. corrected confirmation rate by including global false po- sitives in the denominator. Only one study8 had adop- ted this approach and, in this case, the «biased» con- firmation rate (excluding global false positives) was reckoned for comparison purposes. Both «biased» –de- noted by «*»– and corrected confirmation rates are shown in table 1. On average, biased confirmation rates were three points higher than corrected rates. In these stu- 45 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 Euskadi (Basque Country) (Izarzurgaza, 1994) Soria (Ruiz Liso, 1989) Zaragoza (DGA, 1988) Girona (Sánchez Garrido, 1996) Terrasa (Nava, 1985, 1986) Barcelona (Bosch, 1981, 1983; Pañella, 1989) Mallorca (Cáffaro, 1995) Valencia (García Benavides, 1986,1989) Murcia (Navarro, 1984; Cirera, 2002) Granada (Martínez, 2000) Galicia (Carballeira, 1989) Figure 2. Geographical location of published studies furnishing data on quality of cancer death certification in Spain. Table 1A. Quality of cancer death certification in Spain. Characteristics and classification of published studies sorted by publication year Death certificates Study category Author Geographic location Institution Period analysed or SBDa All-cause/cancer I I I I II(a) II(a) II(b) II(b) II(b) II(b) II(b) II(b) III III García-Benavides, 198610, 198911 Pañella, 198912 Ruiz Liso, 198913 Giménez, 20023 Cáffaro, 19956 Sánchez-Garrido, 199614 Bosch, 198115, 198316 Navarro, 198417 DGA, 198818 Izarzurgaza, 19944 Martínez, 20008 Cirera, 20027 Nava, 1985, 198619;35 Carballeira, 19899 Valencia (city) Barcelona (city) Soria (province) a) National b) National Island of Majorca Girona (province) Barcelona (city) Murcia (province) Zaragoza (city) Euskadi (Basque Country) (region) Granada (province) Murcia (region) Terrassa (city) Galicia (region) University of Alicante Municipal Institute of Health Provincial Hospital CISATER CISATER Cancer Registry Catalonian Institute of Oncology Provincial Hospital Cancer Registry Hospital, Municipal Institute of Health Public Health Authority, Cancer Registry Cancer Registry Cancer Registry Cancer Registry Cancer Registry Comarcal Private Hospital Public Health Authority 1984 1985 1985 1981-1995 1987-1998 1989 1985-1989 1979 May 1981- Oct 1983 1983 1989 1991-1994 1992 1980-1981 1987 1,068/279 1,480/197a 993/260a 1,465/284 773/224a –/1,255 –/244a –/2,945 –/2,928a –/1,366a –/3,945a –/4,772 –/1,658 49/7 90/19a SBD: Statistical Bulletin of Death. aThe study uses SBD. 46 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 dies, all-tumour and corrected all-site three-digit con- firmation rates were comparable to those obtained for categories I and II(a). Only two papers came within category III (necropsy- based studies)9,19. Their results were slightly worse than others, but it should be borne in mind here that in Spain most autopsies are restricted to cases with uncertain diagnosis. Table 2 summarises available information in Spain on detection and confirmation rates for malignant neo- plasms by the main specific locations. The data, sor- ted by the period analysed, revealed that in the interim between the early 1980’s and the most recent study (1992 data), the quality of certification had improved. Highest indices were found for cancer of the stomach, colon and rectum, pancreas, lung, melanoma, female breast, brain and haematological tumours. In contrast, other sites, such as ill-defined tumours and non-mela- noma skin cancer, displayed lower rates of agreement. Furthermore, in order to have a brief overview of the quality of cancer certification for specific sites, pooled estimators were calculated to classify the accuracy of death certification for specific cancers according to Percy’s criteria5, which depend on detection and con- firmation rates (table 3). Ill-defined tumours and ill-defined causes Figure 3 shows the trend in the percentage which ill-defined tumours and ill-defined causes represent of all-cancer and all-cause deaths, respectively, over the calendar period 1980-2002, in both sexes. During the 1980’s, Regional Mortality Registries became respon- Table 1B. Quality of cancer death certification in Spain. Characteristics and classification of published studies sorted by publication year Cancer DC with Cancer deaths detected only DR (%) Author Savailable information by validating source (global false CR (%) Notes All-cause/cancer from validating source positives) 279 154 233 1,173 1,557 644 685 3,298 4,231 1,371 7 19 30 (revised DC without mention of cancer) 36 (revised SBD without mention of cancer) 0 91 (clinical follow-up) 29 (clinical follow-up) 65 (Cancer registry) 61 (Cancer registry) Not searched Not searched Not searched Not searched Not searched Not searched 6 (cancer deaths only detected by necropsy) 5 (cancer deaths only detected by necropsy) 89.9(G) 71.7(3D) 79.9(G) 64.8(3D) 100(G) 100(3D) 75.2(G) 88.1(G) 94.7(G) 93.3(3D) 50.0(G) 38.5(3D) 73.7(G) 42.1(3D) 95.3(G) 76.9(3D) 92.9(G) 68.2(3D) 91.5(G) 80.8 (3D) 97.5(G) 96.0(G) 99.3(G) 73.0(3D) 77.2(3D)a 81%(3D)* 64.4(3D)* 73.1(3D)* 99.1(G) 79.5(3D) 0.80.1(3D)* 96.2(G) 74.0(3D) 76.9(3D)* 98.5(G) 76.7(3D) 79.4(3D)* 85.7(G) 71.4(3D) 73.7(G) 42.1(3D) Studies all DC of this period Studies all DC of this period. Validating source: histopathological records. Unconfirmed cases are considered ill certified No additional cases found Toxic Oil cohort Excludes multiple tumours Only gynaecological cancer Excludes ill-defined & multiple tumours and non-residents in the province Exclude multiple tumours, in situ, skin non-melanoma and non-residents in this region Excludes multiple tumours Necropsy-based Necropsy-based CR: Confirmation rate; DR: Detection rate; G: all-tumour agreement rates (ICD-9 codes 140-208); 3D: all-site three-digit agreement rates. 3D*: all-site three-digit agreement rates with only those death certificate (DC) / Statistical Bulletin of Death (SBD) that really corresponded to malignant tumours used as denominator. García-Benavides, 198610, 198911 Pañella, 198912 Ruiz-Liso, 198913 Giménez, 20023 Cáffaro, 19956 Sánchez-Garrido, 199614 Bosch, 198115, 198316 Navarro, 198417 DGA, 198818 Izarzurgaza, 19944 Martínez, 20008 Cirera, 20027 Nava, 1985, 198619;35 Carballeira, 19899 47 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 Ta bl e 2. S pa ni sh c an ce r-d ea th -c er tif ic at e de te ct io n an d co nf irm at io n ra te s by s ite M ur ci a G ra na da Eu sk ad i M aj or ca G ir on a B ar ce lo na S or ia Va le nc ia 1 98 4 Za ra go za M ur ci a 19 92 91 /9 4 19 89 19 89 85 -8 9 19 85 19 85 (G ar cí a 83 19 81 (C ir er a, (M ar tín ez , B as qu e (C áf fa ro , (S án ch ez , (P añ el la , (R ui z Li so , B en av id es , (D G A , (N av ar ro , 20 02 )6 20 00 )1 7 C ou nt ry ) 19 95 )6 96 )1 4 19 89 )1 2 19 89 )1 3 19 86 ,1 98 9) 9, 12 19 88 )1 8 19 84 )1 7 Lo ca tio n IC D -9 c od es D R C R D R C R D R C R D R C R D R C R D R C R D R C R D R C R D R C R D R C R M ou th & p ha ry nx 14 0- 14 9 56 .6 81 .1 55 .5 89 .2 67 .5 87 .7 57 .8 92 .9 10 0. 0 10 0. 0 60 .0 75 .0 57 .1 80 41 .4 57 .1 O es op ha gu s 15 0 95 .2 69 .0 79 .4 72 .5 90 .1 85 .5 92 .9 76 .5 75 .0 10 0. 0 85 .7 75 .0 84 .6 68 .7 86 .4 76 .0 S to m ac h 15 1 82 .0 88 .5 80 .7 87 .8 88 .2 90 .8 75 .0 84 .2 79 .3 85 .0 89 .2 90 .6 71 .4 86 .9 83 .1 90 .2 75 .3 84 .1 C ol on -r ec tu m 15 3- 15 4 87 .0 96 .2 75 .6 93 .4 91 .6 83 .9 86 .8 92 .3 90 .3 93 .3 82 .6 82 .6 82 .7 90 .5 70 .5 77 .1 C ol on 15 3 90 .5 69 .8 69 .3 71 .1 70 .1 70 .1 81 .2 68 .3 75 .0 71 .4 63 .9 79 .3 52 .0 60 .5 R ec tu m 15 4 48 .6 97 .2 48 .8 84 .4 62 .6 77 .7 51 .5 82 .9 33 .3 50 .0 69 .6 66 .7 55 .6 83 .3 Li ve r 15 5 82 .1 50 89 .9 47 .5 90 .6 47 .5 80 .7 41 .2 66 .6 14 .3 53 .8 38 .9 85 .7 37 .5 53 .3 29 .6 G al lb la dd er 15 6 73 .3 91 .7 59 .7 93 .6 67 .5 81 .3 52 .2 85 .7 75 .0 85 .7 37 .5 10 0 70 .0 66 .7 40 .0 84 .6 P an cr ea s 15 7 97 .4 78 .7 83 .0 86 .6 79 .5 77 .4 82 .9 87 .2 10 0. 0 85 .7 10 0 66 .7 10 0. 0 60 .0 71 .4 52 .6 La ry nx 16 1 83 .3 62 .5 81 .4 64 .2 83 .5 68 .6 85 .0 63 .0 10 0. 0 10 0. 0 80 .0 80 .0 96 .4 79 .4 75 .0 65 .9 Lu ng 16 2 93 .8 89 .8 91 .6 89 .9 93 .7 92 .4 95 .4 95 .4 67 .6 88 .5 10 0. 0 94 .9 84 .6 91 .7 93 .3 91 .2 92 .3 86 .6 S ki n 17 2- 17 3 66 .7 80 .0 59 .3 90 .0 22 .2 10 0 50 .0 50 .0 44 .4 85 .7 M el an om a 17 2 90 .9 83 .3 76 .9 10 0 76 .7 88 .5 50 .0 50 .0 O th er s 17 3 46 .2 75 .0 46 .2 80 .0 44 .0 91 .7 15 .4 50 .0 B re as t-  17 4 92 .1 97 .5 87 .9 98 .6 92 .2 98 .7 91 .7 10 0 94 .1 88 .9 10 0. 0 10 0. 0 88 .0 95 .7 86 .7 98 .6 78 .8 10 0. 0 U te ru s 17 9, 18 0, 18 2 78 .0 86 .7 78 .0 81 .4 73 .7 90 .3 86 .0 88 .0 93 .0 82 .0 83 .3 b 62 .5 62 .5 68 .2 76 .9 62 .5 C er vi x 18 0 51 .7 88 .2 57 .6 97 .1 50 .0 93 .8 68 .0 94 .4 43 .2 86 .4 10 0. 0 50 .0 75 .0 10 0. 0 0. 0 0. 0 20 .0 50 .0 C or pu s 18 2 50 .0 83 .3 41 .9 88 .6 52 .6 45 .5 37 .5 85 .7 43 .9 82 .8 10 0. 0 10 0. 0 7. 1 33 .3 14 .3 33 .3 O va ry 18 3 82 .1 85 .2 70 .1 90 .1 71 .2 78 .7 71 .4 71 .4 83 .7 77 .9 10 0. 0 10 0. 0 36 .4 44 .4 58 .3 87 .5 P ro st at e 18 5 93 .2 84 .6 87 .6 81 .3 90 .8 91 .4 91 .4 85 .5 90 .9 76 .9 68 .8 84 .6 88 .2 65 .2 90 .0 33 .3 O th er g en ita l-  18 6- 18 7 0. 0 0. 0 70 .0 70 .0 77 .8 10 0. 0 50 .0 10 0 10 0. 0 10 0. 0 Te st ic ul ar 18 6 0. 0 10 0. 0 10 0. 0 60 .0 10 0. 0 B la dd er 18 8 77 .9 91 .4 76 .4 90 .2 87 .3 88 .7 74 .4 91 .4 10 0. 0 77 .8 50 .0 70 .0 63 .8 95 .0 58 .8 10 0. 0 K id ne y 18 9 75 .0 80 .0 79 .0 84 .5 80 .6 92 .1 58 .8 83 .3 10 0 66 .7 70 .0 77 .8 66 .7 25 .0 B ra in 19 1 96 .2 92 .6 95 .5 83 .6 94 .4 87 .9 10 0 84 .4 10 0 77 .7 91 .7 78 .6 En do cr in e G la nd s 19 3- 19 4 10 0. 0 71 .4 75 .0 75 .0 73 .7 10 0. 0 10 0 80 10 0. 0 80 .0 Th yr oi d 19 3 10 0. 0 75 .0 64 .7 78 .6 80 .0 10 0. 0 75 .0 10 0 10 0. 0 10 0. 0 Ill -d ef in ed tu m ou rs 19 5- 19 9 58 .2 55 .4 50 .6 30 .0 56 .5 51 .7 52 .6 42 .4 31 .6 30 .0 5. 8 23 .1 Ly m ph om as 20 0- 20 2 90 .2 83 .0 87 .0 77 .7 85 .7 91 .3 10 0. 0 10 0. 0 86 .7 a 92 .9 a 62 .5 76 .9 50 .0 50 .0 H od gk in 20 1 50 .0 50 .0 75 .0 85 .7 10 0. 0 40 .0 60 .0 75 .0 O th er s 20 0, 20 2 81 .6 75 .6 71 .9 85 .3 84 .8 90 .3 63 .6 77 .8 M ul tip le M ye lo m a 20 3 10 0. 0 94 .4 10 0. 0 92 .3 81 .3 92 .9 10 0. 0 10 0. 0 10 0. 0 10 0. 0 Le uk ae m ia 20 4- 20 8 92 .6 b 96 .2 b 96 .4 c 96 .4 c 89 .1 88 .2 10 0. 0 10 0. 0 10 0. 0 10 0. 0 10 0. 0 87 .5 95 .0 86 .3 85 .7 c 80 .0 c C R : c on fir m at io n ra te ; D R I: de te ct io n ra te . a In cl ud es IC D 2 00 -2 03 ; b O nl y ly m ph oi d ca se s w er e fo un d (I C D 2 04 ); c H ae m at op oi et ic a nd r et ic ul ar s ys te m ( IC D -O 1 69 ). R at es fr om r ev ie w ed s tu di es , t ho ug h in s om e ca se s D et ec tio n R at es ( D R ) an d C on fir m at io n R at es ( C R ) w er e ca lc ul at ed w ith d at a su pp lie d in th e pa pe rs . 48 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 Table 3. Accuracy of death certification for specific cancers in Spain according to Percy’s criteria (Percy 1981). Pooled analysis Well-certified Over-certified Under-certified Ill-certified (DR  80 and CR  80) (DR  80 and CR  80) (DR  80 and CR  80) (DR  80 and CR  80) Location ICD-9 DR CR Location ICD-9 DR CR Location ICD-9 DR CR Location ICD-9 DR CR Stomach 151 83 89 Oesophagus 150 87 78 Mouth & pharynx 140-149 59 85 Colon 153 72 70 Colon-rectum 153-154 83 90 Liver 155 85 45 Rectum 154 54 82 Gallbladder 156 58 79 Pancreas 157 84 80 Larynx 161 83 67 Skin 172-173 54 87 Corpus uterus 182 42 76 Lung 162 92 91 Melanoma 172 78 91 Ill-defined tumours 195-199 53 39 Breast- 174 90 98 Skin (non-melanoma) 173 42 80 L. Hodgkin 201 69 69 Uterus 179,180,182 82 83 Cervix uterus 180 51 91 Prostate 185 89 82 Ovary 183 74 81 Brain 191 96 85 Other genital- 186-187 69 82 Lymphomas 200-202 86 80 Testicular 186 78 88 Multiple Myeloma 203 96 94 Bladder 188 76 91 Leukaemia 204-208 93 93 Kidney 189 76 83 Endocrine Glands 193-194 79 83 Thyroid gland 193 76 89 Lymphomas, others 200,202 76 83 CR: confirmation rate; DR: detection rate. sible for the coding process. This change led to an im- provement in the quality of the information, which is re- flected in the downward trend in the proportion of ill-de- fined causes. The initial decline in the percentage of ill-defined causes was accompanied by an increase in the proportion of ill-defined tumours, which registered a less clear pattern. Nevertheless, it should be noted that, coinciding with the introduction of ICD-10 in Spain, 1999 witnessed an increase in these indicators, with the percentage of ill defined causes and ill defined tumours rising by 31% and 10% respectively over the previous year’s figures, followed by an apparent leve- lling-off. Interestingly, women registered higher values for these two indicators of bad certification, in all cases. When proportional mortality was computed using ad- justed rates, women continued to have worse results (data not shown). Discussion Though quality at a national level has not been stu- died, available data suggest that, overall, cancer death certificates in Spain possess an accuracy comparable to that reported for other industrialised countries5,20,21. Indirect estimations such as the proportion of ill-defined causes in Spain show similar percentages to those re- gistered by other developed countries22. The first Spanish study to address death certifica- te reliability was published in 198115. Specifically focu- sed on cancer death certificates, this study solely co- vered the Barcelona metropolitan area. Several authors 10 5 0 Pe rc e n ta ge 1980 1985 1990 1995 2000 % of ill-defined tumours/all tumours Women Both sexes Men % of ill-defined causes/all causes Women Both sexes Men Figure 3. Percentages of deaths due to ill-defined tumours and ill-defined conditions versus all-tumour and all-cause mortality. Trends for the period 1980-2002 by sex and for both sexes. subsequently studied the quality of death certificates in other parts of the country. In this paper, we summari- sed all available information to provide a global view of the quality of Spanish cancer-mortality statistics. In Spain, published quality estimators are basically drawn from regional studies, many of which are spon- sored or undertaken by Cancer Registries. Accordingly, it should be borne in mind that, despite the existence of national coding protocols, inferring quality indicators for the country, such as our pooled estimators, might also be problematic, since decentralisation of the coding pro- cess could cause inter-regional variability, and there are huge areas of the country where death certification qua- lity studies have not been conducted (fig. 2). Only Giménez et al3, in their study on a toxic-oil poisoned cohort, pro- vide national data, though their results could also be mis- leading as they refer to a cohort of sick people, subjec- ted to a thorough follow-up over time. The progressive increase in the number of Cancer Registries in the country might go some way towards having more representati- ve data about quality of cancer death certification in Spain in the future. Nevertheless, results from the different stu- dies were quite similar for most cancer sites. Compared to other causes of death, cancer (ICD 140- 208) seems to be well certified in Spain, with detection rates being as much as 9 points higher for all tumours than for all causes together, and confirmation rates over 20 points higher than for all causes11,12, which could be due to the fact that cancer is usually a well-characterised diag- nosis, and in most cases has histological confirmation. All-tumour detection rates ranged from 79.9 to 100 and the CRs exceeded 90%. Depending upon their re- sults, some studies have classified this broad category as well-certified3,11,13, while others have viewed tumours as being slightly underreported3,12. However, the per- centage of underreporting in Spain, as estimated by Gar- cía-Benavides et al11 and Cáffaro et al6, seems to be around 5-6%, which is comparable to international fi- gures20,23,24. Hence, global cancer mortality figures can be considered accurate and useful for estimating the bur- den of this group of diseases. As expected, when site misclassification was taken into account, agreement estimates were lower. All-site three-digit detection rates from categories I and II(a) stu- dies range from 64.8 to 100 and confirmation rates from 68.2 to 80.8. Based on these indicators, cancer could be deemed to be ill-certified according to Percy’s cri- teria. It is remarkable that, in general, Ruiz-Liso et al13 obtained better results than other studies. The CR range in category II(b) studies was similar (64.4-81%). The de- sign used in such studies excludes global false positi- ves, thus slightly overestimating this indicator. Accor- ding to three studies6-8, in which both correct and biased estimators were available, biased data were on avera- ge three points higher. In the USA5 and France20, CRs were slightly higher than in Spain (82.7 and 86%, res- pectively). Nevertheless, it should be noted that those studies belong to category II(b) and are also biased. If some problematic categories are grouped (this is the case of cervical –ICD 180–, corpus –ICD 182– and unspecified uterine cancer –ICD 179–; or colon –ICD 153– and rectal neoplasms –ICD 154–), all-site three- digit agreement rates improve. This can be seen in Ci- rera and Navarro7, where the proportion of agreement using three-digit ICD was close on 80%, and aggrega- tion of problematic locations raised it to 83%. A com- parable increase was previously described in the USA5 (4%) and in Ontario21 (6%). Analysis of specific anatomic locations shows that, in general, the main leading cancer sites are well cer- tificated. Thus, lung, colon-rectum (ICD 153-154), pros- tate, stomach, pancreas, female breast, uterus (ICD 179- 180,182) and brain cancer, as well as leukaemia, lymphomas, myeloma belong to this category. Together, they represented around 69% of all cancer deaths re- gistered in Spain in 200225. Nonetheless, it should be noted that colon and rectal cancers are respectively ill and undercertified unless they are considered together, since mutual misclassification of the two sites has been reported7,21. A similar situation can be observed with res- pect to uterus. Overall, this location has good accuracy rates, but cervix and corpus uterus are under –and ill– certified, respectively. Mortality due to uterus cancer in Spain registered a steady decrease since 1976, con- trasting with the slightly increasing trend in cervix mor- tality26, which has been explained mainly as a conse- quence of a reassignment of cases previously coded as «uterus non-specified»14. Nevertheless, if uterus is regarded as a single category, its certification has im- proved with time and, in more recent studies, achieves acceptable figures. Some other frequent locations, such as larynx, blad- der or ovary, which rank among the ten leading causes of cancer death in Spain, evince problems in certifica- tion. A certain degree of overreporting has been descri- bed for laryngeal cancer, due to misclassification of head and neck tumours6,8,18. Similarly, there is certain measu- re of overreporting for oesophageal cancer, mainly attri- butable to the inclusion of stomach cases6-8,18, as well as for liver, largely due to misclassification of gallbladder and ill-defined neoplasms6-8,13,18. Percy et al27 warned that in- clusion in ICD-9 code 155 of liver cancer that was not specified as primary or secondary, was a possible cause of misclassification for these tumours, as it might lead to some coders registering secondary liver cancers under this category. Furthermore, there have been reports of underes- timation of urinary bladder cancer, erroneously certified as prostate neoplasm6-8,13,17,18. It should, however, be noted that, even with this underestimation, Spain had the second highest bladder mortality rate within the Eu- ropean Union in 200026. In addition, some Spanish aut- 49 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 hors have reported undernotification of skin cancers due to lack of information on their anatomic location6, the- reby implying their inclusion as ill-defined and unspe- cified tumours (ICD-9 195, 199). Accuracy of ovary-neoplasm certification seems to vary widely among studies, though it can be regar- ded as undercertified according to pooled estima- tors. While some reported cases of death due to ova- rian cancer were really due to abdominal or uterine ne- oplasms, in some studies7,8,14, «unspecified uterus tu- mours» would appear to include some ovarian cancers as well as tumours of the cervix and endome- trium6,8,14,17,18. Ill-defined tumours were badly certified according to Percy’s criteria. Cirera and Navarro7 reported there was clinical information that would allow for almost half of these tumours to be included in other categories. The selfsame problem has been described in other coun- tries, such as Brazil28. Our results show that all cancer sites classified as well certified in Spain have been reported as such in the USA by Percy et al5. However, this author also en- countered good agreement rates for oesophagus, blad- der, gallbladder, thyroid gland and kidney, locations that did not display a good standard in Spanish studies. In Ontario, Canada, Reynolds21 similarly observed good DRs and CRs for all those neoplasms classified as well- certified in Spain, with the exception of pancreas, and also found high rates for cervix uterus, bladder, kidney, ovary and endocrine glands. In France, Laplanche et al20 reported CRs of over 80% for breast, colon-rectum, lung and pancreas, values similar to Spanish figures. In contrast, they found CRs of under 80% for head and neck and cervix, tumours which in Spain register good CRs. Stomach cancer was also well classified in Bra- zil29 and Italy30. In international comparisons, however, a relevant factor to be considered are differences in in- ternational coding practice, since divergences up to 30% have been described by Percy and Muir31 among wes- tern countries using the ICD-9. With respect to accuracy of certification, Percy men- tioned the influence of several factors such as age, sex, geographic area, presence of an autopsy or place of death5. In Spanish studies, a lower quality has been re- ported for older ages and for women6-8,18. These sex-re- lated differences are reflected in the percentage of ill-de- fined tumours and ill-defined causes, which are regularly higher in females and could in part be due, both to gynaecological neoplasms18 and to the older age of women. Insofar as place of death is concerned, a lower quality of death certification has been associa- ted with death at home6,7, though other authors have fai- led to find any difference11. Finally, the quality of certi- fication has been shown to be slightly lower in rural areas18. As Navarro et al17 points out, clinical information is ne- eded to validate death certificates, thus implying the ex- clusion of those cases where this information is not avai- lable. Death certificates lacking complementary clinical or anatomo-pathological data could be of worse quality, as they probably include more home deaths. Navarro found that death certificates excluded for this reason belonged to subjects who were, on average, seven years older than those included in her study. All this may well lead to ove- restimation of the quality reported in many studies. Several strategies have been proposed to motivate and improve physicians’ certification28 such as a periodic assessment of coding practices along with the educa- tion and motivation of medical students and physicians. In Spain, several Regional Health Authorities imple- mented specific workshops that showed their efficacy in enhancing death certificate quality indicators32. Yet, these interventions are questioned by Swift’s study33, which failed to find significant changes in the state of certification after the introduction of formal education into the medical syllabus. A further point of discussion is the effect of the in- troduction of the ICD-10 on the quality of mortality data. To date, we have been unable to find any validation study in Spain covering the ICD-10 coding period. In 1999, Ruiz et al34 compared ICD-9 and ICD-10 coding in a huge sample of Spanish death certificates. They reported that, whereas ill-defined condition figures increased almost a 14% with the use of this latest version, neoplasms se- emed quite stable. In contrast, our data indicate that the ICD-10 effect might be greater than thought, and that it has also affected tumours coding. This could suggest a worsening in the quality of data, and careful survei- llance is thus called for. In conclusion, the quality of cancer death certifica- tion in Spain for all tumours and all main sites has im- proved over the last two decades and can be conside- red comparable to internationally published data. Thus, mortality data constitute a valid indicator to estimate the burden of cancer. However, for some locations, such as the oesophagus or bladder, death certificate informa- tion should be approached with caution. Misclassifica- tion may generate problems for studying mortality trends and planning future needs. It should be noted that, in general, most available information on the qua- lity of death certification reflects the situation from 1970 to 1990, when the ICD-9 was in use. The relatively re- cent introduction of the ICD-10 may have affected qua- lity indicators and should thus be carefully monitored. Finally, our results point to the need to improve death certification in the case of Spanish women. Acknowledgements The work of V. Carvajal was supported by the Carlos III Institute of Health (Grant No. 03/0007). The work of B. Suá- rez was funded by the Network of Epidemiology and Public 50 Pérez-Gómez B et al. Accuracy of cancer death certificates in Spain: a summary of available information Gac Sanit. 2006;20(Supl 3):42-51 51 Pérez-Gómez B et al. 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