Esophageal cancer incidence and mortality in China, 2009
Original Article

Esophageal cancer incidence and mortality in China, 2009

Wanqing Chen1, Yutong He2, Rongshou Zheng1, Siwei Zhang1, Hongmei Zeng1, Xiaonong Zou1, Jie He1

1National Office for Cancer Prevention and Control & National Central Cancer Center, Beijing, China; 2Department of Flow Cytometry, The Fourth Hospital of Hebei Medical University, Shijiazhuang, China

Corresponding to: Wanqing Chen. No.17 Pan-Jia-Yuan South Lane, Chaoyang District, Beijing, 100021, China. Email: chenwq@cicams.ac.cn.

Objective: Esophageal cancer incident cases and deaths in 2009 were retrieved from national database of population based cancer registry to describe esophageal cancer burden in registration areas.

Methods: In 2012, 104 population-based cancer registries reported cancer incidence and mortality data of 2009 to Chinese National Central Cancer Registry. Total 72 registries’ data met the national criteria to be pooled and analyzed. The crude incidence and mortality rates of esophageal cancer were calculated by age, gender and area. China sensus in 1982 and Segi’s world population were applied for age standardized rates.

Results: The crude incidence of esophageal cancer ranked fifth in all cancer sites with rate of 22.14/100,000 (30.44/100,000 for male and 13.64/100,000 for female, 14.21/100,000 in urban and 38.44/100,000 in rural). Age-standardized rates by China population (CASR) and World population (WASR) for incidence were 10.88/100,000 and 14.81/100,000 respectively. The crude mortality of esophageal cancer ranked fourth in all cancer sites with rate of 16.77/100,000 (23.29/100,000 for male and 10.11/100,000 for female, 10.59/100,000 in urban and 29.47/100,000 in rural). The CASR and WASR for mortality were 7.75/100,000 and 10.76/100,000 respectively. For both of incidence and mortality, the rates of esophageal cancer were much higher in males than in females, in rural areas than in urban areas. The overall age-specific incidence and mortality rates showed that both rates were relatively low before 45 years old, and then gradually increased, reaching peak in age group of 80-84.

Conclusions: The burden of esophageal cancer remained high in China, especially for males in rural areas. Effective prevention and control action, such as health education, nutrition intervention and screening should be enhanced in the future.

Keywords: Esophageal cancer; incidence; mortality; cancer registry; China

Submitted Dec 07, 2012. Accepted for publication Jan 08, 2013.

doi: 10.3978/j.issn.2072-1439.2013.01.04

Introduction

Esophageal cancer is the fourth most common cause of cancer death, while the mortality rate was 15.21 per 10,000 (11.19% of the total cancer death) according to the data from The Third National Causes of Death Sampling Survey [2004-2005] (1). Esophageal cancer mortality rates have decreased somewhat over the past three decades with the improvement of its socio-economic status and lifestyle (1). However, esophageal cancer remains prevalent in rural areas and in males (2). Accurate population-based statistics of esophageal cancer are the basis for policy makers and researchers for effective cancer prevention and control.

Material and methods

Data source

National Central Cancer Registry (NCCR) of China was the governmental authority affiliated to Bureau of Disease Control, Ministry of Health, in charge of cancer data collection, evaluation and publication from population-based cancer registries nationwide. All new cancer cases diagnosed in 2009 were reported to cancer registries from all hospitals, community health centers and the other departments, including centers of township medical insurance and the New-type Rural Cooperative Medical System. The death record database was linked and matched with cancer registration database for identifying cancer deaths and supplementing missed cases.

Until June 1st, 2012, there were 104 cancer registries (46 cities and 58 counties) from 27 provinces reporting cancer registration data to NCCR. The overall population coverage was 109,476,347, accounting for 8.20% of the whole population. The cancer registries coded cancer site and histology by the International Classification of Diseases (ICD) for Oncology, third edition and ICD-10. Invasive cases of esophageal cancer (C15) were retrieved from the overall cancer database and analyzed. Demographic information was provided by national statistics bureau.

Quality control

Based on “Guideline of Chinese Cancer Registration” and the standard of data inclusion in “Cancer Incidence in Five Continents Volume IX”, cancer registration data were evaluated by the quality indicators of proportion of morphological verification (MV%), percentage of cancer cases identified with death certification only (DCO%) and mortality to incidence ratio (M/I) (3-5). Generally, data with DCO% less than 20%, an overall MV% of more than 55%, and M/I between 0.55-0.95 were considered acceptable.

Statistical analysis

Crude incidence and mortality rates of esophageal cancer were calculated stratified by sex, area and for 19 age groups (0-, 1-4, 5-9, … 80-84, 85+ years). China sensus in 1982 and Segi’s world population were applied for age standardized rates. The cumulative risk of developing or dying from cancer before 75 years (in the absence of competing causes of death) was calculated and presented as a percentage. Software including MS-FoxPro, MS-Excel, IARCcrgTools issued by IARC and IACR were used for data checkup. SAS software was used to calculate the incidence and mortality rates.

Results

A total of 72 population-based cancer registries with qualified cancer statistics were included in the study. The population covered by these cancer registries was 85,470,522, including 43,231,554 males and 42,238,968 females, accounting for 6.40% of the whole population. Among them, 31 registries were from urban areas, covering a total of 57,489,009 population. And 41 registries were from rural areas, covering a total of 27,981,513 population. The MV%, DCO%, and M/I ratio for the national pooled data were 50.76%, 4.88% and 0.85 respectively. In urban areas, the MV%, DCO%, and M/I ratio were 55.03%, 4.71% and 0.86 respectively. In rural areas, they were 38.68%, 5.35% and 0.84. There were 18,924 new cases diagnosed with esophageal cancer in 2009. Of them, 13,161 were males and 5,763 were females. The number of overall cancer deaths was 14,337, including 10,067 males and 4,270 females. The detailed information for the covering population, incident cases and the cancer deaths of esophageal cancer in each cancer registry was shown in Table 1.

Table 1

Population, number of new cases and deaths of esophageal cancer in cancer registries in 2009.

Registry Urban =1 Rural =2 Population
New cancer cases
Cancer death
Both Male Female Both Male Female Both Male Female
Beijing 1 7,645,186 3,859,586 3,785,600 676 532 144 586 449 137
Qianxi 2 361,312 182,138 179,174 90 78 12 48 40 8
Shexian 2 394,944 205,168 189,776 328 221 107 273 181 92
Cixian 2 634,333 322,621 311,712 688 407 281 506 311 195
Baoding 1 948,612 478,051 470,561 103 73 30 100 59 41
Yangquan 1 683,165 346,023 337,142 153 103 50 126 85 41
Yangcheng 2 383,165 192,119 191,046 357 226 131 239 159 80
Chifeng 1 1,203,006 613,725 589,281 72 62 10 57 47 10
Shenyang 1 3,497,815 1,722,976 1,774,839 331 284 47 247 208 39
Dalian 1 2,266,224 1,136,772 1,129,452 214 193 21 145 130 15
Zhuanghe 2 915,660 461,826 453,834 61 56 5 41 35 6
An’shan 1 1,471,775 731,916 739,859 120 91 29 92 84 8
Benxi 1 955,409 475,113 480,296 99 89 10 70 61 9
Dandong 1 767,011 378,794 388,217 48 39 9 39 34 5
Donggang 2 640,853 323,798 317,055 34 23 11 34 29 5
Dehui 2 943,395 479,486 463,909 28 21 7 19 13 6
Yanji 2 440,957 215,260 225,697 23 21 2 17 17 0
Daoli District,Harbin 1 713,264 351,071 362,193 69 62 7 39 35 4
Nangang District,Harbin 1 1,020,233 508,921 511,312 56 44 12 53 47 6
Shangzhi 2 616,046 314,864 301,182 51 43 8 27 24 3
Shanghai 1 6,181,334 3,084,496 3,096,838 504 351 153 521 355 166
Jintan 2 545,000 262,407 282,593 283 199 84 223 161 62
Suzhou 1 2,392,087 1,183,716 1,208,371 549 382 167 318 231 87
Haian 2 936,785 463,612 473,173 708 445 263 560 370 190
Qidong 2 1,114,951 548,805 566,146 133 89 44 136 90 46
Haimen 2 1,016,228 501,407 514,821 191 134 57 166 114 52
Lianyungang 1 886,862 452,358 434,504 141 106 35 109 76 33
Donghai 2 1,117,858 579,751 538,107 285 219 66 240 182 58
Guanyun 2 1,015,229 534,502 480,727 301 200 101 280 198 82
Chuzhou District, Huai’an 1 1,174,877 609,088 565,789 1,120 662 458 758 435 323
Huaiyin District, Huai’an 1 900,027 465,502 434,525 624 419 205 368 245 123
Xuyi 2 759,450 388,180 371,270 398 275 123 235 154 81
Jinhu 2 352,292 176,689 175,603 216 125 91 165 102 63
Sheyang 2 965,817 494,682 471,135 444 280 164 364 228 136
Jianhu 2 805,465 410,369 395,096 527 305 222 412 276 136
Dafeng 2 724,147 363,326 360,821 348 224 124 303 204 99
Yangzhong 2 272,046 134,758 137,288 269 156 113 249 139 110
Taixing 2 1,128,840 613,199 515,641 615 386 229 518 336 182
Hangzhou 1 6,753,509 3,403,893 3,349,616 890 759 131 660 547 113
Jiaxing 1 509,367 253,819 255,548 64 55 9 54 45 9
Jiashan 2 382,475 189,692 192,783 67 49 18 64 52 12
Haining 2 653,957 322,969 330,988 74 57 17 63 52 11
Shangyu 2 771,321 383,462 387,859 139 128 11 135 119 16
Xianju 2 490,070 255,438 234,632 155 96 59 148 94 54
Feixi 2 858,895 449,882 409,013 397 299 98 220 162 58
Maanshan 1 633,477 323,834 309,643 131 98 33 115 89 26
Tongling 1 433,545 221,375 212,170 104 86 18 92 75 17
Changle 2 673,717 355,091 318,626 69 51 18 52 42 10
Xiamen 1 1,160,135 583,873 576,262 322 260 62 240 176 64
Zhanggong District, Ganzhou 1 420,759 212,159 208,600 36 32 4 31 25 6
Linqu 2 817,857 417,434 400,423 132 107 25 105 75 30
Wenshang 2 762,828 388,454 374,374 464 314 150 316 194 122
Feicheng 2 733,501 358,739 374,762 731 501 230 504 345 159
Yanshi 2 602,266 306,192 296,074 237 128 109 167 97 70
Linzhou 2 1,080,241 557,392 522,849 860 459 401 605 361 244
Xiping 2 858,002 434,899 423,103 260 145 115 190 108 82
Wuhan 1 4,832,174 2,484,622 2,347,552 435 337 98 350 288 62
Yunmeng 2 524,801 261,237 263,564 41 37 4 29 26 3
Hengdong 2 713,458 373,923 339,535 35 25 10 21 15 6
Guangzhou 1 3,968,216 2,014,580 1,953,636 302 246 56 249 208 41
Sihui 2 413,363 211,351 202,012 31 25 6 21 17 4
Zhongshan 1 1,468,391 732,333 736,058 140 127 13 120 110 10
Liuzhou 1 1,038,208 533,050 505,158 53 41 12 37 32 5
Fusui 2 444,332 236,000 208,332 17 15 2 12 11 1
Jiulongpo District, Chongqing 1 798,618 402,961 395,657 73 58 15 71 54 17
Qingyang District,Chengdu 1 534,701 277,154 257,547 70 55 15 52 44 8
Ziliujing District,Zigong 1 357,600 179,873 177,727 62 54 8 41 33 8
Yanting 2 610,103 316,499 293,604 573 366 207 478 306 172
Jingtai 2 233,609 119,953 113,656 21 19 2 17 15 2
Liangzhou District,Wuwei 1 990,583 524,276 466,307 493 367 126 286 223 63
Xining 1 882,839 439,175 443,664 113 88 25 64 50 14
Xinyuan 2 271,944 138,895 133,049 76 52 24 45 33 12
Total 85,470,522 43,231,554 42,238,968 18924 13161 5763 14337 10067 4270

Incidence

The crude incidence rate for esophageal cancer was 22.14/100,000 in 2009, accounting for 7.74% of overall new cancer cases. It ranked fifth most common cancers in all cancer sites following cancers of lung, stomach, colon-rectum and liver. The age-standardized rates by China (CASR) population and by World population (WASR) were 10.88/100,000 and 14.81/100,000, respectively. Among the patients aged 0-74, the cumulative incidence rate was 1.88%.

Esophageal cancer occurred more often among men than women. For males, esophageal cancer was the fifth most common cancer and the crude incidence rate was 30.44/100,000, whereas the CASR and WASR were 15.62/100,000 and 21.27/100,000 respectively. For females, esophageal cancer was the sixth most common cancer and the crude incidence rate was 13.64/100,000, where as the CASR and WASR were 6.27/100,000 and 8.59/100,000. The crude incidence rate in urban areas (ranked sixth most common cancer) was 14.21/100,000 and it was lower than that in rural areas (ranked the third most common cancer with incidence rate of 38.44/100,000). After age standardization, incidence rate in urban (6.65/100,000 for WASR) was still much lower than that in rural (20.57/100,000 for WASR) (Table 2).

Table 2

Esophagus incidence by sex and area in registration areas in 2009.

Area    Sex New cases Incidence (1/105)
CASRa (1/105) WASRb (1/105) Cumulative rate 0-74 (%) Rank
Rate %
All areas    Both 18,924 22.14 7.74 10.88 14.81 1.88 5
   Male 13,161 30.44 9.57 15.62 21.27 2.69 5
   Female 5,763 13.64 5.39 6.27 8.59 1.09 6
Urban    Both 8,167 14.21 4.68 6.65 9.07 1.13 6
   Male 6,155 21.24 6.43 10.46 14.25 1.77 5
   Female 2,012 7.06 2.56 2.99 4.13 0.51 11
Rural    Both 10,757 38.44 15.38 20.57 27.95 3.57 3
   Male 7,006 49.18 16.78 27.22 37.05 4.69 3
   Female 3,751 27.31 13.31 13.97 19.03 2.44 3

Age-specific incidence rates of esophageal cancer for both genders and areas were compared. Overall, the age-specific incidence rate was relatively low in subjects before 45 years old. However, the rate was dramatically increasing for patients after 45 years old, reaching peak for subjects of 80-84 years old (129.26/100,000). For males, subjects in the age group of 85 years or more had highest age-specific rates, whereas for females, subjects in the age group of 80-84 years old had highest rates. Generally, esophageal cancer among males had a higher age-specific incidence rate than those among females except for those in small age groups (<30 years old). Similarly, the age-standardized esophageal cancer rates in rural were generally higher than that in urban areas except for subjects in small age groups (Table 3, Figure 1).

Table 3

Age-specific incidence rates of esophageal cancer in cancer registration areas in 2009 (1/105).

Age group All areas
Urban
Rural
Both Male Female Both Male Female Both Male Female
all 22.14 30.44 13.64 14.21 21.24 7.06 38.44 49.18 27.31
0- 0.32 0.31 0.34 0.52 0.50 0.55 0.00 0.00 0.00
1- 0.04 0.07 0.00 0.00 0.00 0.00 0.10 0.18 0.00
5- 0.03 0.00 0.06 0.00 0.00 0.00 0.07 0.00 0.14
10- 0.02 0.04 0.00 0.00 0.00 0.00 0.05 0.10 0.00
15- 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
20- 0.04 0.08 0.00 0.04 0.07 0.00 0.05 0.09 0.00
25- 0.10 0.11 0.08 0.06 0.08 0.04 0.18 0.18 0.18
30- 0.29 0.30 0.27 0.23 0.23 0.24 0.38 0.42 0.34
35- 1.16 1.90 0.41 0.76 1.27 0.25 1.96 3.15 0.74
40- 3.75 5.97 1.49 2.46 4.29 0.59 6.36 9.33 3.31
45- 10.81 17.60 3.77 7.79 13.89 1.44 17.62 26.04 8.98
50- 26.87 42.16 11.11 17.67 31.03 3.95 50.30 70.23 29.48
55- 47.05 69.05 24.91 28.44 46.92 10.18 91.51 120.35 61.21
60- 76.78 108.85 44.60 42.92 68.08 18.27 149.91 193.69 103.68
65- 95.43 132.43 59.28 58.17 87.47 30.36 169.64 218.28 119.39
70- 114.04 159.64 72.12 67.14 101.43 36.16 226.79 295.38 161.08
75- 120.96 161.26 85.15 74.1 103.44 47.79 242.67 314.20 180.66
80- 129.26 175.08 92.90 86.2 119.83 58.86 238.22 321.77 175.85
85- 105.19 163.46 68.32 74.91 122.02 44.34 184.20 277.87 128.74
Figure 1 Age-specific incidence rate of esophageal cancer in cancer registration areas in 2009 (1/105).

Mortality

The crude mortality rate for esophageal cancer was 16.77/100,000 in 2009, accounting for 9.29% of cancer deaths in 2009. The CASR and WASR for mortality were 7.75/100,000 and 10.76/100,000, respectively. Among the patients with age of 0-74, the cumulative rate was 1.30%.

The mortality rate of esophageal cancer was much higher in males than in females. For males, the crude rate, CASR and WASR were 23.29/100,000, 11.42/100,000, and 15.86/100,000. For females, the crude rate, CASR and WASR were 10.11/100,000, 4.22/100,000 and 5.96/100,000. In urban areas, the crude rate, CASR and WASR were 10.59/100,000, 4.65/100,000 and 6.47/100,000. In rural areas, they were 29.47/100,000, 14.91/100,000 and 20.69/100,000, lower than those in urban areas (Table 4).

Table 4

Cancer mortality of esophageal cancer in cancer registration areas in 2009.

Area      Sex Deaths Mortality (1/105)
CASR (1/105) WASR (1/105) Cumulative rate 0-74 (%) Rank
Rate    (%)
All areas     Both 14,337 16.77 9.29 7.75 10.76 1.30 4
    Male 10,067 23.29 10.39 11.42 15.86 1.91 4
    Female 4,270 10.11 7.44 4.22 5.96 0.70 6
Urban     Both 6,090 10.59 5.82 4.65 6.47 0.75 5
    Male 4,580 15.80 7.07 7.39 10.27 1.19 5
    Female 1,510 5.30 3.80 2.04 2.91 0.33 7
Rural     Both 8,247 29.47 16.57 14.91 20.69 2.52 4
    Male 5,487 38.51 17.06 20.57 28.55 3.45 4
    Female 2,760 20.09 15.68 9.39 13.16 1.57 3

The mortality trend for esophageal cancer in different age groups was similar to the trend of incidence. Both for males and females, in urban and in rural, the mortality reached peak for subjects of 80-84 years old. (Table 5, Figure 2).

Table 5

Age-specific mortality of esophageal cancer in cancer registration areas in 2009 (1/105).

Age group All areas
Urban
      Rural
Both Male Female Both Male Female Both Male Female
all 16.77 23.29 10.11 10.59 15.80 5.30 29.47 38.51 20.09
0- 0.16 0.00 0.34 0.26 0.00 0.55 0.00 0.00 0.00
1- 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
5- 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
10- 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
15- 0.04 0.07 0.00 0.06 0.11 0.00 0.00 0.00 0.00
20- 0.03 0.05 0.00 0.04 0.07 0.00 0.00 0.00 0.00
25- 0.10 0.14 0.06 0.06 0.04 0.08 0.18 0.35 0.00
30- 0.12 0.12 0.12 0.14 0.14 0.14 0.08 0.08 0.09
35- 0.61 0.84 0.38 0.47 0.61 0.33 0.90 1.29 0.49
40- 1.96 2.94 0.95 1.31 2.23 0.38 3.26 4.38 2.12
45- 5.79 9.69 1.75 4.51 8.19 0.68 8.68 13.11 4.13
50- 15.11 24.63 5.29 10.83 19.52 1.91 26.01 37.52 13.98
55- 28.29 43.14 13.35 16.39 27.46 5.45 56.72 79.47 32.82
60- 46.88 69.08 24.60 25.25 42.34 8.51 93.59 124.73 60.72
65- 67.54 99.24 36.57 39.04 59.78 19.35 124.32 174.58 72.37
70- 92.88 131.15 57.71 52.62 78.23 29.48 189.69 254.54 127.54
75- 116.43 165.97 72.40 71.59 106.39 40.37 232.88 323.57 154.27
80- 145.31 200.47 101.54 86.70 127.31 53.67 293.60 394.67 218.17
85- 139.91 207.10 97.39 96.26 151.22 60.58 253.82 361.38 190.12
Figure 2 Age-specific mortality of esophageal cancer in cancer registration areas in 2009 (1/105).

Discussion

Cancer registry annual report provides updated cancer statistics in cancer registration areas in China (6-8). This paper analyzed incidence and mortality rates of esophageal cancer in 2009 of China, based on 72 population-based cancer registries’ data. Data shows that the crude incidence and mortality rate of esophageal cancer in registration areas were 22.14/100,000 and 16.77/100,000. The age-standardized incidence and mortality rates by World population were 14.81/100,000 and 10.76/100,000. Esophageal cancer was more common in males than in females, in urban areas than in rural areas. The most recent cancer statistics on esophageal cancer might provide basic information for esophageal cancer prevention and control.

Esophageal cancer retains its status of top 4th leading cause of cancer deaths and the fifth most common diagnosed cancer in China in 2009. The incidence rate of esophageal cancer relatively increased compared the data in 2003-2007 (19.34 per 10,000) (9). The time trend shown that incidence rates of esophageal cancer had been increasing, however, after age standardization, it kept decreasing in recent 10 years (10). Aging population is a major cause for the increasing burden of esophageal cancer in China and incident cases is predicted to increase (10).

Esophageal cancer is the result of both effect of environmental factors, and lifestyle is one of the most important influencing factors (11-16). However, the exact mechanism is still not clear. The risk factors of esophageal cancer are discrepant in different countries and regions. For example, in developed country smoking, alcohol drinking and Barrett esophagitis are main risk factors (17-20), and in developing country nitrosamine, mold pollution, lack of vitamin, unhealthy lifestyles and smoking are main risk factors (14). If the genetic background can not be changed, change the bad dietary habits and behavior patterns are the most effective prevention of esophageal cancer. Hence, we should carry out health education in population in the long run, and appeal keeping away from the risk factors of esophageal cancer.

Esophageal cancer has very poor prognosis because most tumors are asymptomatic until at advanced stage which are un-resectable with the intention of curing the patient. Promising results have been reported that screening with use of endoscopy may improve prognosis from esophageal cancer (21). It is expected that through primary and secondary prevention, the prevalence of the disease may be controlled in the future.

NCCR is the authoritative source of information on cancer incidence and mortality in China. NCCR collects and publishes these statistics from population-based registries. The population coverage is increasing year by year. Since 2009, the ministry of health built up more cancer registries and provided specific funding to support the development of cancer surveillance. Until the end of 2012, there were 222 cancer registries around China, covering 14% of the whole population. Notably, the new built-up cancer registries need at least 5-year time to ensure data quality and reliability.

The data provided here are the most up-to-date data on incidence and mortality, reflecting the only available population-based information on esophageal cancer of China. In our study, urban population coverage took great part in the overall population, therefore, the representativeness of the data needs to be explained with caution (22). Chinese government is still making effort to improve the quality of the cancer registration data especially in rural areas. The accuracy and representativeness of the population-based cancer statistics would be better in the future.

Acknowledgements

All staff from local cancer registries that have made a great contribution for providing their cancer registration database was acknowledged.

Disclosure: The authors declare no conflict of interest.

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Cite this article as: Chen W, He Y, Zheng R, Zhang S, Zeng H, Zou X, He J. Esophageal cancer incidence and mortality in China, 2009. J Thorac Dis 2013;5(1):19-26. doi: 10.3978/j.issn.2072-1439.2013.01.04

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