Disability-adjusted life years and the trends of the burden of colorectal cancer: a population-based study in Shanghai, China during 2002 to 2016 : Chinese Medical Journal

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Disability-adjusted life years and the trends of the burden of colorectal cancer: a population-based study in Shanghai, China during 2002 to 2016

Zhong, Wei1; Chen, Liping2; Li, Xiaopan3,4; Chen, Yichen4; Zhang, Yao1; Guo, Canjie1; Shen, Yufeng1; Chen, Huimin1

Editor(s): Ni, Jing

Author Information
Chinese Medical Journal: October 04, 2022 - Volume - Issue - 10.1097/CM9.0000000000002064
doi: 10.1097/CM9.0000000000002064



Colorectal cancer (CRC) has been the third most common cancer worldwide and caused significant burden to society, especially for developed countries.[1] However, with the introduction and uptake of screening and sufficient access to treatment, the incidence and mortality in high-income countries have shown a slower growth or even a trend overturn.[2,3] In contrast, in developing countries, recent years have witnessed a rapid rise in the burden of CRC, which is widely believed to be associated with urbanization, agin.g population, and the adoption of a Westernized diet.[4,5]

In China, CRC is one of the top five common cancers among men and women.[6] According to the study on epidemiological trends in CRC, from 2003 to 2011, the CRC incidence increased from 12.8 to 16.8 per 100,000, and the mortality rate attributable to CRC increased from 5.9 to 7.8 per 100,000.[7] Moreover, the burden of CRC has shown vast geographic disparities; the more developed the region is, the more CRC cases there are. As a microcosm of China, Shanghai, where the CRC incidence has been approaching the level of developed countries, also witnessed the huge impact of CRC on society.[7,8]

The Chinese-government-sponsored CRC screening programs have been carried out in urban China.[9,10] Shanghai is among one of the cities that made the earliest attempts. The community-based CRC screening program in Shanghai was launched in 2013, and up to investigation deadline (December 31, 2016), Shanghai has completed two rounds of the screening. Residents aged 50 to 74 years were enrolled as the target population in this program and were screened for CRC by using fecal occult blood testing every 3 years. Since the program is provided as a part of essential public health services, individuals out of the target age range, generally those aged >75 years, were also included in this screening program if they requested participation. After the first two rounds of the program, a total of 444,106 effective primary screenings were made. In our previous study, we reported basically the performance of the large community-based CRC screening program implemented in Shanghai.[11] However, the burden of CRC, especially disability-adjusted life years (DALYs), in Shanghai for recent decades are still not clear. So, in this study, we aimed to exhibit the trends in age-standardized rates (ASRs) of incidence, mortality, and importantly, DALYs of CRC and explore potential changes in the temporal trends of the CRC burden in Shanghai from 2002 to 2016.


Ethical approval

No human participants were involved in the research. The study used secondary data. The ethics approval was obtained from the Ethical Committee at Fudan University School of Public Health (No. IRB#2016-04-0586).

Data sources

Information about CRC for the entirety of Shanghai several decades ago was generally unavailable. Instead, we used information from Pudong New Area, a representative district of Shanghai, which accounts for one-fourth of the population and one-third of the GDP (Gross Domestic Product) of Shanghai. Administrative data from Pudong New Area has been considered as the representative for Shanghai.[12]

The numbers of new CRC diagnoses and cancer-related deaths reported during the period 2002 to 2016 were obtained from the Cancer Registry of Shanghai, Pudong New Area. The population demographics were obtained from the Statistics Bureau and the Public Security Bureau of Pudong New Area. The quality of the data from these sources was checked and validated periodically by the local Centers for Disease Control and Prevention in compliance with standard guidelines.[13]

Study design and samples

We conducted this study to exhibit the age-standardized incidence, mortality, and DALYs of CRC and explore potential changes in the temporal trends of the CRC burden in Shanghai during 2002 to 2016. Study design and samples have been described elsewhere.[11] In short, the target population was 1,092,444 and the total number of invitations was 1,262,214. After the first two rounds of the program, a total of 444,106 effective primary screenings were made. The study was approved by the Centers for Disease Control and Prevention of Shanghai Pudong New Area. Not all data involved in this study are publicly available.

Statistical analysis

The ASR of incidence and mortality were obtained according to Segi world standard population, cancer mortality for selected sites in 24 countries (Sendai, Japan 1960). DALYs are the sum of years of life lost due to premature mortality (YLLs) and years lived with disability (YLDs). The relative contribution of YLLs to DALYs was substantially larger than that of YLDs and substantially increased as age increases. DALYs were calculated using DisMod (version 1.05, World Health Organization, Geneva) and expressed as cases per 1000 persons. During the calculation, the values of disability weights that we used were from the Global Burden of Diseases Study 2010,[14] and the standard life expectancy at birth values were based on West Level 26.[15] All the above measures for disease burden were first calculated for the whole population and then stratified by genders and age groups (<50 years, 50-74 years, and >74 years).

To explore potential changes in the temporal trends of the CRC burden, we performed joinpoint analyses by using the Joinpoint Trend Analysis software (version 4.04, National Cancer Institute, USA), thus enabling expression of trends as an annual percent change (APC). The program reported the minimum number of joinpoints necessary to fit the data best with piecewise linear regression models. A Monte Carlo Permutation method was used to test the significance of the trend over a segment.[16]Z-test was used to assess whether the APC was statistically different from zero. Terms of “increase” or “decrease” were used to describe statistically significant (P < 0.05) APC, while “stable” was used for not statistically significant trends. All statistical analyses were two-sided and performed using the Statistical Package for the Social Sciences software, version 16.0 (SPSS, Inc., Chicago, IL, USA). Statistical significance was set at P < 0.05.


ASR of incidence

As shown in Figure 1, the ASR of CRC incidence was 21.57 in 2002, jumped to a peak of 25.88 in 2013, and then fell back to 19.84 per 100,000 persons in 2016. The ASRs of incidence for men were always higher than that for women. A widening gender gap over the study period was also observed.

Figure 1:
Trends in ASR mortality in Pudong New Area, Shanghai (2002–2016). ASR: Age-standardized rates.

Results from the joinpoint analyses [Table 1] suggested that the increasing trend of ASR incidence prior to 2014 was halted: the overall ASR incidence increased by 0.79% (P < 0.05) per year during 2002 to 2014 and became stable during 2014 to 2016; the significant increasing trend for males (1.75% per year) also disappeared after 2014. For females, the trend was stable during 2002 to 2014, but we observed a significant decreasing trend (5.77% per year, P < 0.050) during 2014 to 2016 [Table 1]. Based on the fact that there was a 0.43% increase (P < 0.001) of ASR incidence during 2002 to 2012, a hypothetical trend was established to predict the change of ASR incidence (2001–2016) without the screening begun in 2013. We found an intersection between hypothetical trend and temporal trend in joinpoint regression [Supplementary Figure 1, https://links.lww.com/CM9/A988], which was mainly attributed to the CRC screening program launched in 2013. Moreover, Table 1 indicated the changes of the incidences were mainly driven by individuals aged 50 to 59 years and those >74 years. We observed that the pre-existing increasing trends disappeared in 2014 for both groups. For the other two age groups we examined, the incidence increased at a steady rate of 1.23% (P < 0.050) per year for those <50 years old, and the incidence were generally stable over the whole study period for those aged 60 to 74 years [Table 1].

Table 1 - Joinpoint analyses of CRC age-specific incidence trends in Pudong New Area, Shanghai (2002–2016).

Age-specific incidence Years APC Years APC Years APC
Total 2002–2014 0.79 2014–2016 −9.35 NA NA
Males 2002–2014 1.75 2014–2016 −10.29 NA NA
Females 2002–2014 −0.41 2014–2016 −5.77 NA NA
Age, years
 <50 2002–2016 1.23 NA NA NA NA
 50–59 2002–2004 −6.27 2004–2014 2.55 2014–2016 −10.19
 60–74 2002–2016 −0.93 NA NA NA NA
 >74 2002–2014 1.14 2014–2016 −13.45 NA NA
P< 0.05. APC: Annual percentage change; CRC: Colorectal cancer.

ASR of mortality

Despite this favorable trend in ASRs of incidence, the ASRs of mortality showed steady growth during the corresponding period. As shown in Figure 2, the peak appeared in 2015 (10.83 per 100,000). There were lower CRC mortalities in females than those in males. However, no notable trends change was observed in gender differentials over the study period [Figure 2]. After the joinpoint analyses, there was also no significant statistical change in the trends of CRC mortality observed after the introduction of the screening program. The overall ASRs of mortality increased at 0.42% (P < 0.05) per year (2002–2016); the increasing trend for males was larger (1.03%, P < 0.05). Although earlier peak of mortality ASR showed in 2003 for female (9.23 per 100,000), it was still stable (−0.54%, P > 0.05) [Supplementary Table 1, https://links.lww.com/CM9/B267].

Figure 2:
Trends in ASR incidence in Pudong New Area, Shanghai (2002–2016). ASR: Age-standardized rates.

Meanwhile, the oldest age group (>74years) experienced a significant increasing trend in mortality at 2.39% (P < 0.001) per year, while either a decreasing or stable trend of morality for the other age groups was observed [Supplementary Table 1, https://links.lww.com/CM9/B267]. Thus, the increasing trend of CRC mortality was mainly driven by individuals aged >74 years.


The ranges of age-standardized DALYs were 2.57 to 4.10 per 1000 for male and 2.49 to 3.19 per 1000 for female during 2002 to 2016. Males suffered from greater CRC burden than females. The gender gap widened across the years over the study period [Figure 3]. Compared to females, male CRC survivors had a lower disability level but higher DALYs due to greater burden of premature deaths for individuals aged 50 years and above [Supplementary Figure 2, https://links.lww.com/CM9/A989], which may have driven the gender differentials.

Figure 3:
Trends in ASR DALYs in Pudong New Area, Shanghai (2002–2016). ASR: Age-standardized rates; DALYs: Disability-adjusted life years.

Similar to the trend of mortality, results of the joinpoint analyses showed that no differential trends in age-standardized DALYs during 2002 to 2016 were detected. Overall ASR of DALYs increased at 4.07% (P < 0.001) per year. The increasing trend was greater among males (3.78% vs. 1.35%). The age group >74 years mainly contributed to the overall increasing trend, since the other age groups experienced either a decreasing or stable trend [Supplementary Table 2, https://links.lww.com/CM9/B267].


In this study, we used administrative data of Pudong New Area over the period 2002 to 2016 to examine the trends in the CRC disease burden. The results showed that the increasing trend of CRC incidence halted after 2014. The mortality and DALY rate increased at 0.42% (P < 0.05) and 4.07% (P < 0.001) per year, respectively, which was mainly driven by men and individuals aged >74 years. Men had a higher incidence, mortality, and DALY rate of CRC than women. Except for mortality, sex difference in the CRC burden has been widening in recent years.

The disease burden of CRC in Shanghai has been quite severe. The incidence and mortality rate of CRC have increased dramatically over the past decade. Compared to the previous literature,[7] the overall ASR ofCRC incidence and mortality for both genders during 2003 to 2011 in Shanghai Pudong New Area were around twice that of the national level in the same period. The results echo with the previous finding that the disease burden of CRC is more severe in the more developed regions of China.[16]

Furthermore, this study is the first to explore the age-standardized DALYs of CRC in Shanghai in recent decades. Our study showed ASRs of DALYs increased from 2.53 in 2002 to 3.51 per 1000 persons in 2016. So, DALYs attributable to CRC in Shanghai may have even exceeded the level of developed countries, such as the US (3.03 per 1000), South Korea (3.18 per 1000), and Japan (3.23 per 1000).[17]

In addition, this study also tried to primarily interpret the short-term change in the trends of CRC with the intervention of the Shanghai CRC screening program. The halted increasing trends of CRC ASR for incidence occurred in a timing that coincided with the introduction of the screening program. The organized CRC screening program was launched in Shanghai for the first time in 2013, with an aggressive goal of providing primary screening for 21% of the target population in 1 year. (The goal has been updated to 7% in following years.) The extensive screening implemented in 2013 may have helped early detect CRC cancers that would have been missed otherwise, which could partly explain the spike in incidence in 2013. However, the incidence returned to the pre-screening level and continued to decline to an even lower level in subsequent years. Furthermore, incidence trends were not observed among those aged <50 years, who were out of the target age range of the program and rarely requested a screening based on individual decisions. These results suggest that screening is beneficial in terms of incidence reduction, which is consistent with previous studies from developed countries.[18-20] Our recent study also showed that improved survival for the CRC patients was associated with Shanghai organized CRC screening program.[21] Although no statistically significant changes were observed in ASRs of mortality and DALYs before and after CRC screening program in this study, we still have reason to believe that the benefits of screening will become more apparent over time.

This study is expected to contribute to better understandings of the recent epidemiological trends of CRC and provide some important insights into the current practice of the screening program in Shanghai. First, among individuals within the target age range of the program, incidence reductions associated with the screening were evident only among those aged 50 to 59 years. Indeed, those aged >60 years disproportionately participated in the screening, because the screening program was incorporated with other public health campaigns that targeted this age group.[11]

However, the first-round results of the program show that the positivity primary screening follow-up rate (the total number of people screened by diagnostic colonoscopy divided by the total number of people that received positive results with primary screening) was significantly lower for participants aged 60 to 74 years compared to those aged 50 to 59 years,[8] which may explain the difference in the incidence trends between the two age groups. Although the overall compliance of colonoscopy (26.26%)[11] in this program was higher than that of studies from China (14.00%)[9] and Henan Province (18.71%),[10] it was still low compared to similar programs in other countries (for example, 53% in the US, and 68% in Australia).[22,23] The failure to detect and remove polyps or adenomas by taking a colonoscopy due to the low compliance may also explain the absence of similar changes in CRC mortality associated with the introduction of the screening program. These results, taken together, imply that compliance was crucial for the benefits of the program to manifest. Second, individuals aged 74 years and above suffer from the most severe burden of CRC compared to the other age groups. DALYs attributable to CRC generally peaked in this age group, and this group has been the main driver in the increasing trend of DALYs during 2002 to 2016. However, individuals aged >74 years were not eligible for screening and thus were not invited by physicians at community health centers, according to the clinical guidelines. However, individual requests for screening from this age group were generally permitted because of concerns about intense physician-patient relationships, which enable us to observe apparent incidence reduction associated with the introduction of the screening program. The results suggest that formally recommending individuals aged 74 years and above to participate in CRC screening based on individual decisions, similar to what is done in the US,[24,25] may help combat the severe disease burden of CRC. In the meantime, more evidence is needed to inform a decision on whether to expand the program to elder age cohorts for the Shanghai population.

Our study has some limitations. First, the incidence and mortality of CRC in 2016 might be underestimated. Usually, we should wait two more years to complete the cancer statistics for a particular year. Otherwise, both incidence and mortality may be underreported as some deaths owing to cancer may not yet be determined. However, we still decided to include the year 2016 into our study period to cover the entire second round of the screening program in Shanghai (from 2014 to 2016). We relied on the data quality control procedures of death and cancer reporting in Shanghai and have tried our best to obtain a complete record of cancer statistics for 2016. Second, similar to other trend analyses, we inferred the effect of the program according to temporal changes in outcome measures. However, other events or changes in risk factors of CRC during the same period may also contribute to pattern changes. The causal relationship between the screening program and the disease burden of CRC should be the focus of future research.

More cost-effectiveness evidence is needed to inform the decisions regarding expanding the screening program to additional age groups, to further explore the potential benefit of the screening program.


In summary, our study showed that the disease burden of CRC in Shanghai continues to be serious, especially among men, and individuals aged >74 years. However, the benefits of the CRC screening program are evident in the trends of ASRs for incidence, suggesting the importance of strategically promoting the CRC screening for to vulnerable individuals, which includes residents aged >74 years.

Availability of data

All data involved in this study are obtained from the Statistics Bureau, Public Security Bureau and Cancer Registry of Shanghai, Pudong New Area and can’t be publicly available.


The authors thank all the staff in Vital Statistics System and Cancer Registry of Pudong New Area from the year of 2002 to 2016, for their valuable contribution in data collection and assuring high data quality.


This study was supported by grants from the National Natural Science Foundation of China (No. 81670546 to WZ, No. 81570544 to CG, No. 81772519 to HC), the General Project of Scientific Research of Shanghai Municipal Commission of Health and Family Planning (No. 201540407 to XL), the Reserve Academic Leaders Training Program of Pudong New Area Center for Disease Control and Prevention (No. PDCDC-HBXD2020-05 to XL), and the Shanghai Public Health System Construction Three-year Action Plan Outstanding Youth Talent Training Program (No. GWV-10.2-YQ43 to YC).

Conflicts of interest



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Colorectal cancer; Disability-adjusted life years; Disease burden; Regression analysis; Screening program

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