The Cancer Incidence and Trends From 2011 to 2018 in Ma’anshan,China: A Registry-Based Observational Study

Abstract

Background

The cancer burden in China has been increasing over the decades. However, the cancer incidence remains unknown in Ma’anshan, which is one of the central cities in the Yangtze River Delta in Eastern China. The study was designed to describe the cancer incidence and trends in Ma’anshan from 2011 to 2018, providing information about cancer etiology that is useful for prevention programs.

Methods

The cancer incidence rate and age-standardized incidence rate (ASIR) were calculated using the cancer registry data in Ma’anshan during 2011-2018. The average annual percentage change (AAPC) of the ASIR was analyzed by the Joinpoint regression analysis. Age, period, and cohort effects on cancer incidence were estimated through the age-period-cohort model.

Results

There were 13,508 newly diagnosed cancer cases in males and 9558 in females in Ma’anshan during 2011-2018. The ASIR maintained a steady trend in both males and females. Age effects showed that cancer risk increased with age in both genders; no visible period effects were detected during this study period. Cohort effects changed slowly until the end of the 1950s, then started decreasing in males while increasing in females after 1960. Lung, gastric, female breast, colorectal, cervical, esophageal, liver, thyroid, lymphoma, and pancreatic cancer were the most common cancers in Ma’anshan during the study period. The ASIR of gastric cancer (AAPC: −3.72%), esophageal cancer (AAPC: −8.30%), and liver cancer (AAPC: −5.55%) declined, while that of female breast cancer (AAPC: 3.91%), colorectal cancer (AAPC: 3.23%), and thyroid cancer (AAPC: 22.38%) rose.

Conclusion

During 2011-2018, the cancer incidence in Ma’anshan was lower than that in China, nation-wide. The incidence of upper gastrointestinal cancer decreased gradually while female breast, colorectal, and thyroid cancers showed an upward trend, consistent with the changes in the cancer spectrum in China. Further studies should be designed to discover the underlying causes of these findings.

Keywords

cancer incidence joinpoint regression analysis age-period-cohort model cancer spectrum

Introduction

Cancer is one of the major non-infectious chronic diseases of humans. According to Global Cancer Statistics 2020, there were 19,300,000 new cancer cases worldwide in 2020. Predictions suggest that the number of new cancer cases will increase to 28,400,000 by 2024. Due to the huge population size of China, which accounts for one-fifth of the global population, cancer cases and deaths in China constituted 49.3% and 58.3%, respectively, of the global total in 2020.¹ Many studies have revealed that the cancer incidence in China has been increasing since 2000.^2,3 Cancer treatment is not only costly but also time-consuming, and most cancer patients cannot be cured completely. Cancer in China has become a significant public health problem, putting a heavy disease burden on individuals and society.²

Cancer registration has been operating in China for 63 years, since the first cancer registry was established in 1959 in Linzhou, Henan Province. The National Central Cancer Registry was founded in 2002 to be the national bureau to manage cancer registration. The quality of data from the cancer registration system has gradually improved.⁴ Up to 2019, nearly 438 million people, or 31.5% of the Chinese population, have been covered by cancer registration sites, nationwide.⁴ Continuous cancer surveillance data play a vital role in cancer epidemiological studies. The establishment of a cancer registration system is also essential to standardize management of cancer patients and improve public health policies.

Ma’anshan City is located in the east of Anhui Province, spanning both sides of the Yangtze River, and it is adjacent to the 2 provincial capitals, Nanjing and Hefei. The city started cancer registration in 1996,⁵ and established the first national cancer registry in Anhui Province in 2006. Data provided by the local cancer registry has been consistently included in the Chinese Cancer Registry Annual Report and Cancer Incidence in 5 Continents since 2008, indicating their relatively high data quality.⁶ In addition, Ma’anshan is one of the central cities of the Yangtze River Delta, the most economically active region in China .⁷ However, there have been few studies of cancer incidence in Ma’anshan during the past decade. With the aim of providing insights into cancer etiology and guiding prevention measures, we describe the cancer incidence and trends in Ma’anshan from 2011 to 2018. We analyze the age, period, and cohort effects on cancer incidence and compared them to the results at the national level.

Material and Methods

Study Design and Data Source

This was a retrospective observational study using data from the cancer registry of Ma’anshan City, Anhui Province, China. The cancer registry covers the whole city, consisting of 3 districts and 3 counties, since the administrative restructuring was completed in 2011. As an eastern city, the Ma’anshan cancer registry has a higher population coverage rate than the national average, which is 31.5%.⁴ Cancer case registration and quality control follow the requirements of the Chinese Guideline for Cancer Registration⁸ and the International Agency for Research on Cancer.

This study analyzed cancer incidence rates from 2011 to 2018 in Ma’anshan. The original cancer incidence data were obtained from the cancer registration system of Ma’anshan. Records with death certificates only were excluded from the dataset. After deduplication, all persons diagnosed with cancer, as defined by the International Classification of Diseases version 10 (ICD-10: C00-C97), from 2011 to 2018 were included in the analyses. The dataset provided complete information on patients’ demographic details, such as sex and age, cancer type (ICD-10), and the year of diagnosis. Population data were derived from the local Ministry of Civil Affairs by year, sex, and 5-year age groups. The reporting of this study conforms to the STROBE guidelines (Supplemental File S1).⁹ The data analyzed in this study do not contain personal-level information; therefore, ethical approval was not required (Ma’anshan Center for Disease Control and Prevention Medical Ethics Committee; project number: 2023001). The participating registry has given its consent to the study. The study was performed in accordance with the Declaration of Helsinki.

Quality Evaluation

According to the Chinese National Cancer Center, the quality evaluation metrics of cancer registration data consist of the percentage of cases verified through morphology (MV%, standard: >66%), the percentage of cases reported only through death certificates (DCO%, standard: >10%), the percentage of other cases with an unspecified or unknown primary site (O&U%, standard: >10%), etc.¹⁰ In this study, MV%, DCO%, and O&U% of Ma’anshan cancer registration data from 2011 to 2018 were 73.72%, 2.32%, and 1.55%, respectively. In general, the cancer registration data involved in this study reached the quality control standard used in China.

Statistical Analysis

We calculated the cancer incidence and age-standardized incidence rates (ASIR: <1, 1-4, 5-9, 10-14, …, 75-79, 80-84, and >85) per 100,000 persons based on the world standard population (ASIR-world) and the fifth Chinese population census (ASIR-China). The subsequent analysis only used the ASIR-world.

Trends in cancer incidence rates and ASIR-world were estimated using the “Joinpoint” regression model, which is a type of piecewise linear regression method. This model can estimate the number of turning points (Joinpoints) within a given period, utilizing the least square method.¹¹ We applied the log-linear model to calculate the annual percentage change (APC), average annual percentage change (AAPC), and the corresponding 95% confidence interval (CI) for a specific time period. When there is no turning point, the APC of this period is equal to AAPC. In this section, we performed Joinpoint analysis via the “Joinpoint” software (Version 4.9.0.0) developed by the National Cancer Institute, USA.¹¹

We used the Age-Period-Cohort model to evaluate the effect of age, period, and birth cohort on cancer incidence. Age effects on diseases are associated with biological factors like immune decline.¹² Period effects represent variations in disease incidence over time that are associated with all age groups simultaneously,¹³ such as the change of diagnostic criteria or disease registration policy, and the development of early screening technology. Cohort effects show the impact of different disease risk factors on different generations,¹² as people born in different calendar years may go through different social events in their lifetime. Therefore, they are exposed to various risk factors, leading to variations in disease incidence among generations. In this study, we grouped age (20-84 years old) with a 5-year interval and period (2011-2018) with a 1-year interval to identify individuals who belonged to the same birth cohort (1931-1998). People under 20 years old and above 84 years old were excluded, due to the few new cases. The Age-Period-Cohort model was developed using the R package Epi.¹⁴

A two-sided P < 0.05 was considered statistically significant, and 95% confidence intervals were reported. All analysis was conducted with R (Version 4.0.4) and SPSS (Version 26.0).

Results

New Cancer Cases and Incidence Rate

There were 13,508 male and 9558 female cancer cases that were newly diagnosed in Ma’anshan from 2011 to 2018. Table 1 provides the numbers of cancer cases, incidence rates, and age-standardized incidence rates for each year using the fifth Chinese population census (ASIR-China) and the world standard population (ASIR-world). The cancer incidence rate showed no significant fluctuations during this period, ranging from 117.85 to 134.79 per 100,000. The ASIR was lower than the incidence rate, with ASIR-China ranging from 73.32 to 78.52 per 100,000, and the ASIR-world ranging from 70.96 to 76.60 per 100,000. The ASIR-world of males was consistently higher than that of females.

Table 1.

Cancer Cases and Incidence From 2011 to 2018 in Ma’anshan.

Years	Cancer Cases			Incidence Rate per 100000			ASIR-China per 100000			ASIR-World per 100000
Years	Males	Females	All	Males	Females	All	Males	Females	All	Males	Females	All
2011	1599	1095	2694	135.39	99.10	117.85	86.24	64.03	74.99	85.46	61.33	73.24
2012	1656	1082	2738	140.55	97.90	119.91	89.16	62.74	75.70	87.92	59.92	73.71
2013	1613	1131	2746	136.92	102.27	120.23	84.92	64.41	74.49	83.77	61.33	72.36
2014	1784	1224	3008	151.85	111.02	132.09	90.20	67.73	78.52	89.45	64.77	76.60
2015	1702	1167	2874	144.47	105.43	125.77	85.31	63.52	74.08	84.46	60.72	72.18
2016	1795	1153	2950	151.78	103.67	128.55	88.04	60.30	73.89	87.93	57.25	72.25
2017	1714	1366	3084	145.53	123.04	134.79	81.31	73.53	76.91	80.83	69.35	74.52
2018	1645	1340	3013	139.57	120.47	131.52	76.00	70.87	73.32	75.66	66.54	70.96

ASIR-China, age-standardized incidence by the fifth Chinese population census; ASIR-world, age-standardized incidence by the world standard population.

Joinpoint Regression of the ASIR-World

The results of Joinpoint regression for the average percent change (APC) and annual average percent change (AAPC) of the ASIR-world are presented in Table 2 and Figure 1. The APC and AAPC of the ASIR-world were −1.40% (−3.08%, 0.31%) from 2011 to 2018. For males and females, the APC and AAPC of the ASIR-world were-1.40% (−3.08%, 0.31%) and 1.23% (−0.99%, 3.50%), respectively. All the 95% confidence intervals of the APC and AAPC included zero, indicating that no significant turning points or changes were detected. Furthermore, despite the lack of statistical significance, the changes in the ASIR-world of males and females were in the opposite directions.

Table 2.

APC and AAPC of ASIR-World From 2011 to 2018 in Ma’anshan.

Years	Groups	APC (95%CI)	AAPC (95%CI)
2011∼2018	Males	−1.40 (-3.08, 0.31)	−1.40 (-3.08, 0.31)
	Females	1.23 (-0.99, 3.50)	1.23 (-0.99, 3.50)
	All	−0.27 (-1.19, 0.65)	−0.27 (-1.19, 0.65)

*means P value <0.05; APC, annual percent change; AAPC, average annual percent change; ASIR-world, age-standardized incidence rate by the world standard population.

Figure 1.

Trends of ASIR-world from 2011 to 2018 in Ma’anshan estimated by Joinpoint regression. * means P value <0.05; APC, annual percent change; ASIR-world, age-standardized incidence rate by the world standard population.

Age-Period-Cohort Model

The model described the rates produced by age, period, and cohort effects on cancer incidence. Figure 2 shows that age effects had a significant impact on cancer incidence. The risk of cancer increased with age in both males and females. In males, the incidence rate of the 20-24 age group was the lowest, at 11.61 (6.44, 20.94) per 100,000 person-years, while the highest rate occurred in the 80-84 age group, at 669.54 (575.00, 779.61) per 100,000 person-years. In females, the lowest incidence rate was observed in the 20-24 age group, at 3.89 (2.29, 6.58) per 100,000 person-years, and the highest rate occurred in the 80-84 age group, at 396.19 (316.12, 496.54) per 100,000 person-years. An overall decreasing trend was detected in birth cohort effects for males. The rate exhibited a remarkable decline from 0.86 (0.80, 0.92) in 1958 to 0.24 (0.12, 0.46) in 1998. In contrast, the birth cohort effects for females did not change significantly before 1960, but the rate displayed a noticeable increase from 0.91 (0.83, 1.00) in 1960 to 3.03 (1.69, 5.45) in 1998. The variations in the trends of the period effects were not obvious in either males or females. More details are provided in Supplemental Table S1.

Figure 2.

Age-Period-Cohort model of cancer incidence in Ma’ anshan. (A) Male; (B) Female.

The Incidence Rate of the Most Common Cancers and Cancer-specific Joinpoint Regression

The top 10 most common cancers in Ma’anshan were lung cancer, gastric cancer, female breast cancer, colorectal cancer, cervical cancer, esophageal cancer, liver cancer, thyroid cancer, lymphoma, and pancreatic cancer, as reported in decreasing order of the average ASIR-world during 2011-2018 in Supplemental Table S2. The trends of the ASIR-world for the top 10 cancers from 2011 to 2018 are shown in Figure 3. Overall, the ASIR-world of gastric and lung cancer were the highest before 2016, ranging from 11.42 per 100,000 to 13.77 per 100,000. The ASIR-world of colorectal cancer, female breast cancer, and thyroid cancer were on the rise, while gastric, esophageal, and liver cancers were on the decline. By 2018, female breast cancer became the most prevalent cancer, with an ASIR-world of 11.90 per 100,000.

Figure 3.

ASIR-world of the top 10 cancers from 2011 to 2018 in Ma’anshan. ASIR-world, age-standardized incidence rate by the world standard population.

The results of the Joinpoint regression analysis for each cancer are shown in Figure 4 and Table 3. The ASIR-world of lung cancer, cervical cancer, lymphoma, and pancreatic cancer remained stable from 2011 to 2018. The other 6 cancers exhibited significant trends during this period, with the ASIR-world of female breast, colorectal, and thyroid cancers increasing, while gastric, liver, and esophageal cancers decreased overall. The ASIR-world of female breast cancer showed an upward trend, significantly increasing by 3.91% (1.68%, 6.19%) yearly. Similarly, the ASIR-world of colorectal cancer among all Ma’anshan residents increased by 3.23% (2.26%, 4.22%) annually, but the increase was significant only in males, at 3.84% (0.51%, 7.27%) annually. As the cancer with the greatest variability, the ASIR-world of thyroid cancer in all residents increased remarkably by 22.38% (12.15%, 33.54%) per year.

Figure 4.

Trends of cancer-specific ASIR-world from 2011 to 2018 in Ma’anshan estimated by Joinpoint regression. (A) Lung cancer; (B) Gastric cancer; (C) Female breast cancer; (D) Colorectal cancer; (E) Cervical cancer; (F) Esophageal cancer; (G) Liver cancer; (H) Thyroid cancer; (I) Lymphoma; (J) Pancreatic cancer. * means P value <0.05; APC, annual percent change; ASIR-world, age-standardized incidence rate by the world standard population.

Table 3.

APC and AAPC of ASIR-World for the Top Ten Cancers From 2011 to 2018 in Ma’anshan.

Types of Cancer	Groups	Number of Joinpoints	Location of Joinpoints	Years	APC (%)	AAPC (%)
Lung cancer	Males	0	-	2011-2018	−1.29 (-3.95, 1.44)	−1.29 (-3.95, 1.44)
	Females	0	-	2011-2018	0.09 (-2.99, 3.27)	0.09 (-2.99, 3.27)
	All	0	-	2011-2018	−1.00 (-3.56, 1.63)	−1.00 (-3.56, 1.63)
Gastric cancer	Males	0	-	2011-2018	−3.70 (-7.31, −0.05)	−3.70 (-7.31, −0.05)
	Females	0	-	2011-2018	−3.27 (-8.27, 2.00)	−3.27 (-8.27, 2.00)
	All	0	-	2011-2018	−3.72 (-6.52, −0.84)*	−3.72 (-6.52, −0.84)*
Breast cancer	Females	0	-	2011-2018	3.91 (1.68, 6.19)*	3.91 (1.68, 6.19)*
Colorectal cancer	Males	0	-	2011-2018	3.84 (0.51, 7.27)*	3.84 (0.51, 7.27)*
	Females	0	-	2011-2018	2.42 (-1.94, 6.97)	2.42 (-1.94, 6.97)
	All	0	-	2011-2018	3.23 (2.26, 4.22)*	3.23 (2.26, 4.22)*
Cervical cancer	Females	0	-	2011-2018	0.73 (-3.20, 4.18)	0.73 (-3.20, 4.18)
Esophageal cancer	Males	0	-	2011-2018	−6.78 (-10.25, −3.18)*	−6.78 (-10.25, −3.18)*
	Females	0	-	2011-2018	−9.64 (-15.97, −2.83)*	−9.64 (-15.97, −2.83)*
	All	1	2016	2011-2016	−4.63 (-8.56, 0.54)*	−8.30 (-11.71, −4.76)*
				2016-2018	−16.88 (-31.13, 0.32)
Liver cancer	Males	0	-	2011-2016	−4.49 (-7.80, 1.07)*	−4.49 (-7.80, 1.07)*
	Females	0	-	2011-2018	−5.60 (-9.98, −1.00)*	−5.60 (-9.98, −1.00)*
	All	1	2016	2011-2016	−2.94 (-5.60, 0.22)*	−5.55 (-7.88, −3.16)*
				2016-2018	−11.76 (-22.06, −0.11)*
Thyroid cancer	Males	0	-	2011-2018	17.77 (11.41, 24.48)*	17.77 (11.41, 24.48)*
	Females	0	-	2011-2018	23.65 (11.26, 37.43)*	23.65 (11.26, 37.43)*
	All	0	-	2011-2018	22.38 (12.15, 33.54)*	22.38 (12.15, 33.54)*
Lymphoma	Males	0	-	2011-2018	−2.25 (-7.12, 2.89)	−2.25 (-7.12, 2.89)
	Females	0	-	2011-2018	−4.74 (-12.32, 3.49)	−4.74 (-12.32, 3.49)
	All	0	-	2011-2018	−3.15 (-7.03, 0.90)	−3.15 (-7.03, 0.90)
Pancreatic cancer	Males	0	-	2011-2018	−0.20 (-6.10, 6.06)	−0.20 (-6.10, 6.06)
	Females	0	-	2011-2018	0.83 (-10.95, 14.17)	0.83 (-10.95, 14.17)
	All	0	-	2011-2018	0.26 (-6.51, 7.52)	0.26 (-6.51, 7.52)

*means P value <0.05; APC, annual percent change; AAPC, average annual percent change.

The ASIR-world of gastric cancer in all residents significantly decreased by 3.72% (0.84%, 6.52%) per year. The ASIR-world of esophageal cancer in all residents, males, and females significantly decreased by an average of 8.30% (4.76%, 11.71%), 6.78% (3.18%, 10.25%), and 9.64% (2.83%, 15.97%) per year, respectively. Interestingly, there was a turning point in 2016 for the trend in the ASIR-world of esophageal cancer in all residents. Specifically, the ASIR-world of esophageal cancer in all residents decreased by 4.63% (0.54%, 8.56%) per year from 2011 to 2016 and 16.88% (−0.32%, 31.13%) per year from 2016 to 2018. The ASIR-world of liver cancer in all residents, males, and females showed the same decreasing trend, with declines of 5.55% (3.16%, 7.88%), 4.49% (1.07%, 7.80%), and 5.60% (1.00%, 9.98%) per year, respectively. Additionally, there was a turning point in 2016 for the trend of the ASIR-world for liver cancer in all residents, with the rate decreasing by 2.94% (0.22%, 5.60%) per year from 2011 to 2016 and 11.76% (0.11%, 22.06%) per year during 2016-2018.

Discussion

In this study, we described the cancer incidence and trends from 2011 to 2018 in Ma’anshan, China. During this period, the ASIR-world maintained a steady trend in both males and females, ranging from 70.96 to 76.60 per 100,000 overall. The age effects showed that cancer risk increased with age in both genders, but no visible period effects were detected during this period. Cohort effects changed slowly until the end of the 1950s, then started decreasing in males while increasing in females after 1960. Lung cancer, gastric cancer, female breast cancer, colorectal cancer, cervical cancer, esophageal cancer, liver cancer, thyroid cancer, lymphoma, and pancreatic cancer were the most common cancers in Ma’anshan during this period. The ASIR-world of upper gastrointestinal cancers decreased gradually while female breast cancer, colorectal cancer, and thyroid cancer showed an upward trend.

The Chinese National Cancer Center provides annual data on the cancer incidence rate in China, with the latest update available until 2016. In 2016, the cancer incidence rate and ASIR-world were reported as 293.91 and 186.46 per 100,000, respectively.^2,15 Based on global epidemiological data, Feng et al.¹⁶ estimated that the ASIR-world in 2018 was 201.7 per 100,000. Overall, it is evident that the cancer incidence rate and ASIR-world in Ma’anshan were lower than they were in China, nation-wide. Compared with Eastern China, the ASIR-world in Ma’anshan was also lower than the regional average (186.50 per 100,000 in 2016).¹⁵ As the first city in Anhui Province to have a national-level cancer registry, the Ma’anshan government has been attaching great importance to cancer prevention, carrying out regular cancer prevention events every year to improve the health awareness of residents. In recent years, Ma’anshan City has taken the lead in launching a free HPV vaccination campaign for females between the ages of 9 and 13 in Anhui Province, as one of the first 15 pilot cities in China. Additionally, as Ma’anshan City experiences population outflow, the tumor registry data may not fully capture all the cases in the system. Therefore, the reasons for the lower cancer incidence rate in Ma’anshan compared to the regional average are complex and require further comparison with specific incidence data and the distribution of risk factors from other cities. Furthermore, males exhibited a higher cancer incidence rate and ASIR-world than females did, which is consistent with the national-level trend.^2,15,16 In the Joinpoint regression analysis, we observed that the ASIR-world in Ma’anshan maintained a steady trend in 2011-2018 in both genders, while the ASIR-world for China, overall, remained stable in males in 2007-2016, but exhibited an annual increase of 2.3% in females.¹⁵ From a national perspective, the nationwide screening program for 2 cancers in rural women since 2009 (namely, cervical cancer and breast cancer) may be one of the reasons for the increase in the incidence of female cancers.¹⁷

Based on the results of the age-period-cohort model, we explored the impact of age, period, and birth cohort on cancer incidence. First, age emerged as a crucial factor influencing cancer incidence, with a continuous increase in cancer risk with age in both genders. This finding aligns with those of similar studies conducted in diverse populations worldwide.^12,18 The cumulative exposure to risk factors over a lifetime may gradually damage human biological systems, providing a partial explanation for the observed age effects on cancer incidence.¹⁹ Furthermore, China is now undergoing an accelerated aging process.²⁰ From 2000 to 2020, the proportion of the population over 60 years old in China rose from 10% to 18.70%,²¹ and it is predicted to reach 28% of the total population by 2040.²² According to local census data, the proportion of elderly persons in Ma’anshan rose from 12.74% to 17.24% during the last decade. This demographic shift suggests that more individuals will move into the high-risk group for cancer, leading to a corresponding increase in the burden of cancer. Second, there was no noticeable trend in period effects for either males or females. This indicates that social events and changes, such as economic improvement, environmental pollution, cancer screening, diagnostic techniques, and other factors did not significantly influence cancer incidence from 2011 to 2018 in Ma’anshan. Third, in addition to the variance attributable to age and period effects, birth cohort effects independently impacted cancer risks in both males and females. These effects were divided into 2 main stages based on the trend. The first stage, covering 1931 to 1960, saw males maintaining a relatively high level of cancer risk compared to females, with slowly decreasing trends detected in both genders. This period was marked by World War II, the Great Famine, and other significant social revolutions in China, accompanied by poor sanitary conditions and nutritional status. Individuals born earlier were more likely to have early-life exposure to adverse factors that may play a crucial role in carcinogenesis.^13,23 At the beginning of the latter stage, the end of the 1950s, the birth cohort effect in males started dropping significantly, while the birth cohort effect showed an upward trend in females. Combined with the previous findings, the gender difference in the changing direction of cohort effects was consistent with the trend of cancer incidence, which decreased in males and increased in females (mentioned in the Joinpoint regression of the ASIR-world). In addition, different physiological factors and social roles may partially explain the disparities in the risk factors between males and females.²⁴ More specific explanations still need to be found and confirmed by further research.

The incidence of each type of cancer in Ma’anshan was ranked in descending order in this study, as follows: lung cancer, gastric cancer, female breast cancer, colorectal cancer, cervical cancer, esophageal cancer, liver cancer, thyroid cancer, lymphoma, and pancreatic cancer. The incidence of all these types of cancer was lower than the national level, as well as that in the eastern China.¹⁵ Trends for these cancers were also analyzed for further study. From 2011 to 2018, the incidence of upper gastrointestinal cancers in Ma’anshan demonstrated a downward trend, including esophageal cancer, gastric cancer, and liver cancer. In contrast, the incidence of colorectal cancer, female breast cancer, and thyroid cancer increased gradually during this period, which is the same as the overall trends in China, based on previous studies.²⁵ These observations are consistent with the evolving cancer spectrum in China, transitioning from a developing country to a developed one, with an increasing incidence and burden of female breast cancer and colorectal cancer and a heavy burden of upper gastrointestinal cancers.²⁵ On one hand, the decline in upper gastrointestinal cancer incidence reflects the success of prevention measures and the promotion of health awareness. Taking liver cancer for instance, as part of routine infant immunization from 2002, HBV vaccination has significantly contributed to the decrease in HBV infection in China, which is one of the most important risk factors for liver cancer.²⁶ In addition, the recognized risk factors for upper gastrointestinal cancers, including Helicobacter pylori, aflatoxin, nitrite, and the consumption of hot food, etc., have gained widespread attention. Consequently, more people tend to reduce these exposures by promptly treating infections or adjusting their diets accordingly.² On the other hand, numerous epidemiological studies have found that with improvements in economic and living conditions, people tend to adopt dietary patterns high in fat and low in fiber, contributing to the increase in cancer incidence, such as colorectal cancer and female breast cancer.^27,28 It is postulated that the upward trend of colorectal cancer and female breast cancer incidence in Ma’anshan could partly be attributed to the rapid development of this city as one of the core cities of the Yangtze River Delta in recent years. Furthermore, the implementation of a free screening program for female breast cancer in Ma’anshan City since 2010, along with the incorporation of colonoscopy into routine medical examinations, has contributed to increased cancer diagnosis rates. For thyroid cancer, the increase in incidence might be explained by the sensitivity and accessibility of diagnostic tools like ultrasonography, as reported in a previous study.²⁹ Moreover, exposure to ionizing radiation, level of iodine intake, and obesity have also been reported to influence the development of thyroid cancer.^30-33

In light of the main findings of this study, the cancers with the highest incidence—namely lung cancer and gastric cancer—and those with an upward trend in incidence, namely female breast cancer and colorectal cancer, should be prioritized for cancer prevention efforts in Ma’anshan. As summarized in a previous review,³⁴ the major areas deserving attention in cancer control in China include cancers associated with environmental pollution, tobacco use, occupational carcinogens, infections, excessive alcohol consumption, dietary deficiencies, and obesity. Therefore, we suggest enhancing residents’ knowledge of these common risk factors and fully implementing cancer screening programs, especially targeting high-risk populations, such as the elderly, for the aforementioned cancer types in Ma’anshan. This is also applicable at the national level.

From a methodological perspective, our study employed well-established analytical methods for cancer registry data. For instance, similar statistical metrics and models have been used in various studies^25,35,36 to assess data quality and analyze cancer incidence trends, indicating a certain degree of generalizability. In addition, our study has several strengths. First, we described the cancer incidence and trends in Ma’anshan from 2011 to 2018 using cancer registration data, providing valuable insights for guiding local cancer prevention measures. Second, the age-period-cohort model allowed us to assess the effects of age, period, and cohort on cancer incidence while adjusting for potential sociodemographic confounding factors. However, this study also has several limitations. As a descriptive study, it can only provide exploratory insights into cancer etiology due to the lack of information on risk factors for the population in Ma’anshan City and other cities. Risk factors affecting changes in local cancer incidence should be confirmed through strictly designed association and prospective studies in the future, following epidemiological principles. Furthermore, this study only utilized data from 2011 to 2018 due to data quality and the regional coverage of the cancer registry. Additional studies are needed to explore the long-term trends of cancer incidence. Therefore, we still need to enhance the cancer registration quality through ongoing staff training in registry procedures, database management, and statistics, to provide internationally comparable, valid, and timely cancer incidence data for research and policy-making.³⁷

Conclusion

In general, the cancer incidence in Ma’anshan from 2011 to 2018 was lower than that in China overall, maintaining a stable trend during these years. The incidence increased with age, indicating a significant disease burden accompanying population aging. However, cancer-specific trends varied, even showing opposite patterns, suggesting changes in exposure to different risk factors in Ma’anshan. The findings also indicate the need for targeted preventive measures, including increasing public awareness and early screening.

Supplemental Material

Supplemental Material - The Cancer Incidence and Trends From 2011 to 2018 in Ma’anshan, China: A Registry-Based Observational Study

Supplemental Material for The Cancer Incidence and Trends From 2011 to 2018 in Ma’anshan, China: A Registry-Based Observational Study by Qirong Qin, Yuxin Min, Yijing Xie, Chun Wang, Yan Zhang, Dandan Wu, Jiahua Xu, Na Meng, and Chen Suo in Cancer Control

Supplemental Material

Supplemental Material - The Cancer Incidence and Trends From 2011 to 2018 in Ma’anshan, China: A Registry-Based Observational Study

Footnotes

Author Contributions

QQ: Data curation, Funding acquisition, Project administration, Resources; YM: Formal analysis, Methodology, Visualization, Writing – original draft; YX: Visualization, Writing – review & editing; CW, YZ, DW, JX, and NM: Data curation, Investigation; CS: Funding acquisition, Methodology, Project administration, Writing – review & editing. All authors read and approved the final manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was funded by the National Key Research and Development Program of China (grant number: 2019YFC1315804), National Science & Technology Fundamental Resources Investigation Program of China (grant number: 2019FY101103), the National Natural Science Foundation of China (grant number: 91846302), Shanghai Municipal Science and Technology Major Project (grant number: ZD2021CY001), the Three-Year Action Plan for Strengthening Public Health System in Shanghai (grant number: GWV-10.2-YQ32); an Innovation Grant from Science and Technology Commission of Shanghai Municipality, China (grant number: 20ZR1405600); and the Project funded by Ma’anshan Science and Technology Bureau (grant number: YL-2021-028).

Ethical Statement

ORCID iD

Chen Suo

Data Availability Statement

Data are provided within the manuscript or supplementary information files.

Supplemental Material

Supplemental material for this article is available online.

Appendix

References

Sung

Ferlay

Siegel

, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209-249.

Sun

Cao

, et al. Cancer burden in China: trends, risk factors and prevention. Cancer Biol Med. 2020;17(4):879-895.

Liu

Zhou

Wang

, et al. Secular trend of cancer death and incidence in 29 cancer groups in China, 1990-2017: a joinpoint and Age-Period-Cohort analysis. Cancer Manag Res. 2020;12:6221-6238.

Wei

Zeng

Zheng

, et al. Cancer registration in China and its role in cancer prevention and control. Lancet Oncol. 2020;21(7):e342-e349.

Chronic Disease Prevention Health Management Department Ma’anshan Center for Disease Control and

Prevention.

“CDC Receives Another Award of Outstanding Contribution to National Tumor Registry” [EB/OL]. May 1 2021. https://www.mascdc.net/news/zxnews/2021/12/31/b353732a488a32c9bcd43a53a627d301.html

Chen

Zheng

Baade

, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115-132.

Yang

. A study of the economic growth effects of market integration: an examination of 27 cities in the Yangtze River Delta city cluster. PLoS One. 2023;18(11):e0287970.

Center NC . Chinese Guideline for Cancer Registration. Beijing: 2016: People’s Medical Publishing House; 2016.

von Elm

Altman

Egger

Pocock

Gøtzsche

Vandenbroucke

. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med. 2007;147(8):573-577.

10.

Hao

Wei

Center

. China Cancer Registry Annual Report 2021. Beijing, China: Ministry of Health; 2023.

11.

Kim

Fay

Feuer

Midthune

. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med. 2000;19(3):335-351.

12.

Liu

Jiang

, et al. Secular trends in incidence and mortality of bladder cancer in China, 1990-2017: a joinpoint and age-period-cohort analysis. Cancer Epidemiol. 2019;61:95-103.

13.

Jiang

Xie

, et al. Mortality trends in colorectal cancer in China during 2000-2015: a joinpoint regression and Age-Period-Cohort analysis. Prev Chronic Dis. 2018;15:E156.

14.

Carstensen

. Age-period-cohort models for the Lexis diagram. Stat Med. 2007;26(15):3018-3045.

15.

Zheng

Zhang

Zeng

, et al. Cancer incidence and mortality in China, 2016. J Natl Cancer Cent. 2022;2(1):1-9.

16.

Feng

Zong

Cao

. Current cancer situation in China: good or bad news from the 2018 Global Cancer Statistics? Cancer Commun. 2019;39(1):22.

17.

Sun

Cao

, et al. Breast and cervical cancer screening adherence in Jiangsu, China: an ecological perspective. Front Public Health. 2022;10:967495.

18.

De Carvalho

Borges

Da Silva

. Incidence of colorectal cancer in selected countries of Latin America: age-Period-Cohort effect. Asian Pac J Cancer Prev. 2020;21(11):3421-3428.

19.

Ben-Shlomo

Kuh

. A life course approach to chronic disease epidemiology: conceptual models, empirical challenges and interdisciplinary perspectives. Int J Epidemiol. 2002;31(2):285-293.

20.

Song

, et al. Basic and translational aging research in China: present and future. Protein Cell. 2019;10(7):476-484.

21.

Zhou

Qian

. Industrial structure upgrading, population aging and migration: an empirical study based on Chinese provincial panel data. PLoS One. 2023;18(10):e0291718.

22.

The

. Population ageing in China: crisis or opportunity? Lancet. 2022;400(10366):1821.

23.

Wang

Mubarik

Zhang

, et al. Long-term trends of liver cancer incidence and mortality in China 1990-2017: a joinpoint and Age-Period-Cohort analysis. Int J Environ Res Publ Health. 2019;16(16):2878.

24.

Dong

Cioffi

Wang

, et al. Sex differences in cancer incidence and survival: a pan-cancer analysis. Cancer Epidemiol Biomarkers Prev. 2020;29(7):1389-1397.

25.

Qiu

Cao

. Cancer incidence, mortality, and burden in China: a time-trend analysis and comparison with the United States and United Kingdom based on the global epidemiological data released in 2020. Cancer Commun. 2021;41(10):1037-1048.

26.

Tanaka

Katayama

Kato

, et al. Hepatitis B and C virus infection and hepatocellular carcinoma in China: a review of epidemiology and control measures. J Epidemiol. 2011;21(6):401-416.

27.

Azeem

Gillani

Siddiqui

Jandrajupalli

Poh

Syed Sulaiman

. Diet and colorectal cancer risk in Asia--a systematic review. Asian Pac J Cancer Prev. 2015;16(13):5389-5396.

28.

De Cicco

Catani

Gasperi

Sibilano

Quaglietta

Savini

. Nutrition and breast cancer: a literature review on prevention, treatment and recurrence. Nutrients. 2019;11(7):1514.

29.

Zheng

Dal Maso

Zhang

Wei

Vaccarella

. Mapping overdiagnosis of thyroid cancer in China. Lancet Diabetes Endocrinol. 2021;9(6):330-332.

30.

Wang

Shang

Ping

Liu

. Thyroid cancer: incidence and mortality trends in China, 2005-2015. Endocrine. 2020;68(1):163-173.

31.

Sinnott

Ron

Schneider

. Exposing the thyroid to radiation: a review of its current extent, risks, and implications. Endocr Rev. 2010;31(5):756-773.

32.

Laurberg

Bülow Pedersen

Knudsen

Ovesen

Andersen

. Environmental iodine intake affects the type of nonmalignant thyroid disease. Thyroid. 2001;11(5):457-469.

33.

Kitahara

Gamborg

Berrington de González

Sørensen

Baker

. Childhood height and body mass index were associated with risk of adult thyroid cancer in a large cohort study. Cancer Res. 2014;74(1):235-242.

34.

Bode

Dong

Wang

. Cancer prevention and control: alarming challenges in China. Natl Sci Rev. 2016;3(1):117-127.

35.

Wang

Pan

Chen

, et al. Trends in incidence and mortality of esophageal cancer in Huai'an district, a high-risk area in Northern Jiangsu Province, China. Cancer Control. 2022;29:10732748221076824.

36.

Politis

Higuera

Chang

Gomez

Bares

Motta

. Trend analysis of cancer mortality and incidence in Panama, using joinpoint regression analysis. Medicine (Baltim). 2015;94(24):e970.

37.

Quintana

Velásquez

Rodríguez

, et al. History of the national cancer registry of Panama. J Registry Manag. 2023;50(1):19-25.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.10 MB

0.02 MB