Primary malignant bone tumors incidence, mortality, and trends in China from 2000 to 2015 : Chinese Medical Journal

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Original Article

Primary malignant bone tumors incidence, mortality, and trends in China from 2000 to 2015

Xi, Yunfeng1; Qiao, Liying1; Na, Buqi1; Liu, Huimin1; Zhang, Siwei2; Zheng, Rongshou2; Wang, Wenrui1; Sun, Kexin2; Wei, Wenqiang2; He, Jie2

Editor(s): Ni, Jing

Author Information
Chinese Medical Journal ():10.1097/CM9.0000000000002547, February 28, 2023. | DOI: 10.1097/CM9.0000000000002547
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Abstract

Introduction

Primary malignant bone tumors originating from bone tissue, are generally rarer than secondary bone tumors, and account for about 0.2% of all neoplasms.[1] Cancer registration is the most basic and important component in cancer prevention and treatment. Population-based cancer registries can be used to assess cancer burden and its change; provide a basis for research on cancer causes and prevention; provide clues regarding the prevalence of risk factors of cancer; and monitor the effects of programs on prevention, early detection or screening, treatment, and palliative care. Mortality and morbidity data are widely used to establish and evaluate cancer prevention strategies and control measures, allocate medical resources, and conduct scientific research. The National Central Cancer Registry of China (NCCRC), which is subordinate to National Cancer Center, is one of the largest cancer registration networks worldwide and the source of population-based cancer epidemiological survey data in China.[2,3-5]

The research on primary malignant bone tumors is rare. Previous studies in China were devoted to incidence and mortality. In this study, we reported the incidence and death due to primary malignant bone tumors in 2015 and the changing trends of incidence and death from 2000 to 2015.

Methods

Data source and quality control

Data were extracted from the NCCRC using the International Statistical Classification of Diseases and Related Health Problems 10th Revision (ICD-10) codes C40.0 to C41.9.[6] All contributed data were checked and evaluated based on the Guidelines for Chinese Cancer Registration[7] and Cancer Incidence in Five Continents Volume X,[8] with reference to the relevant data quality criterion of the International Agency for Research on Cancer/International Association of Cancer Registries.[9] The main quality control indicators are the percentage of cases morphologically verified (MV%), the percentage of death certificate-only cases (DCO%), the mortality-to-incidence ratio (M/I), and the percentage of the diagnosis of unknown basis (UB%). Eligible datasets to be analyzed met the following criteria: MV% not <66% for all cancers combined, DCO% <15%, M/I between 0.6 and 0.8, and UB% <5.

Data collection

The data collection of population-based cancer registry adopts the combination of both active and passive registrations. Active registration means that the registry sends staff actively check the diagnosis and treatment history of new tumor cases in various medical units and extract them from a unified tumor case registration form. Passive registration is that the medical staff responsible for the diagnosis and treatment of tumor cases in various medical institutions fill in tumor report cards or forms, which are summarized by the hospital and submitted to the tumor registry regularly.

The data of tumor death cases in the cancer registry system are derived from the data records of all-cause-of-death registry reports. However, due to the gap between the completeness of the death cause registration report and the accuracy of the underlying cause of death judgment, the two disease surveillance systems of cancer registration and all-cause death are used to improve the registration quality. The completeness of the all-cause registration data and the accuracy of the underlying cause of death were supplemented by the follow-up information of tumor cases.

Statistical analysis

Data from 368 registries were pooled to produce national estimates. Crude incidence and mortality rates were calculated by age groups (0–19, 20–59, and >60 years old), gender, and area (urban/rural). The number of new cases and that of deaths were estimated using the age-specific incidence/mortality rates and corresponding populations, nationally. Age-standardized rates were calculated using the direct standardization method applying the Chinese standard population in 2000 and Segi's World standard population. The study calculated the cumulative incidence and mortality from persons 0 to 75 years old. All rates were expressed as per 100,000 person years. SAS software (Version 9.4; SAS Institute Inc., Cary, NC, USA) was used for statistical analysis. The annual percentage change (APC) of the rate was calculated for time trend analysis from 2000 to 2015 using the Joinpoint Regression Program (Version 4.5.0.1; National Cancer Institute, Rockville, MD, USA).

Results

Basic information from contributing cancer registries

In total, 501 cancer registries from 31 provinces in China submitted their 2015 cancer registration data to NCCRC, including 173 cities (urban areas) and 328 counties and county-level areas (rural areas). Data from 368 registries (134 urban and 234 rural areas) met the quality control criteria. The data covered a population of 309,553,499 persons (156,934,140 male and 152,619,359 female cancer patients; 148,804,626 in urban and 160,748,873 in rural areas), accounting for 25.52% of the national population.

Incidence and mortality rates

In 2015, there were 24,200 estimated new cases (14,000 males and 10,200 females), accounting for approximately 0.62% of all cancers. The crude incidence of primary bone tumor was 1.77/100,000, and age-standardized incidence rate relative to the Chinese population (ASIRC) and world population (ASWRC) were 1.35/100,000 and 1.32/100,000, respectively. The crude incidence of primary bone tumors was higher in rural (1.95/100,000) than in urban areas (1.63/100,000). The ASIRC in rural areas was 1.25 times higher than in urban areas [Table 1].

Table 1 - Incidence and mortality rate of primary malignant bone tumor in China, 2015.
New cases Crude rate New cases of primary malignant bone tumor/new cases of all cancers ASIRC/ASMRC ASIRW/ASMRW Cumulative rate for 0-74-year-old persons Truncated rate for 35-64-year-old persons
Rate Area Sex (×104) (1/105) (%) (1/105) (1/105) (%) (1/105) Rank among all cancers
Incidence All Both 2.42 1.77 0.62 1.35 1.32 0.13 1.65 22
Male 1.40 1.99 0.65 1.56 1.52 0.16 1.89 18
Female 1.02 1.53 0.58 1.14 1.11 0.11 1.41 20
Urban Both 1.25 1.63 0.53 1.22 1.19 0.12 1.47 22
Male 0.73 1.86 0.58 1.43 1.39 0.14 1.73 18
Female 0.52 1.38 0.48 1.01 0.98 0.10 1.19 20
Rural Both 1.17 1.95 0.75 1.52 1.48 0.15 1.93 21
Male 0.66 2.15 0.75 1.73 1.69 0.18 2.11 18
Female 0.51 1.73 0.74 1.31 1.28 0.13 1.74 20
Mortality All Both 1.79 1.31 0.77 0.90 0.89 0.10 1.05 19
Male 1.06 1.51 0.72 1.08 1.06 0.12 1.28 17
Female 0.73 1.10 0.86 0.73 0.72 0.08 0.80 17
Urban Both 0.92 1.19 0.69 0.80 0.79 0.08 0.90 19
Male 0.55 1.38 0.65 0.96 0.94 0.10 1.12 17
Female 0.37 1.00 0.76 0.65 0.64 0.07 0.68 19
Rural Both 0.87 1.45 0.87 1.04 1.02 0.11 1.25 16
Male 0.52 1.66 0.80 1.24 1.23 0.14 1.53 15
Female 0.35 1.22 0.98 0.85 0.82 0.09 0.97 15
ASIRC: Age-standardized incidence rate by Chinese standard population in 2000; ASIRW, Age-standardized incidence rate by world standard population (Segi's population); ASMRC: Age-standardized mortality rate by Chinese standard population in 2000; ASMRW: Age-standardized mortality rate by world standard population (Segi's population).

There were 17,900 estimated primary bone tumor deaths (10,600 males and 7300 females), accounting for 0.77% of all cancer-related deaths. The crude mortality rate was 1.31/100,000, and the age-standardized mortality rate relative to the Chinese population (ASMRC) and world population (ASMRW) were 0.90 and 0.89 per 100,000, respectively. The crude mortality rate was higher in rural (1.45/100,000) than that in urban areas (1.19/100,000). The ASMRC in rural areas was 1.3 times higher than in urban areas [Table 1].

Age-specific incidence and mortality

The age-specific incidence rate of primary bone tumor followed a double-peak phenomenon. The rate increased from the age of 5 years, peaked at the age of 10−14 and 15−19 years in girls and boys, respectively, and declined thereafter. The rates observed were lower for patients aged <45 years but increased dramatically from the age of 45 years and peaked at the age of 80 to 84 years in both sexes. After the age of 15 years, the age-specific incidence rates in males were higher than those in females in each age group. Among women in rural areas, the incidence trend declined in the age group of 65 to 70 years; however, overall incidence trends of the urban and rural areas were similar [Figure 1A].

F1
Figure 1:
Age-standardized to the Segi Standard Population primary bone tumor incidence (A) and mortality (B) rate in China, 2015.

The age-specific mortality rate of primary bone tumor reached a small peak in the age group of 5 to 9 years. The trend was slowly upward before the age of 45 years and rapid upward thereafter, peaking at the age of 80 to 84 years. The age-specific mortality rates were higher in rural than those in urban areas, regardless of sex, particularly among people aged >45 years. For rural subjects of both gender and urban females, age-specific mortality peaked in the 80 years. However, age-specific mortality in urban males peaked in the ≥85 years group [Figure 1B].

Trends in incidence and mortality

Trends in primary bone tumor ASIRW and ASMRW showed downward trends, with declines of 2.2% (95% confidence interval [CI], 1.4–3.0%) and 4.8% (95% CI, 3.9–5.7%) per year, respectively [Table 2].

Table 2 - Trends in primary malignant bone tumor incidence and mortality rates (age-standardized to the Segi Standard Population) by area and sex: China, 2000 to 2015.
Trend 1 Trend 2


Rate Area Sex Years APC (95% CI) Years APC (95% CI)
Incidence All 2000–2015 −2.2 (−3.0 to −1.4)
Male 2000–2015 −2.5 (−3.4 to −1.6)
Female 2000–2006 1.4 (−2.1 to 5.0) 2006–2015 −3.9 (−5.7 to −2.1)
Urban 2000–2015 −3.5 (−4.4 to −2.6)
Male 2000–2015 −3.5 (−4.6 to −2.4)
Female 2000–2015 −3.6 (−5.1 to −2.0)
Rural 2000–2003 17.5 (−1.9 to 40.8) 2003–2015 −3.2 (−5.3 to −1.1)
Male 2000–2003 14.8 (−4.2 to 37.4) 2003–2015 −2.8 (−4.9 to −0.7)
Female 2000–2007 6.8 (−0.3 to 14.4) 2007–2015 −7.0 (−12.1 to −1.7)
Mortality All 2000–2015 −4.8 (−5.7 to −3.9)
Male 2000–2015 −5.1 (−6.2 to −4.1)
Female 2000–2015 −4.3 (−5.2 to −3.4)
Urban 2000–2005 −8.9 (−11.8 to −5.9) 2005–2015 −3.1 (−4.1 to −2.0)
Male 2000–2004 −10.6 (−15.3 to −5.7) 2004–2015 −4.1 (−5.2 to −3.0)
Female 2000–2015 −3.6 (−5.1 to −2.1)
Rural 2000–2007 4.1 (−1.1 to 9.6) 2007–2015 −7.4 (−11.2 to −3.4)
Male 2000–2007 4.0 (−2.5 to 10.8) 2007–2015 −7.1 (−11.9 to −2.2)
Female 2000–2007 4.7 (−0.4 to 10.0) 2007–2015 −7.5 (−11.2 to −3.7)
The APC is significantly different from zero (P < 0.05).APC: Annual percentage change; CI: Confidence interval.

The ASIRW in males followed a significant downward trend, while in females, it remained stable at an early stage, following a significant downward trend (3.9%, 95% CI, 2.1–5.7%) thereafter. The ASMRW of primary bone tumor in both sexes also showed significant downward trends, with a decline of 5.1% (95% CI, 4.1–6.2%) per year in males and a decline of 4.3% (95% CI, 3.4–5.2%) per year in females [Table 2 and Figure 2A].

F2
Figure 2:
Trends in primary malignant bone tumor incidence and mortality (age-standardized to the Segi's Standard Population) by sex (A) and regions (B) in China, 2000 to 2015.

The incidence of primary malignant bone tumors in urban areas showed a downward trend, with a decline of 3.5% (95% CI, 3.9–5.7%) per year. Significant declining trends in mortality rates were observed in urban areas. During the 2000 to 2005 period, it decreased by 8.9% per year, and during the 2005 to 2015 period, it decreased by 3.1% annually.

However, the incidence and mortality of primary malignant bone tumors in rural areas showed stable trends at an early stage, following downward trends thereafter. The incidence of primary malignant bone tumors has been decreasing at a rate of 3.2% (95% CI, 1.1–5.3%) per year since 2003; and the mortality rate has been declining at a rate of 7.4% per year since 2007(95% CI, 3.4–11.2%) [Table 2 and Figure 2B].

The age-specific incidence (standardized to the Segi Standard Population) showed stable trends in the age group of 0 to 19 years and downward trends in age group more than 19 years old. Interestingly, the age-specific incidence in males showed upward trends before the age of 19 years (95% CI, 0.4%–3.0%) and downward trends in subjects more than 19 years old [Table 3].

Table 3 - Trends in primary malignant bone tumor incidence rates by sex and age: China, 2000 to 2015.
Sex Age (years) Years APC (95% CI)
Total All 2000–2015 −2.2 (−3.0 to −1.4)
0–19 2000–2015 1.3 (−0.2 to 2.8)
20–59 2000–2015 −2.3 (−3.7 to −0.9)
≥60 2000–2015 −3.9 (−4.7 to −3.1)
Female All 2000–2015 −2.0 (−3.1 to −1.0)
0–19 2000–2015 0.6 (−1.8 to 3.1)
20–59 2000–2015 −1.9 (−3.6 to −0.3)
≥60 2000–2015 −3.4 (−4.4 to −2.4)
Male All 2000–2015 −2.5 (−3.4 to −1.6)
0–19 2000–2015 1.7 (0.4 to 3.0)
20–59 2000–2015 −2.6 (−4.1 to −1.0)
≥60 2000–2015 −4.4 (−5.7 to −3.2)
The APC is significantly different from zero (P < 0.05).APC: Annual percentage change; CI: Confidence interval.

The age-specific mortality (age-standardized to the Segi Standard Population) rate showed decreasing trends in all age groups. Both sexes showed stable trends in the age groups of 0 to 19 years and downward trends in subjects more than 19 years old [Table 4].

Table 4 - Trends in primary malignant bone tumor mortality rates by sex and age: China, 2000 to 2015.
Sex Age (years) Years APC (95% CI)
Total All 2000–2015 −4.8 (−5.7 to −3.9)
0–19 2000–2007 −8.4 (−14.2 to −2.1)
2007–2015 5.5 (−0.1 to 11.3)
20–59 2000–2015 −5.4 (−6.3 to −4.4)
≥60 2000–2015 −5.3 (−6.2 to −4.3)
Female All 2000–2015 −4.3 (−5.2 to −3.4)
0–19 2000–2015 1.2 (−1.6 to 4.1)
20–59 2000–2015 −5.6 (−6.9 to −4.3)
≥60 2000–2015 −4.9 (−5.9 to −4.0)
Male All 2000–2015 −5.1 (−6.2 to −4.1)
0–19 2000–2015 −2.8 (−6.9 to 1.5)
20–59 2000–2015 −5.1 (−6.5 to −3.6)
≥60 2000–2015 −5.6 (−6.9 to −4.4)
The APC is significantly different from zero (P < 0.05).APC: Annual percentage change; CI: Confidence interval.

Discussion

This study estimated primary malignant bone tumors burden and trends in China based on the data of 368 local cancer registries that met the inclusion criteria. It was estimated that 24,200 new diagnosed cases (0.62% of all cancers) and 17,900 deaths from primary malignant bone tumors occurred in China in 2015 with the incidence rate of 1.77 per 100,000 and mortality rate of 1.31 per 100,000. Both age-specific incidence and mortality rates of primary malignant bone tumors showed bimodal distribution and downward trends.

Bone and joint cancer represents 0.2% of all new cancer cases in the US. The rate of new cases of bone and joint cancer was 1.00 per 100,000.[10] In our study, 24,200 cases of newly diagnosed primary malignant bone tumors were estimated, which accounted for 0.62% of all cancers, with a higher incidence in male than in female patients. The incidence of primary malignant bone tumors in England also showed a higher incidence in male than in female patients.[11] Sex differences in primary malignant bone tumors incidence may be due to hormonal regulation; specifically, the androgen receptor (AR) with CAG and GGN repeat length variation may contribute to tumorigenesis and osteosarcoma. The short AR CAG repeat length might be a risk factor for osteosarcoma in the Chinese population.[12] Compared with the incidence of bone tumors in 2014, the incidence in 2015 increased by 0.01 per 100,000, but there was no change in the ASIRC and ASIRW.[13]

Global incidence of primary malignant bone tumor data shows two peaks: one is in the second decade of life and the other is in the seventh and eighth decades of life. The second peak starts with a gradual increase after the age of 40 years. These peaks were consistent across all continents.[14] Our research also showed that the incidence of bone tumor had a bimodal age distribution. The first peak was in the age group of 10−14 and 15−19 years in girls and boys, respectively, and declined thereafter. The rates observed were lower for patients aged <45 years but increased dramatically from the age of 45 years and peaked at the age of 80 to 84 years in both sexes. These findings were similar to those of a Brazilian study. The incidence peak of osteosarcoma in female patients was earlier (10–14 years) than in male patients (15–19 years).[15] The reason for this bimodal phenomenon may be related to the pathogenesis of morphological types. Osteosarcoma and Ewing sarcoma were the most commonly diagnosed primary malignant tumors, with a relatively higher incidence in children and young people (10–24 years) than in adults. The distribution of Ewing sarcoma incidence was more clearly skewed to younger age groups than that of osteosarcoma.[16] Chondrosarcomas were more common in older age groups.[17] Yes-associated protein 1(YAP) and transcriptional co-activatorwith PDZ-binding motif (TAZ) are intracellular messengers that serve as key regulatory roles in mesenchymal stem cell development in several steps of osteochondrogenesis. As they regulate self-renewal, proliferation, migration, invasion, and differentiation of stem cells, perturbed expression of YAP/TAZ signaling components plays important roles in tumorigenesis and metastasis.[18] However, the quality of China's tumor registration data needs to be improved, and it is impossible to report the incidence and death data of tumor types.

These data indicate that such tumors may be closely related to specific age characteristics. Osteosarcoma mainly occurs during the period of sudden growth associated with puberty; it is also related to height at the time of diagnosis, suggesting that bone growth is an important factor.[19] Concurrently, the incidence of osteosarcoma is the highest during puberty, when insulin-like growth factor 1 levels are at their highest; this biological pathway is likely to play an important role in osteosarcoma etiology. Insulin-like growth factors play critical roles in carcinogenesis, and their circulating levels are associated with the risk of several cancers.[20]

In the past 10 years in the US, the annual average age-adjusted rate of new bone and joint cancer cases has increased by 0.4%.[10] In China, the incidence trend of bone tumors from 2000 to 2015 shows the opposite result, with a decrease of 2.2% per year. The age-standardized incidence rate of primary bone tumors in male showed a downward trend, while in female showed a significant downward trend after 2006. The incidence rate in urban areas showed a significant downward trend. However, in rural areas, there was a significant downward incidence trend only after 2003. Although the overall incidence rate in China shows a significant decline in our study, there are also reports that the incidence of osteosarcoma in the Qiannan Bouyei and Miao autonomous prefecture showed an upward trend from 1999 to 2018, with an annual increase of 4.8%.[21] By age group, the 0 to 39 years age group and the ≥80 years age group showed a stable incidence trend, whereas the 40 to 79 years age group showed a downward trend.

Genetic factors play a major role in the pathogenesis of osteosarcoma. A study showed that TCF21 rs12190287 polymorphism was significantly associated with a higher risk of osteosarcoma. In addition, rs12190287 polymorphism was correlated with the clinical Enneking GTM (grade–tumor site–metastasis) grade and metastasis potential of osteosarcoma, suggesting that rs12190287 polymorphism plays an important role in the carcinogenesis and progression of osteosarcoma.[22]

The incidence rate of bone tumors in the 40 to 79-year-old population is decreasing, which may be related to changes in risk factors. With the development of the economy and the improvement of people's living standards, people are paying more and more attention to their health. Reducing certain risk factors such as smoking and drinking, as well as controlling the risk of environmental and occupational carcinogens, coupled with a healthy and balanced diet and physical exercise, can significantly reduce the occurrence of cancer.[23]

In 2014, the reported crude mortality rate from bone tumors was 1.72 per 100,000, and the ASIRC was 0.88 per 100,000.[13] Compared to 2014, the mortality rate of primary malignant bone tumors in 2015 decreased by 0.41 per 100,000. The US data show that bone and joint cancer represent 0.3% of all cancer deaths. The death rate was 0.5 per 100,000 per year.[10] Compared to that reported between 2003 and 2007 (1.36/100,000), the mortality rate decreased by 0.04/100,000.[1] Similar to age-specific incidence rate, the age-specific mortality rate reached a small peak in the age group of 15 to 19 years. Mortality rates were lower before the age of 45 years and increased dramatically thereafter, peaking at the age of 80 to 84 years for both sexes.

The study shows that the trend of primary bone tumor mortality is decreasing. The death rate of primary bone tumors in urban areas has decreased every year. However, in rural areas the rate has declined since 2007. According to previous reports, during the 2003 to 2007 period, the bone tumor mortality rate decreased by 6.35%, of which the urban mortality rate decreased by 16.10% and the rural mortality rate increased by 20.36%.[1] There may be several reasons for these findings. Most rural patients have a low economic status and health literacy and tend to underuse available medical resources, such as screening and treatment services.[24] Rural residents lack the awareness of cancer risk factors and symptoms and had limited access to high quality medical resources.[25] Similar to the age-specific incidence trend, the age-specific mortality rate from primary malignant bone tumors also showed a downward trend. The decline in mortality coincides with an increase in survival from 17.1% in 2003 to 2005 to 26.5% in 2012 to 2015. Recent improvements in medical technology and an increase in the rate of early diagnosis and treatment of cancer alongside progress in research likely contribute to this trend.[26] With the current multimodality treatments, approximately three-quarters of all patients diagnosed with osteosarcoma are cured, and 90% to 95% of patients diagnosed with osteosarcoma can be successfully treated with limb-sparing approaches instead of amputation. As a result, the 5-year survival rates have improved to almost 70% in patients with localized Ewing sarcoma.[27] The reason for the increase in cancer survival rate may be related to the improvement of China's health care system and the New Cooperative Medical Scheme.[28,29]

Although the Chinese government has made great efforts to reduce the burden of cancer in China, it is still a major health problem. The different burdens by sexes and geographical regions deepen the complexity and increase the difficulty of controlling cancer effectively.[30]

This is the first study to report primary bone tumor incidence and mortality rates as well as associated trends for the period between 2000 and 2015 in China. The APC model estimated the risk of morbidity and death from primary malignant bone tumors in a specific population by simultaneously adjusting factors such as time, age, and cohort. Describing the changing trends of primary malignant bone tumors at different ages, periods, and cohorts overcomes the mutual influence of these factors in univariate analysis to some extent. Therefore, the APC model is convincing in describing disease effects and theory.

There was a limitation in our study which might challenge its reliability. The low percentage of primary malignant bone tumors cases with morphological verification was 42.43% in our study. This may be related to the much higher proportion of unspecified bone tumors in China.[13] Due to the low MV% of bone cancer in the original data, we were unable to discuss age-specific incidence rates by different types of cancer. In the future, the collection of morphological classification information will be strengthened to provide better guidance for clinicians to formulate more timely cancer prevention and control strategies.

We confirmed that primary malignant bone tumors are more common in men than in women and have a bimodal distribution with age. Adolescents and older adults constitute the groups most affected by these cancers. The age-standardized incidence and mortality rates of primary malignant bone tumors showed downward trends since 2000. The incidence and mortality rates of primary bone tumor in rural areas are higher compared to those in urban areas. Targeted prevention measures are required to monitor and control primary malignant bone tumors incidence and to improve the quality of life of affected patients. This research can provide a scientific basis for the prevention and control of primary malignant bone tumors, as well as basic information for the follow-up research.

Acknowledgements

We gratefully acknowledge the cooperation of the population-based cancer registries for their hard work on cancer registration data collection, sorting, verification, and database creation. We take full responsibility for the analyses and interpretation of these cancer registry data.

Funding

This study was supported by grants from the National Key Research and Development Program of China (No. 2018YFC1311704) and CAMS Innovation Fund for Medical Sciences (CIFMS) (No. 2018-I2M-3-003).

Conflicts of interest

None.

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Keywords:

Bone neoplasms; Incidence; Mortality; Quality of life; Registries; Age; China

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