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. 2021 Feb 10;16(2):e0246800. doi: 10.1371/journal.pone.0246800

Trends in breast cancer incidence in Ho Chi Minh City 1996–2015: A registry-based study

Dung X Pham 1,2,#, Thao-Quyen H Ho 3,‡, Tung D Bui 4,‡, Lan T Ho-Pham 5,6,*,#, Tuan V Nguyen 6,7,8,9,#
Editor: Mohammad R Akbari10
PMCID: PMC7875422  PMID: 33566857

Abstract

The burden of breast cancer in Vietnam has not been documented. This study sought to estimate the incidence of breast cancer in Ho Chi Minh City, the largest economic center of Vietnam, from 1996 to 2015. This was a population-based study using the Ho Chi Minh City Cancer Registry as a source of data (coverage period: 1996–2015). The Registry adopted the International Classification of Diseases for Oncology, 3rd Edition for the classification of primary sites and morphology, and guidelines from the International Agency for Research on Cancer and the International Association of Cancer Registries. Using the population statistics from census data of Ho Chi Minh City, the point incidence of breast cancer for 5-year period was estimated. Based on the national population, we calculated the age-standardized rate (ASR) of breast cancer between 1996 and 2015. Overall 14,222 new cases of breast cancer (13,948 women, or 98%) had been registered during the 1996–2015 period; among whom, just over half (52%) were in the 2nd stage and 26% in the 3rd and 4th stages. In women, the median age at diagnosis was 50 years and there was a slight increase over time. The ASR of breast cancer during the 2011–2015 period was 107.4 cases per 100,000 women, representing an increase of 70% compared to the rate during the 1996–2000 period. In men, there was also a significant increase in the ASR: from 1.13 during the 1996–2001 period to 2.32 per 100,000 men during the 2011–2015 period. These very first data from Vietnam suggest that although the incidence of breast cancer in Vietnam remains relatively low, it has increased over time.

Introduction

Breast cancer is the most common cancer in women worldwide. In the United States alone, projected statistics in 2019 showed that approximately 30% of all cancers in women were attributable to breast cancer [1, 2]. Moreover, in the Asia Pacific region, incomplete data indicate that breast cancer was the most common type of cancer, accounting for 18% of total cancers in women [3]. In absolute number, the International Agency for Research on Cancer (IARC) estimated that in 2018 alone, 2.1 million women were diagnosed with breast cancer, and 627 women died from the disease [4]. With the rapid aging of the population worldwide, the burden of breast cancer is expected to increase in the future.

There is a geographic disparity in the distribution of breast cancers. At present, the incidence of breast cancer in Asian populations is lower than in white populations. The age-adjusted incidence rate of cancer in Asian populations was 29 per 100,000 women, which is about a third of that in the American population (~93 per 100,000 women); however, the risk of mortality from breast cancer in Asians is higher than that in women of European descent [5]. More interestingly, Asian women tend to have breast cancer at a younger age than their white counterparts: 47% of women with a diagnosis of breast cancers aged 50 years or younger, but this proportion was 33% in the world [3].

Although there have been extensive studies on breast cancer in economically advantaged countries, the incidence, prevalence, and risk factors for breast cancer in Vietnam have not been well documented. Results from one case-control study found that breast density, age at first menarche, menopause status, number of pregnancies, number of babies born, hormone use and no physical activities were significantly associated with breast cancer in Vietnamese women [6]. Vietnam is the 15th most populous country in the world, with a population of 97 million [7]. Almost 23% of the population aged 50 years and older. However, until now, there has been no systematic documentation of the incidence of breast cancer in Vietnam over the past 20 years. In this study, we sought to estimate the incidence of breast cancer in Ho Chi Minh City, the largest city in Vietnam. Our result provides important data concerning the burden of breast cancer in the country that is rapidly transiting from an agricultural economy to a modern economy.

Study design and methods

The anonymized data for this study were extracted from the Ho Chi Minh City Cancer Registry. The Registry was established in 1990 to document all diagnosed cancer cases in the City. Cancer patients admitted to any hospital in the City were ascertained and checked for possible duplication. The coverage period was from January 1, 1996 to December 31, 2015. This study was restricted to people who were identified as residents of Ho Chi Minh City on their patient records. We focused on Ho Chi Minh City, because (i) it is the largest center of commerce in the country, with a population of 8.2 million (2014 statistics); (ii) the ascertainment and documentation of cancers in the City is more complete than any other provinces in the country; and (iii) the City offers an opportunistic setting for studying the burden of cancers in a transitional population. The study was approved by the Ethics Committee of the Oncology Hospital of Ho Chi Minh City. Because all data were anonymized no individual patient consent was required.

The Ho Chi Minh City Cancer Registry adopted the International Classification of Diseases for Oncology, 3rd Edition (ICDO-3) for the classification of primary sites and morphology, and guidelines from the International Agency for Research on Cancer and the International Association of Cancer Registries. Based on the ICDO-3, we identified breast cancer cases from 1 January 1996 to 31 December 2015 inclusive. The identification was further ascertained by tumor site code, morphology code, and behavior type.

Data from all registries was collected and assessed based on guidelines from the International Agency for Research on Cancer and the International Association of Cancer Registries, adapted to a low and middle-income context. Data was validated through clinical records, coded, and verified according to guidelines.

Age-and-gender population statistics were obtained from census data managed by the General Statistics Office (GSO) of Ho Chi Minh City. Population statistics were available for 1999, 2004, 2009, and 2014. Age-and-gender population statistics in 1999 for Vietnam were obtained from the Bureau of Statistics of Vietnam.

Using the population statistics of Ho Chi Minh City, we computed the point incidence rate of breast cancer (per 100,000 population) for each 5-year interval: 1996–2000, 2001–2005, 2006–2010, and 2011–2015 inclusive. The reason for aggregating 5-year data was to improve the stability of statistical estimates. We used the direct method of standardization to calculate the age-standardized rate (ASR), by applying the age-specific rates observed in a period to the national population in 1999. In this approach, the ASR can be thought of as a weighted average rate, with the weights being the proportion of the national population in each age group.

We employed a logistic joint point regression model [8] to identify temporal changes in the incidence of breast cancer over the coverage period. Assuming that the annual incidence of cases in the population follows the Binomial distribution, the logistic joint point regression uses the logit of the incidence rate as the dependent variable to identify the best fit for joint points (i.e., inflexion points) at which there is a significant change in trends. Based on exploratory analysis, we allowed maximum of 2 points in the model. The analyses were conducted using the R Statistical Environment [9] and "ljr" package [8].

Results

Between January 1, 1996 and December 31, 2015, 14,222 new cases of breast cancer (13,948 women, or 98%) had been registered in the Registry (Table 1). Almost 100% of cancers were classified as malignant. Based on the data on stage (n = 422 women), just over half (52%) were in the 2nd stage, and 26% of cases were in the 3rd and 4th stages.

Table 1. Clinical characteristics of 13948 women and 274 men with breast cancer in Ho Chi Minh City, 1996–2015.

Women (n = 13948) Men (n = 274) Total (n = 14222)
Type of cancer
In situ 44 (0.3%) 0 (0%) 44 (0.3%)
Malignant 13892 (99.6%) 274 (100%) 14166 (99.6%)
Uncertain 12 (0.1%) 0 (0%) 12 (0.1%)
Stage of cancer
I 87 (0.6%) 0 (0%) 87 (0.6%)
II 223 (1.6%) 4 (1.5%) 227 (1.6%)
III 69 (0.5%) 0 (0%) 69 (0.5%)
IV 43 (0.3%) 1 (0.4%) 44 (0.3%)
Unknown 13525 (97.0%) 269 (98.2%) 13794 (97.0%)
Base of Diagnostic
Biochemical/Immuno tests 6 (0.0%) 0 (0%) 6 (0.0%)
Clinical examination only 40 (0.3%) 1 (0.4%) 41 (0.3%)
Clinical test 1066 (7.6%) 25 (9.1%) 1091 (7.7%)
Cytology/Haematology 1284 (9.2%) 19 (6.9%) 1303 (9.2%)
Exploratory surgery 270 (1.9%) 6 (2.2%) 276 (1.9%)
Histology of Metastasis 214 (1.5%) 6 (2.2%) 220 (1.5%)
Histology of Primary 11033 (79.1%) 217 (79.2%) 11250 (79.1%)
Missing 35 (0.3%) 0 (0%) 35 (0.2%)
Treatment
Chemotherapy 1523 (10.9%) 27 (9.9%) 1550 (10.9%)
Hormonotherapy 38 (0.3%) 1 (0.4%) 39 (0.3%)
No treatment 2527 (18.1%) 56 (20.4%) 2583 (18.2%)
Others 80 (0.6%) 3 (1.1%) 83 (0.6%)
Radiotherapy 96 (0.7%) 24 (8.8%) 120 (0.8%)
Surgery 9543 (68.4%) 161 (58.8%) 9704 (68.2%)
Missing 141 (1.0%) 2 (0.7%) 143 (1.0%)
Status
Alive 13437 (96.3%) 260 (94.9%) 13697 (96.3%)
Dead 101 (0.7%) 4 (1.5%) 105 (0.7%)
Unknown 354 (2.5%) 10 (3.6%) 364 (2.6%)
Missing 56 (0.4%) 0 (0%) 56 (0.4%)
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Note: number in bracket represents the column-wise percentage.

The median age at diagnosis was 50 years (IQR: 43–59) and 55 years (IQR: 47–65) for women and men, respectively. In women, there was a slight but statistically significant increase in the average age of diagnosis of breast cancer between 1996 and 2015. Between 1996 and 2000, the median age at diagnosis was 49, and this was increased to 51 yrs during 2011 and 2015 (P = 0.006). Between 1996 and 2000, 48.8% of women with a breast cancer diagnosis aged 50 years and older, and this proportion was increased to 55.8% during 2011 and 2015 (Table 2).

Table 2. Age distribution of breast cancer by age group and by sex in Ho Chi Minh City, Vietnam (1996–2015).

Gender Age group 1996–2000 2001–2005 2006–2010 2011–2015
Women <30 24 (1.3) 33 (1.2) 45 (1.2) 81 (1.5)
30–39 256 (13.4) 368 (12.9) 457 (12.0) 622 (11.6)
40–49 702 (36.7) 1090 (38.3) 1310 (34.3) 1668 (31.1)
50–59 431 (22.5) 726 (25.5) 1194 (31.3) 1749 (32.6)
60–69 302 (15.8) 401 (14.1) 519 (13.6) 834 (15.5)
70–79 153 (8.0) 182 (6.4) 224 (5.9) 326 (6.1)
80+ 47 (2.5) 48 (1.7) 70 (1.8) 86 (1.6)
All ages 1915 2848 3819 5366
Men <30 0 0 2 (2.4) 1 (1.0)
30–39 3 (9.7) 10 (16.9) 4 (4.7) 7 (7.1)
40–49 10 (32.3) 9 (15.3) 22 (25.9) 24 (24.2)
50–59 8 (25.8) 12 (20.3) 26 (30.6) 29 (29.3)
60–69 7 (22.6) 13 (22.0) 10 (11.8) 23 (23.2)
70–79 2 (6.5) 10 (16.9) 18 (21.2) 14 (14.1)
80+ 1 (3.2) 5 (8.5) 3 (3.5) 1 (1.0)
All ages 31 59 85 99
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Note: numbers in brackets represent the sex-specific percent of the total for each 5-year interval.

Joint point regression analysis identified 2 breakpoints, 1999 and 2005, in the incidence of breast cancer in women throughout 1996–2015 (Fig 1). The average rates of increase in the incidence during the period of 1996–1999, 2000–2005, and 2006–2015 were 0.019, 0.001, and 0.013, respectively.

Fig 1. Estimated annual incidence rate of breast cancer (per 1000 population) in women during the 1996–2015 period in Ho Chi Minh City.

Fig 1

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In women, the 5-year age-standardized incidence rate of breast cancer was 62.2 cases per 100,000 population during the 1996–2000 period, and this was progressively increased to 107.4 during the 2011–2015 period, representing a 70% increase over the 20-year period. In men, there was also a significant increase in the age-standardized incidence rate: from 1.13 during the 1996–2001 period to 2.32 during the 2011–2015 period, representing an increase of 2.1-fold (Table 3).

Table 3. Unadjusted and standardized incidence rate (per 100,000 persons over 5 years) of breast cancer in Ho Chi Minh City (1996–2015) stratified by gender.

Gender Estimate 1996–2000 2001–2005 2006–2010 2011–2015
Women Unadjusted 73.3 (1.67) 89.7 (1.68) 102.5 (1.66) 137.1 (1.87)
Standardized 62.2 (0.38) 72.5 (0.41) 79.3 (0.43) 107.4 (0.51)
Rate Ratio 1.00 1.20 1.30 1.70
Men Unadjusted 1.28 (0.23) 2.01 (0.26) 2.47 (0.27) 2.74 (0.28)
Standardized 1.13 (0.05) 1.77 (0.06) 2.01 (0.07) 2.32 (0.08)
Rate Ratio 1.00 1.60 1.80 2.10
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Note: numbers in brackets represent standard error.

Discussion

It has been projected that economically less developed countries are going to bear a greater burden of breast cancer than more developed countries [10]. However, research on risk factors for and incidence of breast cancer in population among less developed countries have been scarce. In this study, by using a well-characterized registry-based data of the largest city in Vietnam, we have shown that over the past 20 years, the incidence of breast cancer had increased by 70% and that the increase was mainly attributable to those age groups of 50 and 70. These very first results from Vietnam deserves further elaboration.

It seems clear that the age-standardized incidence of breast cancer in this study is lower than that in white populations. For instance, in the United States, between 2009 and 2016, the age-standardized incidence rate was approximately 200 per 100,000 woman-years [11] which is higher than in Australia (~131 per 100,000 women) [12]. In China, the age-standardized incidence of breast cancer was observed at 28.4 per 100,000 women [13]. In Vietnam’s neighboring country Thailand, the incidence rate was estimated to be 31.2 per 100,000 woman-years [14]. In our study, the annualized age-standardized incidence rate was 21.5 per 100,000 women throughout 2011 and 2015, which can still be considered low relative to populations in more economically developed countries.

We found that the incidence of breast cancer in our cohort had been increasing over time, and this trend is consistent with previous observations [15–17]. In the 1996–2000 period, the age-standardized incidence rate was 12.4 per 100,000 women which is comparable with a previous estimate [18]. However, 20 years later, this incidence was increased by almost two-fold. It has been projected that the incidence of all cancers in the two major cities of Vietnam will be increased by approximately 17% over the next 5 years [19]. The increase in breast cancer incidence rates has been found in China, Japan, and Thailand [20]. This increase in the incidence plus the large population sizes in Asia imply that more cancer cases will be observed in Asian populations than in white populations. The increase in life expectancy and the aging of the population contribute three-fifths and the increased age-standardized rates contribute two-fifths of future trend [21]. If this assumption holds and given the improvement in life expectancy in Vietnamese women (~79.4 years) [22], it is expected that breast cancer will impose a heavy burden in Vietnam shortly. The increase in cancer incidence could also reflect better registration of cases and/or public awareness over the coverage period.

The age structure of cancer cases in our cohort merits a comment. We found that the median age at diagnosis of breast cancer was 50 years (in women), which is almost identical to the median age at diagnosis of breast cancer among Singaporean [23] and Korean [24] women. In economically more developed countries, the average age at breast cancer diagnosis was ~54 years [25] or 59 years [26]. Thus, our finding reaffirms the common ’law’ that Asian women tended to have breast cancer at a younger age than their white counterparts.

Almost 100% of breast cancer tumors in this study were in the invasive stage, only 0.3% was in situ, and 26% of cases were diagnosed at late stage III and IV. The proportion of in-situ tumors was 16% in the United States [27] and 14% in South Korea [24]. Delayed diagnosis of cancer is a major factor that contributes to the increased risk of premature death, lower cancer survival and increases the burden of cancer. Indeed, the overall 5-year relative survival rate is 99% for localized disease, 85% for regional disease and 27% for distant-stage disease [28]. Our finding implies that a more aggressive screening strategy for identifying cancer cases earlier is warranted.

Our findings should be interpreted within the context of the study’s strengths and weaknesses. The data were ascertained from a well-developed registry that could capture total cancer incidence in Ho Chi Minh City. It is worth noting that virtually all breast cancer cases are treated at hospitals within the City, with a very small proportion being treated overseas, and the data were therefore likely complete. However, a caveat of the study is that we could not follow individual patients to ascertain their survival status, and as a result, we could not analyze the rate of mortality among these patients. Moreover, our finding concerning incidence may not be generalized to rural or non-urban areas where the incidence is expected to be lower than that in urban areas.

In conclusion, our registry-based data suggest that although breast cancer incidence in Ho Chi Minh City remained relatively low compared to white populations, there was an increasing trend up to 70% over the past 20 years. Our data also confirm that Vietnamese women tend to have breast cancer at younger ages compared to white women. These findings imply that breast cancer screening should be targeted women of younger ages.

Acknowledgments

We gratefully acknowledge the assistance of the Ho Chi Minh City Oncology Hospital, Vietnam.

Data Availability

Data from all registries was collected and assessed based on guidelines from the International Agency for Research on Cancer and the International Association of Cancer Registries, adapted to a low and middle-income context. Registry data are stored in a computerized data at the Oncology Hospital of Ho Chi Minh City. The dataset includes the following variables: age, sex, diagnosis, year of diagnosis, cancer stage, treatment, and survival status. All authors had no special access privileges in accessing these datasets which other interested researchers would not have. Age-and-gender population statistics were obtained from census data managed by the General Statistics Office (GSO) of Ho Chi Minh City. Age-and-gender population statistics in 1999 for Vietnam was obtained from the Bureau of Statistics of Vietnam. There is no URL for the population data. However, request for data access can be made to the General Statistics Office of Ho Chi Minh City, contact through email tdnlinh@ump.edu.vn.

Funding Statement

The authors received no specific funding for this work.

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Trends in breast cancer incidence in Ho Chi Minh City 1996 - 2015: a registry-based study

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We will update your Data Availability statement to reflect the information you provide in your cover letter.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: No

Reviewer #2: Yes

Reviewer #3: No

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

Reviewer #2: Yes

Reviewer #3: No

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

Reviewer #3: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

Reviewer #2: Yes

Reviewer #3: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The research was only a descriptive analysis of the number of newly discovered breast cancer patients, not a cohort study as described in the method. Data was not analysed nor discussed in any depths other than age standardized and age specific. More should be done in depth of lag time, time of diagnosis, diagnosis reason and age of diagnosis from these supposedly complete data from that long period of time that can yield so much more than a simple analysis like this. Plus, the screening strategy over that long period of time should be explained in details to rule out any bias and confoundings in the finding of increasing/decreasing incidence rate.

Reviewer #2: The author need to include the approved decision from Ethics Committee.

The author need to explain more how they do the standardized estimation (result in table 3) especially total of those who come for screening for cancel was not showed.

Some text error recorded e.g (end of page 5, table 3 - unadjusted and some where else)

Reviewer #3: Comments for article “Trends in breast cancer incidence in Ho Chi Minh City 1996 - 2015: a registry-based study”

This article deals with the evolution of breast cancer incidence in Ho Chi Minh City of Vietnam country between 1996 to 2015. This is an important issue, since such analyses enable a measurement of the burden for the health system, to make choices for health policy.

Nevertheless, such analyses require three major things that also need to address in this article

1. How far are the data reliable? How can we be sure of the exhaustivity of the data, from 1996 to 2015 in specified country? The effects observed may be just an effect of a better registration of the cancer cases. A detailed description of methods of registration in that country should be provided, to discuss the evolution of incidence rates.

2. To discuss the observed trends, we need information about health facilities in underline country and health policy concerning breast cancer.

3. The application of relevant statistical methods are major concern to get the precise results.

Therefore, last two points are lacking and make this work difficult to appreciate, although the subject is of real importance and manuscript comprises of a large data set but needs major revision in terms of data analysis, technical writing, sentence structure improvement, and removal of grammatical errors.

Major highlights are pointed out as follow:

Introduction

Line 79-80: “Vietnam is the 15th most populous country in the world, with a population of

97 million (2020 statistics). Please Cite reference here.

Additionally, breast cancer risk factors should also be addressed in introduction.

Study design and method

This section needs to include relevant statistical methods used for data analysis. It is recommended that use median and IQR for nonparametric data (age diagnosis) and use kruskal wallis test to measure the difference among age groups of diagnosed cases in case of scale measurements and use chi-square where percentages are compared. Further, Join-point regression can be used for trend analysis.

Line 115-116 “we computed the point incidence of breast cancer for each 5-year period… 2010, and 2011 - 2015 inclusive”. Briefly, mention how that incidence rate was calculated?

Line 118-119: “we calculated the age-standardized incidence rate for each of the 4 periods…” How age-standardized incidence rate was calculated?

Line 119-121: “We also employed a segmented Poisson regression model to estimate the change in the incidence of breast cancer over time. All statistical analyses were conducted using the R Statistical Environment….”.

It is recommended that use join-point regression technique and report your results in form of estimated annual percentage change (EAPC) with 95% UI. Please mention R version and package name that used for analysis.

Results

Line 125: findings (13,498 women, or 95%) and same in abstract, are inconsistent with results calculated in Table 1. (Table 1 has 13,948 women, 98%). Additionally report p-value of test difference and chi-square value.

Line 133-138, “The average at diagnosis was 52 years (SD 11.6) and 56.3 years (13.4) for women and men, respectively. In women, there was a slight but statistically significant increase …….(Table 2)”.

Firstly, data is nonparametric so authors should report median with IQR for age diagnosis, rather than mean and SD. Author reported median age in abstract but results section included mean age? Please be consistent. Authors reported that “in women statistically significant increase in the average age of diagnosis of breast cancer during 1996 and 2015….”. This difference look non-significant; please report p-value with test statistic value. Also, include these results in Table. Table 2 can be revised using joint-point regression estimate (EAPC with 95%UI for each duration).

Line:143-149: “Segmented regression indicated that there were two trends in the incidence of breast cancer in women: the first period occurred between ….(Figure 1). Further analysis showed that there was a statistically significant increase in the age-specific incidence of breast cancer over the period of 1996 and 2015, and the increase ….(Figure 2). In women, the increase in the age-specific incidence rate was observed among those aged…..”.

Join-point regression is widely used trend analysis technique and segmented regression is a part of it. Therefore, it is suggested that use main name of the technique for convenience of the readers.

Figure 1 and 2 , are not readable. A better presentation is needed here. Author should draw the trends across ages, years and cohort by year and age group (e.g. within age Group, within year and within cohort). Through these 3 figures Table 2 results can be well representative.

Line 160: Table 3. Briefly explain how the standardization was performed (ASR)?

Conclusion

Line 53-54: “These very first data from Vietnam suggest that although the incidence of breast cancer in Vietnam remains relatively low, it has increased over time, and that the increase was mainly attributable to those age groups of 50 and 70”.

Finally, authors concluded that “Our data also confirm that Vietnamese women tend to have breast cancer at younger ages compared to Caucasian women”. Younger ages? Conclusion is not consistent with the findings. (Further, most of the GBD studies reported that women breast cancer is more prevalent in older ages worldwide). Make any changes to the abstract that align with those made in the text.

Minor comments

Line 34: Revise sentence structure (In line with the related literature, for example, see following literature)

1. (Nguyen TP, Luu HN, Nguyen MV, Tran MT, Tuong TT, Tran CT, Boffetta P. Attributable Causes of Cancer in Vietnam. JCO global oncology. 2020 Feb;6:195-204.

2. Nguyen SM, Deppen S, Nguyen GH, Pham DX, Bui TD, Tran TV. Projecting cancer incidence for 2025 in the 2 largest populated cities in Vietnam. Cancer Control. 2019 Jul 22;26(1):1073274819865274.

3. Pham T, Bui L, Kim G, Hoang D, Tran T, Hoang M. Cancers in Vietnam—burden and control efforts: a narrative scoping review. Cancer Control. 2019 Jul 17;26(1):1073274819863802.)

Line 51: age-standardized incidence rate, replace it with ASR as its already mentioned in the abstract.

Line 55: those age groups of 50 and 70 years…

Line 60: 2019 showed that approx……..

Line 61: improper sentence structure.. What is meant by was also the most..?

Line 69: is lower than in Caucasian populations…….. remove “in”

Line 71 & 72. Mention reference 5 once after the completion of related information.

Line 73: women tends to have breast cancer in …….

Line 125: write as 1st Jan. 1996……

Line 127-128: Rewrite these lines

Line 133: word age is missing, modify as … The average age at diagnosis was 52 years ….

Line 145: later instead of latter

158: repetitive words in one sentence

Line 189: revise the sentence

198: unable to understand the statement

Line 202: Asian women tends to ….

Line 224: cancer incidence rates in Vietnam's urban population remain …..

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

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Attachment

Submitted filename: Comments for Trends in breast cancer incidence....pdf

Click here for additional data file. (221.5KB, pdf)
PLoS One. 2021 Feb 10;16(2):e0246800. doi: 10.1371/journal.pone.0246800.r002

Author response to Decision Letter 0

3 Nov 2020

Reviewer 1

"The research was only a descriptive analysis of the number of newly discovered breast cancer patients, not a cohort study as described in the method. Data was not analysed nor discussed in any depths other than age standardized and age specific. More should be done in depth of lag time, time of diagnosis, diagnosis reason and age of diagnosis from these supposedly complete data from that long period of time that can yield so much more than a simple analysis like this. Plus, the screening strategy over that long period of time should be explained in details to rule out any bias and confoundings in the finding of increasing/decreasing incidence rate."

Authors: The Reviewer is correct that this study was a descriptive analysis of breast cancer incidence using a registry data base. Because the data were derived from a registry, it was not possible to have a complete clinical data such as reason for diagnosis or lag time. The data were not from a screening program.

Although the study is descriptive in nature, the data are very important. These data represent the first documentation of breast cancer incidence from Vietnam. Because of its descriptive nature, we mainly employed descriptive statistical methods that are also used by virtually all previous studies.

Reviewer 2

"The author need to include the approved decision from Ethics Committee."

Authors: The study was indeed approved by the hospital ethics committee. We have now included the approval.

"The author need to explain more how they do the standardized estimation (result in table 3) especially total of those who come for screening for cancel was not showed."

Authors: We have expanded the Methods section to describe the computation of age-standardized rate.

"Some text error recorded e.g (end of page 5, table 3 - unadjusted and somewhere else)"

Authors: Thank you. We have gone through the manuscript and corrected all mis-spelling words.

Reviewer 3

"This article deals with the evolution of breast cancer incidence in Ho Chi Minh City of Vietnam country between 1996 to 2015. This is an important issue, since such analyses enable a measurement of the burden for the health system, to make choices for health policy. Nevertheless, such analyses require three major things that also need to address in this article."

Authors: Thank you for your positive remarks on our work. Indeed, the incidence of cancer in Vietnam has not been well documented. We hope that this paper provides data pertaining to the most important cancer (i.e. breast cancer) in Saigon, a major city in Vietnam, and that the data will help future planning of cancer prevention.

"1. How far are the data reliable? How can we be sure of the exhaustivity of the data, from 1996 to 2015 in specified country? The effects observed may be just an effect of a better registration of the cancer cases. A detailed description of methods of registration in that country should be provided, to discuss the evolution of incidence rates."

Authors: We cannot really comment on the degree of accuracy of the data. However, under the assumption that patients affected by cancer seek medical attention, we can confirm that the registry captures virtually all cancer cases in Ho Chi Minh City. However, as the reviewer mentions, the increase in the incidence could be due to better ascertainment and public awareness, and this is now mentioned in the Discussion. We have now extended the description of the registry in the Methods section.

"2. To discuss the observed trends, we need information about health facilities in underline country and health policy concerning breast cancer."

Authors: In Ho Chi Minh City, all major hospitals provide care to patients affected by cancer.

"3. The application of relevant statistical methods are major concern to get the precise results.

Therefore, last two points are lacking and make this work difficult to appreciate, although the subject is of real importance and manuscript comprises of a large data set but needs major revision in terms of data analysis, technical writing, sentence structure improvement, and removal of grammatical errors."

Authors: This is a descriptive study, and we have employed descriptive statistical methods. We consider that more advanced statistical methods are not necessary for this type of study. We have now gone through the manuscript again, and corrected all errors.

"Major highlights are pointed out as follow:

Introduction

Line 79-80: "Vietnam is the 15th most populous country in the world, with a population of 97 million (2020 statistics). Please Cite reference here."

Authors: We have inserted a reference.

"Additionally, breast cancer risk factors should also be addressed in introduction."

Authors: We consider that risk factor discussion is not relevant in this paper, because the paper does not address the issue of risk factors for breast cancer.

"Study design and method

This section needs to include relevant statistical methods used for data analysis. It is recommended that use median and IQR for nonparametric data (age diagnosis) and use kruskal wallis test to measure the difference among age groups of diagnosed cases in case of scale measurements and use chi-square where percentages are compared. Further, Join-point regression can be used for trend analysis."

Authors: We have used the joint-point regression analysis. All other analyses were mainly descriptive. Classical tests such as Chi-square, Kruskal-Wallis oneway ANOVA are for hypothesis testing. Here, we do not test any scientific hypothesis, and those tests are not necessary.

"Line 115-116 "we computed the point incidence of breast cancer for each 5-year period… 2010, and 2011 - 2015 inclusive". Briefly, mention how that incidence rate was calculated?

Line 118-119: "we calculated the age-standardized incidence rate for each of the 4 periods…" How age-standardized incidence rate was calculated?"

Authors: The calculation of age-standardized rate was based on the direct method of standardization, which is straightforward for basic epidemiologic studies. We however have described the calculation in the Methods section.

"Line 119-121: "We also employed a segmented Poisson regression model to estimate the change in the incidence of breast cancer over time. All statistical analyses were conducted using the R Statistical Environment….".

It is recommended that use join-point regression technique and report your results in form of estimated annual percentage change (EAPC) with 95% UI. Please mention R version and package name that used for analysis."

Authors: There are many methods to identify inflexion point in time series analysis, and joint point regression is one of them. We have now used the joint-point logistic regression analysis.

"Line 125: findings (13,498 women, or 95%) and same in abstract, are inconsistent with results calculated in Table 1. (Table 1 has 13,948 women, 98%). Additionally report p-value of test difference and chi-square value."

Authors: Thank you for spotting this error. The actual number was 13,948 or 98% of total. There was no hypothesis in this study, and we don't think P-value is relevant here.

"Line 133-138, "The average at diagnosis was 52 years (SD 11.6) and 56.3 years (13.4) for women and men, respectively. In women, there was a slight but statistically significant increase ……. (Table 2)"."

Authors: Thank you. We have now reported the trend.

"Firstly, data is nonparametric so authors should report median with IQR for age diagnosis, rather than mean and SD. Author reported median age in abstract but results section included mean age? Please be consistent. Authors reported that "in women statistically significant increase in the average age of diagnosis of breast cancer during 1996 and 2015….". This difference look non-significant; please report p-value with test statistic value. Also, include these results in Table. Table 2 can be revised using joint-point regression estimate (EAPC with 95%UI for each duration)."

Authors: We are not sure of the comment of "data is non-parametric'. In this dataset, the mean and median were highly comparable, and this is expected for a continuous variable such as age. However, we agree with the reviewer that the median is a better statistic. We have now reported the median age at diagnosis, and P-value based on the linear regression model.

"Line:143-149: "Segmented regression indicated that there were two trends in the incidence of breast cancer in women: the first period occurred between ….(Figure 1). Further analysis showed that there was a statistically significant increase in the age-specific incidence of breast cancer over the period of 1996 and 2015, and the increase ….(Figure 2). In women, the increase in the age-specific incidence rate was observed among those aged….".

Join-point regression is widely used trend analysis technique and segmented regression is a part of it. Therefore, it is suggested that use main name of the technique for convenience of the readers."

Authors: We realize that joint-point regression is commonly used in trend analysis. However, this is a purely descriptive study, and we consider that such an analysis is not our main focus. A simple plot of incidence against year is good enough to see a change point. Nevertheless, we have now provided a result of joint-point regression analysis. We emphasize that our aim is to provide actual data on the burden of breast cancer; we are not interested in statistical exercises.

"Figure 1 and 2 , are not readable. A better presentation is needed here. Author should draw the trends across ages, years and cohort by year and age group (e.g. within age Group, within year and within cohort). Through these 3 figures Table 2 results can be well representative."

Authors: We agree with the reviewer. We have removed both figures from the manuscript.

"Line 160: Table 3. Briefly explain how the standardization was performed (ASR)?"

Authors: This has been described in the Methods section.

"Conclusion

Line 53-54: "These very first data from Vietnam suggest that although the incidence of breast cancer in Vietnam remains relatively low, it has increased over time, and that the increase was mainly attributable to those age groups of 50 and 70"."

"Finally, authors concluded that "Our data also confirm that Vietnamese women tend to have breast cancer at younger ages compared to Caucasian women". Younger ages? Conclusion is not consistent with the findings. (Further, most of the GBD studies reported that women breast cancer is more prevalent in older ages worldwide). Make any changes to the abstract that align with those made in the text."

Authors: We consider that our conclusion is consistent with the data. However, we have removed the sentence "and that the increase was mainly attributable to those age groups of 50 and 70". The median age at diagnosis of breast cancer in this study was 50, whereas in the United States and Australia, this figure is 56-62.

"Minor comments

Line 34: Revise sentence structure (In line with the related literature, for example, see following literature)

1. (Nguyen TP, Luu HN, Nguyen MV, Tran MT, Tuong TT, Tran CT, Boffetta P. Attributable Causes of Cancer in Vietnam. JCO global oncology. 2020 Feb;6:195-204.

2. Nguyen SM, Deppen S, Nguyen GH, Pham DX, Bui TD, Tran TV. Projecting cancer incidence for 2025 in the 2 largest populated cities in Vietnam. Cancer Control. 2019 Jul 22;26(1):1073274819865274.

3. Pham T, Bui L, Kim G, Hoang D, Tran T, Hoang M. Cancers in Vietnam-burden and control efforts: a narrative scoping review. Cancer Control. 2019 Jul 17;26(1):1073274819863802.)"

Authors: We have mentioned the papers in the Introduction.

"Line 51: age-standardized incidence rate, replace it with ASR as its already mentioned in the abstract."

Authors: Thank you.

"Line 55: those age groups of 50 and 70 years…"

"Line 60: 2019 showed that approx…….."

"Line 61: improper sentence structure.. What is meant by was also the most..?"

"Line 69: is lower than in Caucasian populations…….. remove "in"."

"Line 71 & 72. Mention reference 5 once after the completion of related information."

"Line 73: women tends to have breast cancer in ……."

"Line 125: write as 1st Jan. 1996……"

"Line 127-128: Rewrite these lines"

"Line 133: word age is missing, modify as … The average age at diagnosis was 52 years …."

"Line 145: later instead of latter"

"158: repetitive words in one sentence"

"Line 189: revise the sentence"

"198: unable to understand the statement"

"Line 202: Asian women tends to …."

"Line 224: cancer incidence rates in Vietnam's urban population remain ….."

Authors: Thank you so much for your helpful remarks. We have modified the sentences as indicated. We greatly appreciate the reviewer's meticulous comments and helpful suggestions.

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file. (20.8KB, docx)

Decision Letter 1

Mohammad R Akbari

20 Jan 2021

PONE-D-20-16460R1

Trends in breast cancer incidence in Ho Chi Minh City 1996 - 2015: a registry-based study

PLOS ONE

Dear Dr. Ho-Pham,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

There are some more issues related to this manuscript according to the first reviewer that need to be addressed. There are also some writing corrections suggested by the second reviewer in the attached file.

==============================

Please submit your revised manuscript by Mar 06 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Mohammad R. Akbari

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

Reviewer #3: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: The article remain several spelling and gramma error. Some technical error mention in commend should be addressed (attached track-change version).

Reviewer #3: The authors have improved the presentation of their work and answered most of my queries satisfactorily. However, I remain very concern about the following points. Therefore, before it can be published, the following points need to clarify in the manuscript.

1. Where authors use the word significant or statistical significant with the results reported, give the p-value or 95% uncertainty interval with that findings, e.g. line 50, 145.

2. For better presentation of results in table 2 it is suggest to authors, insert one column in Table 2 with p-value heading and report p value there for women and men separately, that will indicate the significant difference among periods by ages.

3. To make article results more interesting for readers, I would like to suggest to authors, also draw estimated annual incidence rate by cancer type, e.g. compare Malignant and other cancer type trend (like figure 1), If authors have sufficient data for type of cancer by period.

4. Line 48, Authors reported, “The ASR of breast cancer during 2011-2015 period was 21.5 cases per 100,000 women…”. Why the ASR reported in line 48 and in Table 3 are inconsistent, e.g. women ASR during 2011-2015. Brief clarification needed on how these ASR was calculated? Also need to clarify or fix this confusion.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: Yes: Pham Quang Thai

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

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PLoS One. 2021 Feb 10;16(2):e0246800. doi: 10.1371/journal.pone.0246800.r004

Author response to Decision Letter 1

22 Jan 2021

"Reviewer #2: The article remain several spelling and gramma error. Some technical error mention in commend should be addressed (attached track-change version)."

Authors: Thank you very much for your help and the track changes. We have gone through the changes and corrected them. We however want to retain some technical terms (eg 'inflexion point', 'ljr', "individual person's data").

"Reviewer #3: The authors have improved the presentation of their work and answered most of my queries satisfactorily. However, I remain very concern about the following points. Therefore, before it can be published, the following points need to clarify in the manuscript.

1. Where authors use the word significant or statistical significant with the results reported, give the p-value or 95% uncertainty interval with that findings, e.g. line 50, 145."

Authors: As we stated previously, this study aimed at describing the trend of breast cancer incidence over the 1996-2015 period; it was not designed to test any hypothesis that requires P-value.

"2. For better presentation of results in table 2 it is suggest to authors, insert one column in Table 2 with p-value heading and report p value there for women and men separately, that will indicate the significant difference among periods by ages."

Authors: This table is purely descriptive. The table is not meant to test any hypothesis. We consider that the actual ASR data are much more important and much more informative than any P-value which is largely sample size dependent.

"3. To make article results more interesting for readers, I would like to suggest to authors, also draw estimated annual incidence rate by cancer type, e.g. compare Malignant and other cancer type trend (like figure 1), If authors have sufficient data for type of cancer by period."

Authors: We appreciate your suggestion. However, more than 99% of the cases were malignant; only 0.3% were classified as in-situ.

"4. Line 48, Authors reported, "The ASR of breast cancer during 2011-2015 period was 21.5 cases per 100,000 women…". Why the ASR reported in line 48 and in Table 3 are inconsistent, e.g. women ASR during 2011-2015. Brief clarification needed on how these ASR was calculated? Also need to clarify or fix this confusion."

Authors: The number quoted in the Abstract is the ASR per year, whereas the number quoted in table 3 refers to the 5-year ASR (2011-2015 period). For consistency, we have used the 5-year rate in the Abstract.

Attachment

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Decision Letter 2

Mohammad R Akbari

27 Jan 2021

Trends in breast cancer incidence in Ho Chi Minh City 1996 - 2015: a registry-based study

PONE-D-20-16460R2

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Acceptance letter

Mohammad R Akbari

1 Feb 2021

PONE-D-20-16460R2

Trends in breast cancer incidence in Ho Chi Minh City 1996 - 2015: a registry-based study 

Dear Dr. Ho-Pham:

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    Attachment

    Submitted filename: Comments for Trends in breast cancer incidence....pdf

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    Attachment

    Submitted filename: Response to Reviewers.docx

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    Submitted filename: Manuscript (Clean).docx

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    Attachment

    Submitted filename: Response to comments.docx

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    Data Availability Statement

    Data from all registries was collected and assessed based on guidelines from the International Agency for Research on Cancer and the International Association of Cancer Registries, adapted to a low and middle-income context. Registry data are stored in a computerized data at the Oncology Hospital of Ho Chi Minh City. The dataset includes the following variables: age, sex, diagnosis, year of diagnosis, cancer stage, treatment, and survival status. All authors had no special access privileges in accessing these datasets which other interested researchers would not have. Age-and-gender population statistics were obtained from census data managed by the General Statistics Office (GSO) of Ho Chi Minh City. Age-and-gender population statistics in 1999 for Vietnam was obtained from the Bureau of Statistics of Vietnam. There is no URL for the population data. However, request for data access can be made to the General Statistics Office of Ho Chi Minh City, contact through email tdnlinh@ump.edu.vn.

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