Development and validation of a nomogram to predict survival after neoadjuvant chemotherapy in elderly women with triple-negative invasive ductal breast cancer: A SEER population-based study

Ying Gao; Jinmiao Wang; Shoujun Wang; Weijie Tao; Ran Duan; Jie Hao; Ming Gao

doi:10.15537/smj.2025.46.1.20240341

References

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1. Arnold M,
2. Morgan E,
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Current and future burden of breast cancer: global statistics for 2020 and 2040. Breast 2022; 66: 15-23.
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1. Giaquinto AN,
2. Sung H,
3. Miller KD,
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Breast cancer statistics, 2022. CA Cancer J Clin 2022; 72: 524-541.
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4.↵
1. Yoon J,
2. Knapp G,
3. Quan ML,
4. Bouchard-Fortier A
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5.↵
1. Baranova A,
2. Krasnoselskyi M,
3. Starikov V,
4. Kartashov S,
5. Zhulkevych I,
6. Vlasenko V, et al.
Triple-negative breast cancer: current treatment strategies and factors of negative prognosis. J Med Life 2022; 15: 153-161.
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6.↵
1. Chen Y,
2. Qi Y,
3. Wang K
. Neoadjuvant chemotherapy for breast cancer: an evaluation of its efficacy and research progress. Front Oncol 2023; 13: 1169010.
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7.↵
1. Biganzoli L,
2. Battisti NML,
3. Wildiers H,
4. McCartney A,
5. Colloca G,
6. Kunkler IH, et al.
Updated recommendations regarding the management of older patients with breast cancer: a joint paper from the European Society of Breast Cancer Specialists (EUSOMA) and the International Society of Geriatric Oncology (SIOG). Lancet Oncol 2021; 22: e327-e340.
OpenUrl CrossRef PubMed
8.↵
1. Zhao J,
2. Yang Y,
3. Pang D,
4. Yu Y,
5. Lin X,
6. Chen K, et al.
Development and validation of a nomogram in survival prediction among advanced breast cancer patients. Ann Transl Med 2020; 8: 1446.
OpenUrl PubMed
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1. Lin S,
2. Mo H,
3. Li Y,
4. Guan X,
5. Chen Y,
6. Wang Z, et al.
Development and validation of a nomogram for predicting survival of advanced breast cancer patients in China. Breast 2020; 53: 172-180.
OpenUrl PubMed
10.↵
1. Zhu Y,
2. Wang J,
3. Xu B
. A novel prognostic nomogram for predicting survival of hormone receptor-positive and HER2 negative advanced breast cancer among the Han-population. Front Oncol 2022; 12: 918759.
OpenUrl PubMed
11.↵
1. Yin F,
2. Wang S,
3. Hou C,
4. Zhang Y,
5. Yang Z,
6. Wang X
. Development and validation of nomograms for predicting overall survival and cancer specific survival in locally advanced breast cancer patients: a SEER population-based study. Front Public Health 2022; 10: 969030.
OpenUrl PubMed
12.↵
1. Wang Z,
2. Xing L,
3. Luo X,
4. Ren G
. A nomogram for survival prediction in 275,812 U.S. patients with breast cancer: a population-based cohort study based on the SEER database. Gland Surg 2022; 11: 1166-1179.
OpenUrl PubMed
13.↵
1. Obidiro O,
2. Battogtokh G,
3. Akala EO
. Triple negative breast cancer treatment options and limitations: future outlook. Pharmaceutics 2023; 15: 1796.
OpenUrl PubMed
14.↵
1. Yang R,
2. Wu Y,
3. Qi Y,
4. Liu W,
5. Huang Y,
6. Zhao X, et al.
A nomogram for predicting breast cancer specific survival in elderly patients with breast cancer: a SEER population-based analysis. BMC Geriatr 2023; 23: 594.
OpenUrl PubMed
15.↵
1. Wang H,
2. Xia GF,
3. Zhang ZR,
4. Luo X,
5. Zhu JY,
6. Wang HK
. Development and validation of a prognostic nomogram for breast cancer patients who underwent chemoradiotherapy and surgery: a retrospective cohort study based on the SEER database and 2 Chinese cohorts. Am J Cancer Res 2023; 13: 5065-5081.
OpenUrl PubMed
16.↵
1. Extermann M,
2. Leeuwenburgh C,
3. Samiian L,
4. Sehovic M,
5. Xu J,
6. Cubitt C, et al.
Impact of chemotherapy on medium-term physical function and activity of older breast cancer survivors, and associated biomarkers. J Geriatr Oncol 2017; 8: 69-75.
OpenUrl PubMed
17.↵
1. Williams AD,
2. Dang CT,
3. Sevilimedu V,
4. Morrow M,
5. Barrio AV
. Neoadjuvant chemotherapy for breast cancer in the elderly: are we accomplishing our treatment goals? Ann Surg Oncol 2022; 29: 8002-8011.
OpenUrl PubMed
18.↵
1. Assunção Ribeiro da Costa RE,
2. Rocha de Oliveira FT,
3. Nascimento Araújo AL,
4. Vieira SC
. Impact of pathologic complete response on the prognosis of triple-negative breast cancer patients: a cohort study. Cureus 2023; 15: e37396.
OpenUrl PubMed
19.
1. Huang M,
2. O’Shaughnessy J,
3. Zhao J,
4. Haiderali A,
5. Cortes J,
6. Ramsey S, et al.
Evaluation of pathologic complete response as a surrogate for long-term survival outcomes in triple-negative breast cancer. J Natl Compr Canc Netw 2020; 18: 1096-1104.
OpenUrl PubMed
20.↵
1. Houvenaeghel G,
2. de Nonneville A,
3. Cohen M,
4. Sabiani L,
5. Buttarelli M,
6. Charaffe E, et al.
Neoadjuvant chemotherapy for breast cancer: pathologic response rates but not tumor size, has an independent prognostic impact on survival. Cancer Med 2024; 13: e6930.
OpenUrl
21.↵
1. Van den Ende NS,
2. Nguyen AH,
3. Jager A,
4. Kok M,
5. Debets R,
6. van Deurzen CHM
. Triple-negative breast cancer and predictive markers of response to neoadjuvant chemotherapy: a systematic review. Int J Mol Sci 2023; 24: 2969.
OpenUrl CrossRef PubMed
22.↵
1. Von Waldenfels G,
2. Loibl S,
3. Furlanetto J,
4. Machleidt A,
5. Lederer B,
6. Denkert C, et al.
Outcome after neoadjuvant chemotherapy in elderly breast cancer patients - a pooled analysis of individual patient data from 8 prospectively randomized controlled trials. Oncotarget 2018; 9: 15168-15179.
OpenUrl CrossRef PubMed
23.↵
1. Omair A,
2. Alkushi A,
3. Alamri G,
4. Almojel T,
5. Alsadun S,
6. Masuadi E, et al.
Assessing the correlation of rate of pathological complete response and outcome in post neoadjuvant chemotherapy setting and molecular subtypes of breast cancer. Cureus 2023; 15: e37449.
OpenUrl PubMed
24.↵
1. Guan D,
2. Jie Q,
3. Wu Y,
4. Xu Y,
5. Hong W,
6. Meng X
. Real-world data on breast pathologic complete response and disease-free survival after neoadjuvant chemotherapy for hormone receptor-positive, human epidermal growth factor receptor-2-negative breast cancer: a multicenter, retrospective study in China. World J Surg Oncol 2022; 20: 326.
OpenUrl PubMed
25.↵
1. LeVasseur N,
2. Sun J,
3. Gondara L,
4. Diocee R,
5. Speers C,
6. Lohrisch C, et al.
Impact of pathologic complete response on survival after neoadjuvant chemotherapy in early-stage breast cancer: a population-based analysis. J Cancer Res Clin Oncol 2020; 146: 529-536.
OpenUrl PubMed
26.↵
1. Huang M,
2. O’Shaughnessy J,
3. Zhao J,
4. Haiderali A,
5. Cortés J,
6. Ramsey SD, et al.
Association of pathologic complete response with long-term survival outcomes in triple-negative breast cancer: a meta-analysis. Cancer Res 2020; 80: 5427-5434.
OpenUrl Abstract/FREE Full Text
27.↵
1. Choi JY,
2. Woen D,
3. Jang SY,
4. Lee H,
5. Shin DS,
6. Kwak Y, et al.
Risk factors of breast cancer recurrence in pathologic complete response achieved by patients following neoadjuvant chemotherapy: a single-center retrospective study. Front Oncol 2023; 13: 1230310.
OpenUrl PubMed
28.↵
1. Aldrich J,
2. Canning M,
3. Bhave M
. Monitoring of triple negative breast cancer after neoadjuvant chemotherapy. Clin Breast Cancer 2023; 23: 832-834.
OpenUrl PubMed
29.↵
1. Pan H,
2. Wang H,
3. Qian M,
4. Mao X,
5. Shi G,
6. Ma G, et al.
Comparison of survival outcomes among patients with breast cancer with distant vs ipsilateral supraclavicular lymph node metastases. JAMA Netw Open 2021; 4: e211809.
OpenUrl
30.↵
1. Rosen RD,
2. Sapra A
. TNM classification. [Updated 2023; accessed 2024 February 13.]. Available from: https://www.ncbi.nlm.nih.gov/sites/books/NBK553187/
31.↵
1. Prakash O,
2. Hossain F,
3. Danos D,
4. Lassak A,
5. Scribner R,
6. Miele L
. Racial disparities in triple negative breast cancer: a review of the role of biologic and non-biologic factors. Front Public Health 2020; 8: 576964.
OpenUrl PubMed
32.↵
1. Siddharth S,
2. Sharma D
. Racial disparity and triple-negative breast cancer in African-American women: a multifaceted affair between obesity, biology, and socioeconomic determinants. Cancers (Basel) 2018; 10: 514.
OpenUrl PubMed
33.↵
1. Jiao D,
2. Ma Y,
3. Zhu J,
4. Dai H,
5. Yang Y,
6. Zhao Y, et al.
Impact of marital status on prognosis of patients with invasive breast cancer: a population-based study using SEER database. Front Oncol 2022; 12: 913929.
OpenUrl PubMed

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Keywords

[1] 1.↵
Arnold M,
Morgan E,
Rumgay H,
Mafra A,
Singh D,
Laversanne M, et al.
Current and future burden of breast cancer: global statistics for 2020 and 2040. Breast 2022; 66: 15-23.
OpenUrl CrossRef PubMed

[2] Arnold M,

[3] Morgan E,

[4] Rumgay H,

[5] Mafra A,

[6] Singh D,

[7] Laversanne M, et al.

[8] 2.↵
Alkabban FM,
Ferguson T
. Breast cancer. [Updated 2024; accessed 2024 February 25]. Available from: https://pubmed.ncbi.nlm.nih.gov/29493913/

[9] Alkabban FM,

[10] Ferguson T

[11] 3.↵
Giaquinto AN,
Sung H,
Miller KD,
Kramer JL,
Newman LA,
Minihan A, et al.
Breast cancer statistics, 2022. CA Cancer J Clin 2022; 72: 524-541.
OpenUrl CrossRef PubMed

[12] Giaquinto AN,

[13] Sung H,

[14] Miller KD,

[15] Kramer JL,

[16] Newman LA,

[17] Minihan A, et al.

[18] 4.↵
Yoon J,
Knapp G,
Quan ML,
Bouchard-Fortier A
. Cancer-specific outcomes in the elderly with triple-negative breast cancer: a systematic review. Curr Oncol 2021; 28: 2337-2345.
OpenUrl PubMed

[19] Yoon J,

[20] Knapp G,

[21] Quan ML,

[22] Bouchard-Fortier A

[23] 5.↵
Baranova A,
Krasnoselskyi M,
Starikov V,
Kartashov S,
Zhulkevych I,
Vlasenko V, et al.
Triple-negative breast cancer: current treatment strategies and factors of negative prognosis. J Med Life 2022; 15: 153-161.
OpenUrl PubMed

[24] Baranova A,

[25] Krasnoselskyi M,

[26] Starikov V,

[27] Kartashov S,

[28] Zhulkevych I,

[29] Vlasenko V, et al.

[30] 6.↵
Chen Y,
Qi Y,
Wang K
. Neoadjuvant chemotherapy for breast cancer: an evaluation of its efficacy and research progress. Front Oncol 2023; 13: 1169010.
OpenUrl PubMed

[31] Chen Y,

[32] Qi Y,

[33] Wang K

[34] 7.↵
Biganzoli L,
Battisti NML,
Wildiers H,
McCartney A,
Colloca G,
Kunkler IH, et al.
Updated recommendations regarding the management of older patients with breast cancer: a joint paper from the European Society of Breast Cancer Specialists (EUSOMA) and the International Society of Geriatric Oncology (SIOG). Lancet Oncol 2021; 22: e327-e340.
OpenUrl CrossRef PubMed

[35] Biganzoli L,

[36] Battisti NML,

[37] Wildiers H,

[38] McCartney A,

[39] Colloca G,

[40] Kunkler IH, et al.

[41] 8.↵
Zhao J,
Yang Y,
Pang D,
Yu Y,
Lin X,
Chen K, et al.
Development and validation of a nomogram in survival prediction among advanced breast cancer patients. Ann Transl Med 2020; 8: 1446.
OpenUrl PubMed

[42] Zhao J,

[43] Yang Y,

[44] Pang D,

[45] Yu Y,

[46] Lin X,

[47] Chen K, et al.

[48] 9.
Lin S,
Mo H,
Li Y,
Guan X,
Chen Y,
Wang Z, et al.
Development and validation of a nomogram for predicting survival of advanced breast cancer patients in China. Breast 2020; 53: 172-180.
OpenUrl PubMed

[49] Lin S,

[50] Mo H,

[51] Li Y,

[52] Guan X,

[53] Chen Y,

[54] Wang Z, et al.

[55] 10.↵
Zhu Y,
Wang J,
Xu B
. A novel prognostic nomogram for predicting survival of hormone receptor-positive and HER2 negative advanced breast cancer among the Han-population. Front Oncol 2022; 12: 918759.
OpenUrl PubMed

[56] Zhu Y,

[57] Wang J,

[58] Xu B

[59] 11.↵
Yin F,
Wang S,
Hou C,
Zhang Y,
Yang Z,
Wang X
. Development and validation of nomograms for predicting overall survival and cancer specific survival in locally advanced breast cancer patients: a SEER population-based study. Front Public Health 2022; 10: 969030.
OpenUrl PubMed

[60] Yin F,

[61] Wang S,

[62] Hou C,

[63] Zhang Y,

[64] Yang Z,

[65] Wang X

[66] 12.↵
Wang Z,
Xing L,
Luo X,
Ren G
. A nomogram for survival prediction in 275,812 U.S. patients with breast cancer: a population-based cohort study based on the SEER database. Gland Surg 2022; 11: 1166-1179.
OpenUrl PubMed

[67] Wang Z,

[68] Xing L,

[69] Luo X,

[70] Ren G

[71] 13.↵
Obidiro O,
Battogtokh G,
Akala EO
. Triple negative breast cancer treatment options and limitations: future outlook. Pharmaceutics 2023; 15: 1796.
OpenUrl PubMed

[72] Obidiro O,

[73] Battogtokh G,

[74] Akala EO

[75] 14.↵
Yang R,
Wu Y,
Qi Y,
Liu W,
Huang Y,
Zhao X, et al.
A nomogram for predicting breast cancer specific survival in elderly patients with breast cancer: a SEER population-based analysis. BMC Geriatr 2023; 23: 594.
OpenUrl PubMed

[76] Yang R,

[77] Wu Y,

[78] Qi Y,

[79] Liu W,

[80] Huang Y,

[81] Zhao X, et al.

[82] 15.↵
Wang H,
Xia GF,
Zhang ZR,
Luo X,
Zhu JY,
Wang HK
. Development and validation of a prognostic nomogram for breast cancer patients who underwent chemoradiotherapy and surgery: a retrospective cohort study based on the SEER database and 2 Chinese cohorts. Am J Cancer Res 2023; 13: 5065-5081.
OpenUrl PubMed

[83] Wang H,

[84] Xia GF,

[85] Zhang ZR,

[86] Luo X,

[87] Zhu JY,

[88] Wang HK

[89] 16.↵
Extermann M,
Leeuwenburgh C,
Samiian L,
Sehovic M,
Xu J,
Cubitt C, et al.
Impact of chemotherapy on medium-term physical function and activity of older breast cancer survivors, and associated biomarkers. J Geriatr Oncol 2017; 8: 69-75.
OpenUrl PubMed

[90] Extermann M,

[91] Leeuwenburgh C,

[92] Samiian L,

[93] Sehovic M,

[94] Xu J,

[95] Cubitt C, et al.

[96] 17.↵
Williams AD,
Dang CT,
Sevilimedu V,
Morrow M,
Barrio AV
. Neoadjuvant chemotherapy for breast cancer in the elderly: are we accomplishing our treatment goals? Ann Surg Oncol 2022; 29: 8002-8011.
OpenUrl PubMed

[97] Williams AD,

[98] Dang CT,

[99] Sevilimedu V,

[100] Morrow M,

[101] Barrio AV

[102] 18.↵
Assunção Ribeiro da Costa RE,
Rocha de Oliveira FT,
Nascimento Araújo AL,
Vieira SC
. Impact of pathologic complete response on the prognosis of triple-negative breast cancer patients: a cohort study. Cureus 2023; 15: e37396.
OpenUrl PubMed

[103] Assunção Ribeiro da Costa RE,

[104] Rocha de Oliveira FT,

[105] Nascimento Araújo AL,

[106] Vieira SC

[107] 19.
Huang M,
O’Shaughnessy J,
Zhao J,
Haiderali A,
Cortes J,
Ramsey S, et al.
Evaluation of pathologic complete response as a surrogate for long-term survival outcomes in triple-negative breast cancer. J Natl Compr Canc Netw 2020; 18: 1096-1104.
OpenUrl PubMed

[108] Huang M,

[109] O’Shaughnessy J,

[110] Zhao J,

[111] Haiderali A,

[112] Cortes J,

[113] Ramsey S, et al.

[114] 20.↵
Houvenaeghel G,
de Nonneville A,
Cohen M,
Sabiani L,
Buttarelli M,
Charaffe E, et al.
Neoadjuvant chemotherapy for breast cancer: pathologic response rates but not tumor size, has an independent prognostic impact on survival. Cancer Med 2024; 13: e6930.
OpenUrl

[115] Houvenaeghel G,

[116] de Nonneville A,

[117] Cohen M,

[118] Sabiani L,

[119] Buttarelli M,

[120] Charaffe E, et al.

[121] 21.↵
Van den Ende NS,
Nguyen AH,
Jager A,
Kok M,
Debets R,
van Deurzen CHM
. Triple-negative breast cancer and predictive markers of response to neoadjuvant chemotherapy: a systematic review. Int J Mol Sci 2023; 24: 2969.
OpenUrl CrossRef PubMed

[122] Van den Ende NS,

[123] Nguyen AH,

[124] Jager A,

[125] Kok M,

[126] Debets R,

[127] van Deurzen CHM

[128] 22.↵
Von Waldenfels G,
Loibl S,
Furlanetto J,
Machleidt A,
Lederer B,
Denkert C, et al.
Outcome after neoadjuvant chemotherapy in elderly breast cancer patients - a pooled analysis of individual patient data from 8 prospectively randomized controlled trials. Oncotarget 2018; 9: 15168-15179.
OpenUrl CrossRef PubMed

[129] Von Waldenfels G,

[130] Loibl S,

[131] Furlanetto J,

[132] Machleidt A,

[133] Lederer B,

[134] Denkert C, et al.

[135] 23.↵
Omair A,
Alkushi A,
Alamri G,
Almojel T,
Alsadun S,
Masuadi E, et al.
Assessing the correlation of rate of pathological complete response and outcome in post neoadjuvant chemotherapy setting and molecular subtypes of breast cancer. Cureus 2023; 15: e37449.
OpenUrl PubMed

[136] Omair A,

[137] Alkushi A,

[138] Alamri G,

[139] Almojel T,

[140] Alsadun S,

[141] Masuadi E, et al.

[142] 24.↵
Guan D,
Jie Q,
Wu Y,
Xu Y,
Hong W,
Meng X
. Real-world data on breast pathologic complete response and disease-free survival after neoadjuvant chemotherapy for hormone receptor-positive, human epidermal growth factor receptor-2-negative breast cancer: a multicenter, retrospective study in China. World J Surg Oncol 2022; 20: 326.
OpenUrl PubMed

[143] Guan D,

[144] Jie Q,

[145] Wu Y,

[146] Xu Y,

[147] Hong W,

[148] Meng X

[149] 25.↵
LeVasseur N,
Sun J,
Gondara L,
Diocee R,
Speers C,
Lohrisch C, et al.
Impact of pathologic complete response on survival after neoadjuvant chemotherapy in early-stage breast cancer: a population-based analysis. J Cancer Res Clin Oncol 2020; 146: 529-536.
OpenUrl PubMed

[150] LeVasseur N,

[151] Sun J,

[152] Gondara L,

[153] Diocee R,

[154] Speers C,

[155] Lohrisch C, et al.

[156] 26.↵
Huang M,
O’Shaughnessy J,
Zhao J,
Haiderali A,
Cortés J,
Ramsey SD, et al.
Association of pathologic complete response with long-term survival outcomes in triple-negative breast cancer: a meta-analysis. Cancer Res 2020; 80: 5427-5434.
OpenUrl Abstract/FREE Full Text

[157] Huang M,

[158] O’Shaughnessy J,

[159] Zhao J,

[160] Haiderali A,

[161] Cortés J,

[162] Ramsey SD, et al.

[163] 27.↵
Choi JY,
Woen D,
Jang SY,
Lee H,
Shin DS,
Kwak Y, et al.
Risk factors of breast cancer recurrence in pathologic complete response achieved by patients following neoadjuvant chemotherapy: a single-center retrospective study. Front Oncol 2023; 13: 1230310.
OpenUrl PubMed

[164] Choi JY,

[165] Woen D,

[166] Jang SY,

[167] Lee H,

[168] Shin DS,

[169] Kwak Y, et al.

[170] 28.↵
Aldrich J,
Canning M,
Bhave M
. Monitoring of triple negative breast cancer after neoadjuvant chemotherapy. Clin Breast Cancer 2023; 23: 832-834.
OpenUrl PubMed

[171] Aldrich J,

[172] Canning M,

[173] Bhave M

[174] 29.↵
Pan H,
Wang H,
Qian M,
Mao X,
Shi G,
Ma G, et al.
Comparison of survival outcomes among patients with breast cancer with distant vs ipsilateral supraclavicular lymph node metastases. JAMA Netw Open 2021; 4: e211809.
OpenUrl

[175] Pan H,

[176] Wang H,

[177] Qian M,

[178] Mao X,

[179] Shi G,

[180] Ma G, et al.

[181] 30.↵
Rosen RD,
Sapra A
. TNM classification. [Updated 2023; accessed 2024 February 13.]. Available from: https://www.ncbi.nlm.nih.gov/sites/books/NBK553187/

[182] Rosen RD,

[183] Sapra A

[184] 31.↵
Prakash O,
Hossain F,
Danos D,
Lassak A,
Scribner R,
Miele L
. Racial disparities in triple negative breast cancer: a review of the role of biologic and non-biologic factors. Front Public Health 2020; 8: 576964.
OpenUrl PubMed

[185] Prakash O,

[186] Hossain F,

[187] Danos D,

[188] Lassak A,

[189] Scribner R,

[190] Miele L

[191] 32.↵
Siddharth S,
Sharma D
. Racial disparity and triple-negative breast cancer in African-American women: a multifaceted affair between obesity, biology, and socioeconomic determinants. Cancers (Basel) 2018; 10: 514.
OpenUrl PubMed

[192] Siddharth S,

[193] Sharma D

[194] 33.↵
Jiao D,
Ma Y,
Zhu J,
Dai H,
Yang Y,
Zhao Y, et al.
Impact of marital status on prognosis of patients with invasive breast cancer: a population-based study using SEER database. Front Oncol 2022; 12: 913929.
OpenUrl PubMed

[195] Jiao D,

[196] Ma Y,

[197] Zhu J,

[198] Dai H,

[199] Yang Y,

[200] Zhao Y, et al.

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Development and validation of a nomogram to predict survival after neoadjuvant chemotherapy in elderly women with triple-negative invasive ductal breast cancer

A SEER population-based study

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Development and validation of a nomogram to predict survival after neoadjuvant chemotherapy in elderly women with triple-negative invasive ductal breast cancer

A SEER population-based study

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