Use of lipid parameters in the diagnosis of prognosis in patients with locally advanced breast cancer during neoadjuvant chemotherapy

Abstract

The present application provides the use of low density lipoprotein, total cholesterol and non-high density lipoprotein as a combined diagnostic marker in the preparation of a diagnostic composition for predicting the prognosis of a locally advanced breast cancer patient receiving neoadjuvant chemotherapy, if: the low density lipoprotein level after neoadjuvant chemotherapy - the low density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L; the total cholesterol level after neoadjuvant chemotherapy - the total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L; the non-high density lipoprotein level after neoadjuvant chemotherapy - the non-high density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L; if one or more of the above three detected levels are met, it indicates that the patient has a poor prognosis. The present application also provides a system for diagnosing the prognosis of a locally advanced breast cancer patient receiving neoadjuvant chemotherapy. The present application finds that the changes in the levels of low density lipoprotein, total cholesterol and non-high density lipoprotein during neoadjuvant chemotherapy can be used as potential prognostic biomarkers in clinical applications.

Description

Technical fields:

[0001] This invention belongs to the field of biomedical detection and relates to diagnostic markers, specifically the use of blood lipid indicators in diagnosing the prognosis of patients with locally advanced breast cancer who have received neoadjuvant chemotherapy. Background technology:

[0002] Breast cancer is the leading cause of cancer death and morbidity among women (1). For patients with locally advanced breast cancer, neoadjuvant chemotherapy plays an increasingly important role in the overall treatment management process. Its main advantages are that it can reduce tumor size, lower tumor stage, and eliminate micrometastases before surgery. Neoadjuvant chemotherapy can enable patients who are not candidates for surgery to undergo radical surgery, while increasing the possibility of breast-conserving surgery and even improving patient survival outcomes (2,3). For patients with locally advanced breast cancer who receive neoadjuvant chemotherapy, accurate prediction of their prognosis is crucial for subsequent clinical treatment decisions. Currently, the main basis for predicting prognosis is the essential characteristics of the tumor (clinical stage, pathological stage, other tumor biomarkers, etc.), without considering the patient's own metabolic factors.

[0003] Previous studies have shown that high-fat diets, obesity, and hyperlipidemia are not only closely related to the occurrence and development of various tumors (4-6), but also closely related to increased tumor metastasis (7-9). Lipids are one of the main energy sources for tumor cells, an indispensable component of biological membranes, a molecule required for intracellular and extracellular signal transduction, and a key component of metabolic reprogramming (10-13). Studies have shown that lipid metabolism reprogramming is related to tumor proliferation, invasion, energy production, plasma membrane remodeling, oncogenic signal propagation, and chemotherapy resistance (14). To meet the demand for excess lipids, tumor cells promote endogenous lipid synthesis by regulating specific enzymes, and take up exogenous lipids from the tumor microenvironment and peripheral blood circulation (15). These results indicate that lipid metabolism plays an important role in the occurrence and development of various cancers. Previous studies have included lipidomics in predicting the efficacy and prognosis of breast cancer patients (16), but lipidomics testing is time-consuming, labor-intensive, and expensive, making it difficult to conduct on a large scale in clinical practice. Therefore, selecting circulating lipid metabolism biomarkers that have prognostic value, are easy to measure, and are clinically accessible is of great clinical significance and research value.

[0004] References:

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[0006] 2.Heil J,Kuerer HM,Pfob A,Rauch G,Sinn HP,Golatta M,Liefers GJ,Vrancken Peeters MJ.Eliminating the breast cancer surgery paradigm afterneoadjuvant systemic therapy:current evidence and future challenges.Annals ofOncology:Official Journal of the European Society For Medical Oncology,2020,31(1):61-71.

[0007] 3.King TA,Morrow M.Surgical issues in patients with breast cancerreceiving neoadjuvant chemotherapy.Nature reviews Clinical oncology,2015,12(6):335-43.

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[0011] 7.Martin-Perez M,Urdiroz-Urricelqui U,Bigas C,Benitah SA.The role oflipids in cancer progression and metastasis.Cell metabolism,2022,34(11):1675-99.

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[0015] 11.Snaebjornsson MT,Janaki-Raman S,Schulze A.Greasing the Wheels ofthe Cancer Machine:The Role of Lipid Metabolismin Cancer.Cell metabolism,2020,31(1):62-76.

[0016] 12.Cheng C,Geng F,Cheng X,Guo D.Lipid metabolism reprogramming andits potential targets in cancer.Cancer communications(London,England),2018,38(1):27.

[0017] 13.Bian X,Liu R,Meng Y,Xing D,Xu D,Lu Z.Lipid metabolism andcancer.The Journal of experimental medicine,2021,218(1).

[0018] 14. Vasseur S, Guillaumond F. Lipids in cancer: a global view of the contribution of lipid pathways to metastatic formation and treatmentresistance. Oncogenesis, 2022, 11(1):46.

[0019] 15. Butler LM, Perone Y, Dehairs J, Lupien LE, de Laat V, Talebi A, Loda M, Kinlaw WB, Swinnen JV. Lipids and cancer: Emerging roles in pathogenesis, diagnosis and therapeutic intervention. Adv Drug Deliv Rev, 2020, 159: 245-93.

[0020] 16. Hilvo M, Gade S, T,Nekljudova V, T, Sysi-Aho M, Untch M, Huober J, von Minckwitz G, Denkert C, et al. Monounsaturated fatty acids in serum triacylglycerols are associated with response to neoadjuvantchemotherapy in breast cancer patients. International journal of cancer, 2014, 134(7): 1725-33. Summary of the Invention:

[0021] To address the aforementioned technical problems in the prior art, this invention provides the use of blood lipid indicators in diagnosing the prognosis of locally advanced breast cancer patients receiving neoadjuvant chemotherapy. This use of blood lipid indicators in diagnosing the prognosis of locally advanced breast cancer patients receiving neoadjuvant chemotherapy aims to solve the technical problems of time-consuming, labor-intensive, and unavailable large-scale application of lipidomics testing in the prognosis of locally advanced breast cancer patients receiving neoadjuvant chemotherapy in the prior art.

[0022] This invention provides the use of low-density lipoprotein, total cholesterol, and non-high-density lipoprotein as combined diagnostic markers in the preparation of diagnostic compositions for predicting the prognosis of patients with locally advanced breast cancer receiving neoadjuvant chemotherapy, if:

[0023] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0024] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy >

[0025] -0.01mmol / L;

[0026] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0027] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

[0028] This invention also provides a kit for diagnosing the prognosis of patients with locally advanced breast cancer receiving neoadjuvant chemotherapy. The kit contains reagents for detecting low-density lipoprotein, total cholesterol, and non-high-density lipoprotein. If:

[0029] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0030] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy >

[0031] -0.01mmol / L;

[0032] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0033] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

[0034] This invention, through a retrospective analysis of locally advanced breast cancer patients who received neoadjuvant chemotherapy in a prospective database, discovered that changes in the levels of three peripheral blood lipids—low-density lipoprotein (LDL), total cholesterol (TC), and non-high-density lipoprotein (NHDL)—can serve as potential prognostic biomarkers for clinical application.

[0035] This invention also provides the use of low-density lipoprotein, total cholesterol, and non-high-density lipoprotein as combined diagnostic markers in the preparation of a prognostic diagnostic system for patients with locally advanced breast cancer receiving neoadjuvant chemotherapy, if:

[0036] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0037] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L;

[0038] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0039] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

[0040] The present invention also provides a system for prognostic diagnosis of locally advanced breast cancer patients receiving neoadjuvant chemotherapy, the system comprising:

[0041] (1) Data input module: The low-density lipoprotein (LDL) level after neoadjuvant chemotherapy, the LDL level before neoadjuvant chemotherapy, the total cholesterol level after neoadjuvant chemotherapy, the total cholesterol level before neoadjuvant chemotherapy, the non-high-density lipoprotein (NDL) level after neoadjuvant chemotherapy, and the non-high-density lipoprotein (NDL) level before neoadjuvant chemotherapy are detected using a biochemical analyzer. The LDL level after neoadjuvant chemotherapy and the LDL level before neoadjuvant chemotherapy are input; the total cholesterol level after neoadjuvant chemotherapy and the total cholesterol level before neoadjuvant chemotherapy are input; the NDL level after neoadjuvant chemotherapy and the NDL level before neoadjuvant chemotherapy are input.

[0042] (2) Data calculation module: Calculate the data obtained in step (1): Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy; Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy; Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy.

[0043] (3) Data prediction module: Input the data obtained from the data calculation module. If:

[0044] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0045] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy >

[0046] -0.01mmol / L;

[0047] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0048] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

[0049] This invention aims to discover metabolic biomarkers with prognostic value, and for the first time elucidates the impact of changes in blood lipid levels during neoadjuvant chemotherapy on the prognosis of patients with locally advanced breast cancer. This invention overcomes the shortcomings of existing technologies by identifying reliable and convenient circulating lipid metabolism biomarkers for predicting the prognosis of patients with locally advanced breast cancer receiving neoadjuvant chemotherapy. This invention provides an economical and time-saving method for predicting the prognosis of patients with locally advanced breast cancer receiving neoadjuvant chemotherapy.

[0050] Compared with existing technologies, the technical effects of this invention are positive and significant. The peripheral blood lipid levels that this invention requires to detect are more accessible and clinically widespread than lipidomics. The detection is convenient, economical, time-saving, and labor-saving, and easily understood and applied by clinical medical workers at all levels of hospitals. Timely adjustment of abnormal blood lipid status during neoadjuvant chemotherapy may benefit the survival outcomes of patients with locally advanced breast cancer. Attached image description:

[0051] Figure 1 The Kaplan-Meier curves show how changes in blood lipids during neoadjuvant chemotherapy predict different survival outcomes.

[0052] Figure 2 This study presents a multivariate Cox proportional hazards regression model showing the prediction of disease-free survival (DFS) and relapse-free survival (RFS) based on changes in blood lipids during neoadjuvant chemotherapy. Note: Disease-free survival (DFS) is defined as the time from surgery to the first occurrence of local recurrence, regional recurrence, distant metastasis, second primary cancer, or all-cause death. Relapse-free survival (RFS) is defined as the time from surgery to the first occurrence of local recurrence, regional recurrence, distant recurrence, or all-cause death. * P<0.05, ** P<0.01. Detailed implementation method:

[0053] Example 1

[0054] This study included 120 women aged ≥18 years with histologically confirmed invasive breast cancer (T1N1-3, T2-4 N0-3, M0), who had undergone neoadjuvant chemotherapy and successfully underwent radical surgery at the applicant's breast surgery department. Clinical and pathological data (including age, height, weight, menstrual status, clinical stage, and pathological stage) were prospectively collected. Blood lipid levels, including triglycerides (TG), total cholesterol (TC), high-density lipoprotein (HDL), low-density lipoprotein (LDL), and non-high-density lipoprotein (NHDL), were retrospectively collected before and after neoadjuvant chemotherapy using electronic medical records. Blood lipid levels were measured using a Hitachi fully automated biochemical analyzer.

[0055] The change in blood lipid levels (mmol / L) was obtained by subtracting the pre-neoadjuvant chemotherapy blood lipid levels (mmol / L) from the post-neoadjuvant chemotherapy blood lipid levels (mmol / L). Data from enrolled patients (including basic patient information, clinicopathological information, pre-neoadjuvant chemotherapy and post-neoadjuvant chemotherapy blood lipid levels, survival endpoints and their corresponding survival endpoint times) were imported into R language, and the change in blood lipid levels could be calculated using the `surv_cutpoint` function in the `survminer` package.

[0056] The study endpoints included disease-free survival (DFS), relapse-free survival (RFS), distance-recurrence-free survival (DRFS), and locoregional-recurrence-free survival (LRFS). DFS was defined as the time from surgery to the first occurrence of local recurrence, regional recurrence, distant metastasis, second primary cancer, or all-cause death. RFS was defined as the time from surgery to the first occurrence of local recurrence, regional recurrence, distant recurrence, or all-cause death. DRFS was defined as the time from surgery to the first occurrence of distant metastasis or all-cause death. LRFS was defined as the time from surgery to the first occurrence of local recurrence, regional recurrence, or all-cause death.

[0057] Kaplan-Meier analysis was used to assess survival outcomes, and log-rank tests were used to evaluate survival differences between groups. Furthermore, multivariate Cox proportional hazards regression models were used to estimate hazard ratios (HRs) and 95% confidence intervals (CIs). Adjusted factors included hormone receptor status (positive vs. negative), HER2 status (positive vs. negative), Ki67 level (>30% vs. ≤30%), and clinical stage (stage I-II vs. stage III). Statistical analysis was performed using R (version 4.2.2). All statistical tests were two-tailed, and p < 0.05 was considered statistically significant.

[0058] result:

[0059] Using the `surv_cutpoint` function of the `survminer` utility in R, the optimal cutoff values ​​for TG (1.51 mmol / L), TC (-0.01 mmol / L), HDL (-0.51 mmol / L), LDL (0.54 mmol / L), and NHDL (0.85 mmol / L) are calculated as follows: For predicting DFS (Distressed Freezing Disease), the optimal cutoff values ​​are: TG (-0.1 mmol / L), TC (0.14 mmol / L), HDL (-0.13 mmol / L), LDL (0.54 mmol / L), and NHDL (0.85 mmol / L).

[0060] Kaplan-Meier analysis showed that a relative increase in LDL during neoadjuvant chemotherapy (LDL change > 0.54 mmol / L) was associated with shorter disease-free survival (DFS, P = 0.003), relapse-free survival (RFS, P = 0.01), distant metastasis-free survival (DRFS, P = 0.01), and local recurrence-free survival (LRFS, P = 0.0039). (See Appendix) Figure 1 A through D, while changes in TG and HDL were not significantly correlated with patient prognosis.

[0061] Furthermore, relative increases in TC (TC change > -0.01 mmol / L) and NHDL (NHDL change > 0.85 mmol / L) were also associated with worse DFS, see Appendix. Figure 1 E and appendix Figure 1 F.

[0062] Further multivariate Cox proportional hazards regression model was constructed. The results showed that after multivariate adjustment, the relative increases in LDL, TC, and NHDL were still associated with worse DFS and RFS, while changes in TG and HDL were not significantly associated with patient prognosis (see Appendix). Figure 2 ).

[0063] Conclusion: The relative increase of LDL, TC and NHDL during neoadjuvant chemotherapy is an independent risk factor for prognosis in patients with locally advanced breast cancer.

[0064] if:

[0065] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0066] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy >

[0067] -0.01mmol / L;

[0068] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0069] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

[0070] Example 2

[0071] This invention also provides the use of low-density lipoprotein, total cholesterol, and non-high-density lipoprotein as combined diagnostic markers in the preparation of a prognostic diagnostic system for patients with locally advanced breast cancer receiving neoadjuvant chemotherapy, if:

[0072] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0073] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L;

[0074] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0075] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

[0076] The present invention also provides a system for prognostic diagnosis of locally advanced breast cancer patients receiving neoadjuvant chemotherapy, the system comprising:

[0077] (1) Data input module: The low-density lipoprotein (LDL) level after neoadjuvant chemotherapy, the LDL level before neoadjuvant chemotherapy, the total cholesterol level after neoadjuvant chemotherapy, the total cholesterol level before neoadjuvant chemotherapy, the non-high-density lipoprotein (NDL) level after neoadjuvant chemotherapy, and the non-high-density lipoprotein (NDL) level before neoadjuvant chemotherapy are detected using a biochemical analyzer. The LDL level after neoadjuvant chemotherapy and the LDL level before neoadjuvant chemotherapy are input; the total cholesterol level after neoadjuvant chemotherapy and the total cholesterol level before neoadjuvant chemotherapy are input; the NDL level after neoadjuvant chemotherapy and the NDL level before neoadjuvant chemotherapy are input.

[0078] (2) Data calculation module: Calculate the data obtained in step (1): Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy; Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy; Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy.

[0079] (3) Data prediction module: Input the data obtained from the data calculation module. If:

[0080] (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L;

[0081] (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy >

[0082] -0.01mmol / L;

[0083] (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L;

[0084] If one or more of the above three tests meet the criteria, it indicates a poor prognosis for the patient.

Claims

1. The use of low-density lipoprotein, total cholesterol, and non-high-density lipoprotein as combined diagnostic markers in the preparation of a diagnostic composition for predicting the prognosis of patients with locally advanced breast cancer receiving neoadjuvant chemotherapy, if: (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L; (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L; (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L; If all three tests above are satisfactory, it indicates a poor prognosis for the patient.

2. Use of reagents for detecting low-density lipoprotein, total cholesterol, and non-high-density lipoprotein in the preparation of a diagnostic kit for predicting the prognosis of patients with locally advanced breast cancer receiving neoadjuvant chemotherapy; if: (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L; (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L; (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L; If all three tests above are satisfactory, it indicates a poor prognosis for the patient.

3. The use of low-density lipoprotein, total cholesterol, and non-high-density lipoprotein as combined diagnostic markers in the development of a prognostic diagnostic system for patients with locally advanced breast cancer receiving neoadjuvant chemotherapy, if: (1) Low-density lipoprotein level after neoadjuvant chemotherapy – Low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L; (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L; (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L; If all three tests above are satisfactory, it indicates a poor prognosis for the patient.

4. A system for prognostic diagnosis of locally advanced breast cancer patients receiving neoadjuvant chemotherapy, characterized in that, The system includes: (1) Data input module: The low-density lipoprotein (LDL) level after neoadjuvant chemotherapy, the LDL level before neoadjuvant chemotherapy, the total cholesterol level after neoadjuvant chemotherapy, the total cholesterol level before neoadjuvant chemotherapy, the non-high-density lipoprotein (NDL) level after neoadjuvant chemotherapy, and the non-high-density lipoprotein (NDL) level before neoadjuvant chemotherapy are detected using a biochemical analyzer. The LDL level after neoadjuvant chemotherapy and the LDL level before neoadjuvant chemotherapy are input; the total cholesterol level after neoadjuvant chemotherapy and the total cholesterol level before neoadjuvant chemotherapy are input; the NDL level after neoadjuvant chemotherapy and the NDL level before neoadjuvant chemotherapy are input. (2) Data calculation module: Calculates the data obtained by the data input module: Low-density lipoprotein level after neoadjuvant chemotherapy - Low-density lipoprotein level before neoadjuvant chemotherapy; Total cholesterol level after neoadjuvant chemotherapy - Total cholesterol level before neoadjuvant chemotherapy; Non-high-density lipoprotein level after neoadjuvant chemotherapy - Non-high-density lipoprotein level before neoadjuvant chemotherapy. (3) Data prediction module: Input the data obtained from the data calculation module. If: (1) The patient’s low-density lipoprotein level after neoadjuvant chemotherapy – the patient’s low-density lipoprotein level before neoadjuvant chemotherapy > 0.54 mmol / L; (2) Total cholesterol level after neoadjuvant chemotherapy – Total cholesterol level before neoadjuvant chemotherapy > -0.01 mmol / L; (3) Non-high-density lipoprotein level after neoadjuvant chemotherapy – Non-high-density lipoprotein level before neoadjuvant chemotherapy > 0.85 mmol / L; If all three tests above are satisfactory, it indicates a poor prognosis for the patient.

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