Hospital Outcomes of Male Breast Cancer in the United States

ABSTRACT

Objectives: Hospital utilization and costs of female breast cancer have been well documented. However, evidence focusing on male breast cancer is scarce, despite the different clinical characteristics between female and male breast cancer. We aim to estimate hospital length of stay (LOS) and costs associated with male breast cancer in the United States.

Study Design: Retrospective observational study.

Methods: We analyzed the 2012-2016 Health Care Utilization Project National Inpatient Sample of 416 hospitalization events of male patients with breast cancer. Patients who had breast cancer diagnoses were selected based on the primary International Classification of Disease, Ninth Revision or Tenth Revision, Clinical Modification codes. A negative binomial regression and a generalized linear model with a gamma distribution and log-link function were conducted to estimate the LOS and hospital costs after controlling for sociodemographics, clinical characteristics (eg, metastatic status, Elixhauser Comorbidity Index [ECI] score), and hospital characteristics.

Results: On average, male patients with breast cancer stayed for 2.42 days and expensed $9059 per hospital visit. Patients with metastatic status had longer LOS (5.39 vs 3.24 days; P = .005) and higher hospital costs ($11,185 vs $8547; P = .03) than those without. Patients with an ECI score of 3 or more showed longer LOS (4.05 vs 2.68 days; P = .003) and higher hospital costs ($10,043 vs $7022; P < .001) than those with an ECI score of 0.

Conclusions: LOS and hospital costs for male patients with breast cancer were associated with metastatic status and comorbidities. This information can be used to assess the health care resources needed to treat male breast cancer.

Am J Manag Care. 2021;26(6):e181-e187. https://doi.org/10.37765/ajmc.2021.88666

Takeaway Points

• It is well known that there is a substantial economic burden of managed care for the female population with breast cancer in the United States. However, information on health care utilization and costs for male patients with breast cancer is sparse despite the epidemiological differences between male and female breast cancer.
• We found that male patients with breast cancer experienced an estimated hospital stay duration of 2.4 days and costs of $9059 per hospitalization in the United States. Metastatic status and comorbidities were the major predictors of a longer stay and higher costs.
• Our findings will be helpful for the allocation of health care resources for men with breast cancer.

Breast cancer is frequently diagnosed and clinically impacts the mortality of women in the United States.¹ In 2019, 268,600 women were estimated to be diagnosed with breast cancer, and 41,760 women were estimated to die due to breast cancer.² Breast cancer can also be diagnosed in men, as men have breast tissue in which breast cancer can develop.³ Approximately 2670 men were estimated to be diagnosed with breast cancer in 2019.² The prevalence of male breast cancer accounts for less than 1% among total cases of breast cancer⁴; however, the incidence of male breast cancer has steadily increased from 0.85 to 1.44 per 100,000 since 1975.⁵

Physicians treating male patients with breast cancer are advised to extrapolate from the results of clinical trials of female breast cancer or to follow the guidelines for female breast cancer.^6,7 This may be due to the relatively scarce clinical evidence of male breast cancer compared with female breast cancer, as only one-third of trials for patients with breast cancer have been open to male patients.⁸ However, patients with breast cancer show different clinical characteristics by gender. For example, male patients present at older ages and have a higher percentage of estrogen receptor (ER)–positive tumors compared with female patients, and the molecular subtypes and distinct immunophenotypic profiles differ between female and male patients with breast cancer.^9,10 Moreover, the risk of mortality is higher in male patients with breast cancer compared with female patients.^10,11 These differences necessitate research focusing on male breast cancer.

Female breast cancer imposes a substantial economic burden in the United States because of the medical costs and the high incidence rate.^1,12-14 A previous US study found that breast cancer treatment increased substantial health care costs in the managed care population. The study estimated the mean monthly total health care costs per patient with breast cancer at $4421, and hospitalizations mainly induced those costs with a mean expense of $1576.¹⁵ The health care costs for patients with breast cancer were higher than those for patients without cancer (mean monthly total health care costs, $3352; mean monthly hospital costs, $213). Another study reported that the highest portion of medical expenses in female breast cancer is used for hospitalization.¹⁶ Hospital costs for female breast cancer were estimated to be $4100 per day, the second highest cancer-related hospital expenditures in 2009.¹⁷ Breast cancer was one of the most common cancer hospitalizations among adult women in 2009.¹⁷

Although the economic burden due to hospitalization is well known in female breast cancer, no study about hospital utilization and costs in male breast cancer in the United States has been conducted. Estimating hospital utilization and costs is necessary to inform decision makers of the health care resources needed to prevent and treat male breast cancer. Therefore, we aimed to assess hospital utilization and costs associated with male breast cancer in the United States.

MATERIALS AND METHODS

Data Source

We used the hospital discharge data from the 2012-2016 Health Care Utilization Project National Inpatient Sample (HCUP-NIS), which is managed by the Agency for Healthcare Research and Quality (AHRQ). This database is based on information at the hospitalization event level. The HCUP-NIS contains information on hospital inpatient stays extracted from the billing data of hospitals to statewide data organizations across the United States.¹⁸ This database covers more than 97% of the US population based on a 20% stratified sample of discharges from US community hospitals except for rehabilitation and long-term acute care hospitals.

Study Sample

We identified a total of 416 hospital discharges of male patients with breast cancer for this study, with the discharges being those with the diagnosis code of breast cancer using the primary International Classification of Disease, Ninth Revision, Clinical Modification (ICD-9-CM) or Tenth Revision, Clinical Modification (ICD-10-CM) code. We defined patients between 2012 and the third quarter of the 2015 database as having code 175 (malignant neoplasm of male breast) using ICD-9-CM, and patients between the fourth quarter of 2015 and 2016 as having code C50 (malignant neoplasm of breast) using ICD-10-CM.¹⁹ We pooled the data from 2012 to 2016 to ensure a sufficient sample size for reliable estimates. We excluded hospitalization events of patients younger than 18 years at discharge.

Variables

The outcome variables were length of stay (LOS) and hospital costs. The LOS was measured as the number of days per hospitalization. The hospital costs were calculated by multiplying the total charge and cost to charge ratio per hospitalization event. The value of cost to charge ratio provided by the AHRQ was used in this calculation.²⁰ The costs for 2012 to 2015 were inflated to 2016 US$ using the index of personal consumption expenditures for medical care and hospitalization.^21,22

The clinical and hospital characteristics included surgical treatment (yes or no), metastatic status (yes or no), in-hospital mortality (yes or no), Elixhauser Comorbidity Index (ECI) score (0, 1, 2, or ≥ 3), timing of admission (weekday or weekend), hospital location and teaching status (rural, urban and nonteaching, or urban and teaching), hospital census region (Northeast, Midwest, South, or West), and hospital size (small, medium, or large). Other covariates were age (< 50, 50-64, 65-79, or ≥ 80 years), race/ethnicity (White, Black, Hispanic, or others), household income (lowest, second, third, and highest quartiles), and primary payer (government including Medicare/Medicaid, private insurance including health maintenance organization, and others including self-pay and charity).^19,23

The surgical treatment variable was based on the ICD-9/10-CM procedure coding system of breast conservation surgery and mastectomy surgery.^24,25 The ECI score was calculated taking into account the target population of patients with breast cancer.²⁶ The codes for defining surgical treatment and metastatic status are presented in the eAppendix Table (available at ajmc.com).²³

Statistical Analyses

We conducted simple descriptive analyses, such as calculating the mean for the continuous variables and percentages for the categorical variables. A negative binomial regression and a generalized linear model with a gamma distribution and log-link function were conducted to estimate LOS and hospital costs adjusted by factors of sociodemographic, clinical, and hospital characteristics. We then estimated the margins for LOS and hospital costs by each factor from the regression models. Margins were generated by the average marginal effects method. The analyses applied the sampling weights to account for the stratification of the national sample. The threshold for significance was 0.05 for all statistical analyses. All analyses were conducted using Stata version 16 for Windows (StataCorp LLC).

RESULTS

We identified 416 hospitalization events of male patients with breast cancer 18 years and older from the data during 2012 to 2016. The weighted observations were calculated as 416 using the 2012-2016 NIS database, which contains a 20% sample of discharges. The sociodemographic, clinical, and hospital characteristics for the study population are presented in Table 1 [part A and part B]. More than half of the patients were 65 years or older at the time of discharge (n = 238; 57.2%) and more than two-thirds were White (n = 303; 72.8%). Among the patients discharged, approximately 80% received surgeries such as breast conservation surgery or mastectomy (n = 335; 80.5%), and approximately 18% had metastatic status (n = 77; 18.5%). Patients stayed for a mean (standard error [SE]) of 2.42 (0.15) days while spending a mean (SE) of $9059 ($345) per hospitalization.

Table 2 [part A and part B] shows the negative binomial regression estimates on LOS for hospitalization events of male patients with breast cancer. Inpatient hospitalization with surgical treatment showed a significantly lower LOS (incidence rate ratio [IRR], 0.57; 95% CI, 0.41-0.79; P < .001) relative to that without surgical treatment. Those who received surgical treatment during hospitalization had significantly shorter stays (1.87 days) compared with those who did not (3.30 days). In-hospital mortality also significantly lowered the LOS (IRR, 0.61; 95% CI, 0.40-0.94; P = .025). Patients with metastatic status at the time of discharge stayed 1.67 times (95% CI, 1.17-2.37; P = .005) longer than patients without metastatic status. Patients with an ECI score of 3 or greater showed longer LOS (IRR, 1.51; 95% CI, 1.15-1.99; P = .003) than those with a score of 0. Otherwise, LOS was not influenced by age group, household income, primary payer, timing of admission, and hospital-related variables including hospital location, census region, and size of hospital.

Table 3 [part A and part B] presents the generalized linear model estimates on hospital costs among male patients with breast cancer. Looking at hospital costs, they were not influenced by surgical treatment (cost ratio, 0.99; 95% CI, 0.78-1.26; P = .954). Metastatic status was positively associated with higher hospital costs (cost ratio, 1.31; 95% CI, 1.03-1.67; P = .030) than nonmetastatic status ($11,185 vs $8547). The results showed that patients with an ECI score of 1 had 1.19 times higher (95% CI, 1.02-1.39; P = .025) hospital costs than patients who had a score of 0. The likelihood increased with higher ECI scores (score of 2: cost ratio, 1.20; 95% CI, 1.01-1.43; P = .039; score of ≥ 3: cost ratio, 1.43; 95% CI, 1.21-1.69; P < .001). Hospitalizations with in-hospital mortalities had lower hospital costs compared with hospitalizations without mortalities ($5846 vs $8678), but the difference in hospital costs by in-hospital mortality was not statistically significant (cost ratio, 0.67; 95% CI, 0.38-1.18; P = .168).

DISCUSSION

According to the PubMed library, 262,175 articles containing the key words “breast cancer” in the title or abstract have been published as of 2019. Of those articles, only 1406 contained the keywords “male breast cancer,” representing less than 1% among the articles about breast cancer. These search results show that most studies about breast cancer have focused on female breast cancer. Studies reporting the hospital utilization or discharge costs focusing on male breast cancer were absent. The lack of evidence on health care resource utilization of male breast cancer is even more apparent.

To our knowledge, this is the first study to estimate the LOS and costs of inpatient settings and also the first to explore the association between hospital utilization and costs with sociodemographic, clinical, and hospital-level characteristics among male patients with breast cancer using a nationwide database. We found that men with breast cancer stayed for a mean of 2.42 days and cost a mean of $9059 per hospitalization event in the United States. We found that LOS and hospital costs were associated with the metastatic status and the ECI score of patients. The mean LOS and hospital costs increased to 5.39 days and $11,185 for patients with metastatic status. Patients with an ECI score of 3 or more had a mean LOS of 4.05 days and $10,043 in mean hospital costs. Surgery and in-hospital mortality decreased LOS, but hospital costs did not significantly differ by those specific factors.

In male breast cancer treatment, the number of patients who used hormonal therapy steadily increased among ER-positive patients since 2004.²⁷ Additionally, the proportion of orders for Oncotype DX testing increased among male patients with lymph node–negative, ER-positive, and HER2-negative breast cancer. These changes in male breast cancer treatment may have influenced hospital-related outcomes (eg, in-hospital mortality, hospital costs, LOS). Unfortunately, no previous studies have focused on hospital-related outcomes in male breast cancer to compare with the results of this current study. Therefore, we compared the results on hospital-related outcomes for both male and female patients. Previous studies, including reports from HCUP, reported that patients with breast cancer, including both men and women, were hospitalized for approximately 2.5 days.^17,28-32 This value is similar to our current result of LOS (2.42 days). However, the results on hospital costs differed by the study setting. The current study estimated the mean hospital costs as $9059 in 2016. The HCUP report, which analyzed the hospital costs for patients with breast cancer overall, reported the costs as $10,300 in 2009.17 Considering inflation, the costs from the HCUP report can be adjusted to $11,523 in 2016 (Consumer Price Index in 2009, 214.537; 2016, 240.007).³³ Thus, the hospital costs of overall patients with breast cancer are higher than those of male-only patients with breast cancer. A previous study about health care costs suggested that women generally tend to use more health care resources and generate more costs than men.^34,35 However, it is hard to conclude from this previous study alone that this higher hospital cost of overall patients with breast cancer is associated with female patients with breast cancer. Therefore, we suggest further studies to compare the health care costs of patients with breast cancer by gender and to identify the influential factors that induce the differences in cost by gender.

In this research, we showed that the patients with higher ECI scores had a longer LOS and higher hospital costs compared with those with scores of 0. Our findings of the association between specific clinical characteristics (eg, metastatic status and comorbidity) and hospital outcomes (eg, LOS and hospital costs) also aligned with results of a previous study of female patients with breast cancer.³⁶ In this previous study, which included female patients with breast cancer who underwent surgery, results showed increasing LOS with increasing severity of comorbidities, which was measured by the Charlson Comorbidity Index. Moreover, this similar trend was identified in studies of other cancer types.^37,38 Results of those studies showed that LOS and hospital costs significantly increased according to a higher ECI score. Therefore, proactive efforts to reduce chronic conditions may also help to reduce LOS.

Limitations

Our results should be interpreted with caution due to some limitations. First, the HCUP-NIS is a database that provides US regional and national estimates of inpatient utilization, charges, access, quality, and outcomes. Thus, the HCUP-NIS lacks information on details such as the stage of cancer, which precludes an analysis of any advanced disease in association with hospital admissions. Another limitation is that the reason for admission was not considered, as this is difficult to define from the database. Previous studies have reported that the LOS of hospitalizations related to malignant pleural effusions and febrile neutropenia was 4.6 days and 5.74 days, respectively.^39,40 Hospitalization for febrile neutropenia resulted in mean costs of $37,087,³⁹ and hospitalization for mastectomy and immediate breast reconstruction resulted in median costs of $48,741 among patients with breast cancer.²⁹ Those results from previous studies are higher than the result of this current study (LOS, 2.42 days; hospital costs, $9059). As shown in the previous studies, the reason for hospitalization might be a helpful factor to determine hospital costs.

Additionally, we could not distinguish whether 2 hospitalizations for breast cancer meant hospitalizations for 2 different individuals or for the same person, as the database reports per inpatient event. In this study, we combined the patients who underwent each surgery into a single group due to the insufficient sample size in the breast conservation surgery group (n = 17; 4.1%). Generally, patients who undergo breast conservation surgery do not need an overnight stay, whereas those with a mastectomy stay in the hospital for 1 or 2 nights. Therefore, breast conservation surgery and mastectomy may influence LOS and hospital costs differently.⁴¹

CONCLUSIONS

This study suggests that LOS and hospital costs of male patients with breast cancer are associated with some clinical characteristics, such as surgery, metastatic status, comorbidities, and in-hospital mortality. This information can be used to assess the health care resources needed to prevent and treat breast cancer in male patients.

Author Affiliations: College of Pharmacy, The Catholic University of Korea (SKP), Bucheon, Korea; College of Nursing & Disability Aging and Technology Cluster (BPN), University of Central Florida, Orlando, FL; School of Pharmacy, Bouvé College of Health Sciences, Northeastern University (HKC), Boston, MA; Health Outcomes Division, College of Pharmacy, University of Texas at Austin (CP), Austin, TX.

Source of Funding: None.

Author Disclosures: The authors report no relationship or financial interest with any entity that would pose a conflict of interest with the subject matter of this article.

Authorship Information: Concept and design (CP); acquisition of data (SKP, CP); analysis and interpretation of data (SKP, BPN, CP); drafting of the manuscript (SKP, BPN, HKC); critical revision of the manuscript for important intellectual content (BPN, HKC, CP); statistical analysis (SKP); administrative, technical, or logistic support (HKC); and supervision (CP).

Address Correspondence to: Chanhyun Park, PhD, Health Outcomes Division, College of Pharmacy, University of Texas at Austin, 2409 University Ave, Stop A1930, Austin, TX 78712-1117. Email: chanhyun.park@utexas.edu.

REFERENCES

1. Cancer facts & figures 2019. American Cancer Society. 2019. Accessed December 12, 2019. https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/annual-cancer-facts-and-figures/2019/cancer-facts-and-figures-2019.pdf

2. Browse the SEER Cancer Statistics Review (CSR) 1975-2016: Table 1.1. National Cancer Institute. Accessed January 29, 2020. https://seer.cancer.gov/csr/1975_2016/browse_csr.php?sectionSEL=1&pageSEL=sect_01_table.01.html

3. What is breast cancer in men? American Cancer Society. Updated April 27, 2018. Accessed February 20, 2020. https://www.cancer.org/cancer/breast-cancer-in-men/about/what-is-breast-cancer-in-men.html

4. SEER Cancer Statistics Review (CSR) 1975-2015. National Cancer Institute. 2018. Accessed December 12, 2019. https://seer.cancer.gov/archive/csr/1975_2015/

5. Weiss JR, Moysich KB, Swede H. Epidemiology of male breast cancer. Cancer Epidemiol Biomarkers Prev.2005;14(1):20-26.

6. NCCN. Clinical Practice Guidelines in Oncology. Breast cancer, version 4.2021. Accessed April 30, 2020. https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1419

7. Hassett MJ, Somerfield MR, Baker ER, et al. Management of male breast cancer: ASCO guideline. J Clin Oncol. 2020;38(16):1849-1863. doi:10.1200/JCO.19.03120

8. Bogler O. Male breast cancer: opportunities for research and clinical trials. Breast Diseases. 2013;24(3):216-218. doi:10.1016/j.breastdis.2013.07.047

9. Anderson WF, Jatoi I, Tse J, Rosenberg PS. Male breast cancer: a population-based comparison with female breast cancer. J Clin Oncol.2010;28(2):232-239. doi:10.1200/JCO.2009.23.8162

10. Chen X, Liu X, Zhang L, Li S, Shi Y, Tong Z. Poorer survival of male breast cancer compared with female breast cancer patients may be due to biological differences. Jpn J Clin Oncol. 2013;43(10):954-963. doi:10.1093/jjco/hyt116

11. Wang F, Shu X, Meszoely I, et al. Overall mortality after diagnosis of breast cancer in men vs women. JAMA Oncol. 2019;5(11):1589-1596. doi:10.1001/jamaoncol.2019.2803

12. Mariotto AB, Yabroff KR, Shao Y, Feuer EJ, Brown ML. Projections of the cost of cancer care in the United States: 2010-2020. J Natl Cancer Inst.2011;103(2):117-128. doi:10.1093/jnci/djq495

13. Yabroff KR, Lund J, Kepka D, Mariotto A. Economic burden of cancer in the United States: estimates, projections, and future research. Cancer Epidemiol Biomarkers Prev. 2011;20(10):2006-2014. doi:10.1158/1055-9965.EPI-11-0650

14. Cancer stat facts: common cancer sites. National Cancer Institute. Accessed February 21, 2020. https://seer.cancer.gov/statfacts/html/common.html

15. Barron JJ, Quimbo R, Nikam PT, Amonkar MM. Assessing the economic burden of breast cancer in a US managed care population. Breast Cancer Res Treat. 2008;109(2):367-377. doi:10.1007/s10549-007-9650-4

16. Zheng Z, Yabroff KR, Guy GP Jr, et al. Annual medical expenditure and productivity loss among colorectal, female breast, and prostate cancer survivors in the United States. J Natl Cancer Inst. 2016;108(5):djv382. doi:10.1093/jnci/djv382

17. Cancer hospitalizations for adults. Agency for Healthcare Research and Quality statistical brief No. 125. February 2012. Accessed January 12, 2019. https://www.hcup-us.ahrq.gov/reports/statbriefs/sb125.jsp

18. Introduction to the HCUP National Inpatient Sample (NIS): 2017. Agency for Healthcare Research and Quality. December 2019. Accessed December 1, 2019. https://www.hcup-us.ahrq.gov/db/nation/nis/NISIntroduction2017.pdf

19. Zoorob RJ, Salemi JL, Mejia de Grubb MC, Modak S, Levine RS. A nationwide study of breast cancer, depression, and multimorbidity among hospitalized women and men in the United States. Breast Cancer Res Treat. 2019;174(1):237-248. doi:10.1007/s10549-018-5059-5

20. Cost-to-Charge Ratio Files. Agency for Healthcare Research and Quality. April 2021. Accessed May 4, 2021. https://www.hcup-us.ahrq.gov/db/ccr/ip-ccr/ip-ccr.jsp

21. Personal consumption expenditures: net health insurance: medical care and hospitalization (chain-type price index). FRED Economic Data. Accessed December 12, 2019. https://fred.stlouisfed.org/series/DMINRG3A086NBEA

22. Swallow E, Zhang J, Thomason D, Tan RD, Kageleiry A, Signorovitch J. Real-world patterns of endocrine therapy for metastatic hormone-receptor-positive (HR+)/human epidermal growth factor receptor-2-negative (HER2–) breast cancer patients in the United States: 2002-2012. Curr Med Res Opin. 2014;30(8):1537-1545. doi:10.1185/03007995.2014.908829

23. Dehal A, Abbas A, Johna S. Racial disparities in clinical presentation, surgical treatment and in-hospital outcomes of women with breast cancer: analysis of nationwide inpatient sample database. Breast Cancer Res Treat.2013;139(2):561-569. doi:10.1007/s10549-013-2567-1

24. Clinical Classifications Software (CCS) for ICD-10-PCS: downloading information for the CCS for ICD-10-PCS tool (beta version). Agency for Healthcare Research and Quality. Updated November 5, 2019. Accessed October 31, 2019. https://www.hcup-us.ahrq.gov/toolssoftware/ccs10/ccs10.jsp#download

25. Clinical Classifications Software (CCS) 2015. Agency for Healthcare Research and Quality. March 2016. Accessed December 12, 2019. https://www.hcup-us.ahrq.gov/toolssoftware/ccs/CCSUsersGuide.pdf

26. Lage MJ, Borker R, Barber B, Gao S. Healthcare costs in postmenopausal women with hormone-positive metastatic breast cancer. J Med Econ. 2010;13(4):691-697. doi:10.3111/13696998.2010.531829

27. Yadav S, Karam D, Bin Riaz I, et al. Male breast cancer in the United States: treatment patterns and prognostic factors in the 21st century. Cancer. 2020;126(1):26-36. doi:10.1002/cncr.32472

28. Akinyemiju TF, Vin-Raviv N, Chavez-Yenter D, Zhao X, Budhwani H. Race/ethnicity and socio-economic differences in breast cancer surgery outcomes. Cancer Epidemiol. 2015;39(5):745-751. doi:10.1016/j.canep.2015.07.010

29. Bucknor A, Chattha A, Ultee K, et al. The financial impact and drivers of hospital charges in contralateral prophylactic mastectomy and reconstruction: a Nationwide Inpatient Sample hospital analysis. Breast Cancer Res Treat. 2017;165(2):301-310. doi:10.1007/s10549-017-4315-4

30. Vin-Raviv N, Akinyemiju TF, Galea S, Bovbjerg DH. Depression and anxiety disorders among hospitalized women with breast cancer. PLoS One. 2015;10(6):e0129169. doi:10.1371/journal.pone.0129169

31. Vin-Raviv N, Akinyemiju TF, Galea S, Bovbjerg DH. Sleep disorder diagnoses and clinical outcomes among hospitalized breast cancer patients: a Nationwide Inpatient Sample study. Support Care Cancer.2018;26(6):1833-1840. doi:10.1007/s00520-017-4012-1

32. Patel RS, Wen KY, Aggarwal R. Demographic pattern and hospitalization outcomes of depression among 2.1 million Americans with four major cancers in the United States. Med Sci (Basel). 2018;6(4):93. doi:10.3390/medsci6040093

33. Consumer Price Index data from 1913 to 2021. US Inflation Calculator. Accessed August 16, 2020. https://www.usinflationcalculator.com/inflation/consumer-price-index-and-annual-percent-changes-from-1913-to-2008/

34. Muller CF. Health Care and Gender. Russell Sage Foundation; 1990.

35. Owens GM. Gender differences in health care expenditures, resource utilization, and quality of care. J Manag Care Pharm. 2008;14(suppl 3):2-6. doi:10.18553/jmcp.2008.14.S3-A.2

36. Dehal A, Abbas A, Johna S. Comorbidity and outcomes after surgery among women with breast cancer: analysis of Nationwide In-patient Sample database. Breast Cancer Res Treat.2013;139(2):469-476. doi:10.1007/s10549-013-2543-9

37. Adjei Boakye E, Johnston KJ, Moulin TA, et al. Factors associated with head and neck cancer hospitalization cost and length of stay—a national study. Am J Clin Oncol. 2019;42(2):172-178. doi:10.1097/COC.0000000000000487

38. Avila J, Jupiter D, Chavez-MacGregor M, de Oliveira C, Kaul S. High-cost hospitalizations among elderly patients with cancer. J Oncol Pract. 2019;15(5):e447-e457. doi:10.1200/JOP.18.00706

39. Pathak R, Giri S, Aryal MR, Karmacharya P, Bhatt VR, Martin MG. Mortality, length of stay, and health care costs of febrile neutropenia–related hospitalizations among patients with breast cancer in the United States. Support Care Cancer. 2015;23(3):615-617. doi:10.1007/s00520-014-2553-0

40. Taghizadeh N, Fortin M, Tremblay A. US hospitalizations for malignant pleural effusions: data from the 2012 National Inpatient Sample. Chest. 2017;151(4):845-854. doi:10.1016/j.chest.2016.11.010

41. Surgery for breast cancer. American Cancer Society. Updated September 18, 2019. Accessed January 12, 2019. https://www.cancer.org/cancer/breast-cancer/treatment/surgery-for-breast-cancer.html