ABSTRACT
Objective
To verify whether the presence of related nutritional risk indicators prior to COVID-19 diagnosis is associated with poor survival in patients with cancer.
Methods
We retrospectively analyzed the data of hospitalized cancer patients who tested positive for COVID-19 between March 2020 and February 2021. Nutritional risk was defined as the presence of one of the following characteristics: body mass index <20kg/m 2 , scored Patient-generated Subjective Global Assessment ≥9 points or classification B, albumin level <3.5g/dL, and C-reactive protein level ≥10mg/L, evaluated between 7 and 60 days prior to the date of patient inclusion. The endpoint measure was all-cause mortality within 30 days of COVID-19 diagnosis.
Results
A total of 253 patients were included, most of whom were elderly (62.4%) and female (63.6%). Overall, 45.4% of the patients were at nutritional risk. Survival was significantly lower in patients at nutritional risk (8 days; interquartile range [IQR]: 3-29) than in patients not at nutritional risk (16 days; IQR: 6-30) (p<0.001). The presence of prior nutritional risk was associated with increased 30-day mortality (HR: 1.42; 95%CI: 1.03-1.94), regardless of age, gender, tumor site or stage, and other risk factors, and the model had good discrimination accuracy (concordance statistic: 0.744).
Conclusion
The presence of prior nutritional risk indicators is related to poor prognosis in patients with cancer and COVID-19, emphasizing the importance of nutritional care, notably during this pandemic.
COVID-19; Coronavirus; Coronavirus infections; Malnutrition; Nutritional status; Neoplasms; Prognosis
INTRODUCTION
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), resulting in coronavirus disease 2019 (COVID-19), emerged as a global pandemic owing to its rapid transmission and the susceptibility of the population, posing unprecedented challenges to patients and healthcare systems. ( 11. World Health Organization (WHO). COVID-19 clinical management: living guidance, 25 January 2021. Geneva: WHO; 2021 [cited 2021 Mar 30]. Available from: https://apps.who.int/iris/handle/10665/338882
https://apps.who.int/iris/handle/10665/3...
) More severe complications and deaths have been reported among older patients and individuals with underlying conditions, such as cardiovascular, liver, and kidney disease, and cancer. ( 22. Liang W, Guan W, Chen R, Wang W, Li J, Xu K, et al. Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China. Lancet Oncol. 2020;21(3):335-7. , 33. Petrilli CM, Jones SA, Yang J, Rajagopalan H, O’Donnell L, Chernyak Y, et al. Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ. 2020;369:m1966. )
Patients with cancer are generally assumed to be at high nutritional risk ( 44. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48. ) and appear to be at increased risk of adverse outcomes from COVID-19 infection. ( 55. Dai M, Liu D, Liu M, Zhou F, Li G, Chen Z, et al. Patients with cancer appear more vulnerable to SARS-CoV-2: a multi-center study during the COVID-19 outbreak. Cancer Discov. 2020;10(6):783-91.
6. Kuderer NM, Choueiri TK, Shah DP, Shyr Y, Rubinstein SM, Rivera DR, Shete S, Hsu CY, Desai A, de Lima Lopes G Jr, Grivas P, Painter CA, Peters S, Thompson MA, Bakouny Z, Batist G, Bekaii-Saab T, Bilen MA, Bouganim N, Larroya MB, Castellano D, Del Prete SA, Doroshow DB, Egan PC, Elkrief A, Farmakiotis D, Flora D, Galsky MD, Glover MJ, Griffiths EA, Gulati AP, Gupta S, Hafez N, Halfdanarson TR, Hawley JE, Hsu E, Kasi A, Khaki AR, Lemmon CA, Lewis C, Logan B, Masters T, McKay RR, Mesa RA, Morgans AK, Mulcahy MF, Panagiotou OA, Peddi P, Pennell NA, Reynolds K, Rosen LR, Rosovsky R, Salazar M, Schmidt A, Shah SA, Shaya JA, Steinharter J, Stockerl-Goldstein KE, Subbiah S, Vinh DC, Wehbe FH, Weissmann LB, Wu JT, Wulff-Burchfield E, Xie Z, Yeh A, Yu PP, Zhou AY, Zubiri L, Mishra S, Lyman GH, Rini BI, Warner JL; COVID-19 and Cancer Consortium. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet. 2020;395(10241):1907-18. Erratum in: Lancet. 2020;396(10253):758.
7. Miyashita H, Mikami T, Chopra N, Yamada T, Chernyavsky S, Rizk D, et al. Do Patients with cancer have a poorer prognosis of COVID-19? An experience in New York City. Ann Oncol. 2020;31(8):1088-9. - 88. Tian Y, Qiu X, Wang C, Zhao J, Jiang X, Niu W, et al. Cancer associates with risk and severe events of COVID-19: a systematic review and meta-analysis. Int J Cancer. 2021;148(2):363-74. ) In addition, patients with COVID-19 are at high risk of being malnourished, with poor nutritional status having been associated with progression to severe disease and adverse effects ( e.g., intensive care unit admission, mechanical ventilation requirement, and mortality). ( 99. Wei C, Liu Y, Li Y, Zhang Y, Zhong M, Meng X. Evaluation of the nutritional status in patients with COVID-19. J Clin Biochem Nutr. 2020;67(2):116-21.
10. Wang R, He M, Yin W, Liao X, Wang B, Jin X, et al. The Prognostic Nutritional Index is associated with mortality of COVID-19 patients in Wuhan, China. J Clin Lab Anal. 2020;34(10):e23566.
11. Haraj NE, El Aziz S, Chadli A, Dafir A, Mjabber A, Aissaoui O, et al. Nutritional status assessment in patients with Covid-19 after discharge from the intensive care unit. Clin Nutr ESPEN. 2021;41:423-8. - 1212. Ali AM, Kunugi H. Approaches to Nutritional Screening in Patients with Coronavirus Disease 2019 (COVID-19). Int J Environ Res Public Health. 2021;18(5):2772. Review. )
The prevalence of nutritional risk in hospitalized patients with COVID-19 have been described by different screening methods. ( 1313. Li T, Zhang Y, Gong C, Wang J, Liu B, Shi L, et al. Prevalence of malnutrition and analysis of related factors in elderly patients with COVID-19 in Wuhan, China. Eur J Clin Nutr. 2020;74(6):871-5.
14. Silva DF, Lima SC, Sena-Evangelista KC, Marchioni DM, Cobucci RN, Andrade FB. Nutritional Risk Screening Tools for older adults with COVID-19: a systematic review. Nutrients. 2020;12(10):2956.
15. Bedock D, Bel Lassen P, Mathian A, Moreau P, Couffignal J, Ciangura C, et al. Prevalence and severity of malnutrition in hospitalized COVID-19 patients. Clin Nutr ESPEN. 2020;40:214-9. - 1616. Pironi L, Sasdelli AS, Ravaioli F, Baracco B, Battaiola C, Bocedi G, et al. Malnutrition and nutritional therapy in patients with SARS-CoV-2 disease. Clin Nutr. 2021;40(3):1330-7. ) Despite the possible contribution of poor nutritional status to the acquisition and unfavorable outcomes of COVID-19 infection, there are several knowledge gaps in clinical nutrition applicable to the COVID-19 pandemic, and there is very limited data on the prognostic and predictive role of nutritional risk in these patients. ( 1717. Mechanick JI, Carbone S, Dickerson RN, Hernandez BJ, Hurt RT, Irving SY, Li DY, McCarthy MS, Mogensen KM, Gautier JB, Patel JJ, Prewitt TE, Rosenthal M, Warren M, Winkler MF, McKeever L; ASPEN COVID-19 Task Force on Nutrition Research. Clinical Nutrition Research and the COVID-19 Pandemic: a scoping review of the ASPEN COVID-19 Task Force on Nutrition Research. JPEN J Parenter Enteral Nutr. 2021;45(1):13-31. Review.
18. Zhang P, He Z, Yu G, Peng D, Feng Y, Ling J, et al. The modified NUTRIC score can be used for nutritional risk assessment as well as prognosis prediction in critically ill COVID-19 patients. Clin Nutr. 2021;40(2):534-41. - 1919. Allard L, Ouedraogo E, Molleville J, Bihan H, Giroux-Leprieur B, Sutton A, et al. Malnutrition: Percentage and association with prognosis in patients hospitalized for coronavirus disease 2019. Nutrients. 2020;12(12):3679. ) The interactions of COVID-19 with pre-existing malignancy and nutritional status are poorly described. Indeed, to the best of our knowledge, only one study has evaluated the prognostic role of nutritional risk in a subsample of hospitalized adult patients with cancer and COVID-19. ( 2020. Liang J, Jin G, Liu T, Wen J, Li G, Chen L, et al. Clinical characteristics and risk factors for mortality in cancer patients with COVID-19. Front Med. 2021;15(2):264-74. )
Given that nutritional impairment is common in adult patients with cancer, ( 2121. Muscaritoli M, Lucia S, Farcomeni A, Lorusso V, Saracino V, Barone C, Plastino F, Gori S, Magarotto R, Carteni G, Chiurazzi B, Pavese I, Marchetti L, Zagonel V, Bergo E, Tonini G, Imperatori M, Iacono C, Maiorana L, Pinto C, Rubino D, Cavanna L, Di Cicilia R, Gamucci T, Quadrini S, Palazzo S, Minardi S, Merlano M, Colucci G, Marchetti P; PreMiO Study Group. Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget. 2017;8(45):79884-96.
22. D’Almeida CA, Peres WA, de Pinho NB, Martucci RB, Rodrigues VD, Ramalho A. Prevalence of malnutrition in older hospitalized cancer patients: a multicenter and multiregional study. J Nutr Health Aging. 2020;24(2):166-71.
23. de Pinho NB, Martucci RB, Rodrigues VD, D’Almeida CA, Thuler LC, Saunders C, et al. High prevalence of malnutrition and nutrition impact symptoms in older patients with cancer: results of a Brazilian multicenter study. Cancer. 2020;126(1):156-64. - 2424. Wiegert EV, de Oliveira LC, Calixto-Lima L, Mota E Silva Lopes MS, Peres WA. Cancer cachexia: Comparing diagnostic criteria in patients with incurable cancer. Nutrition. 2020;79-80:110945. ) it follows that the deleterious consequences of malnutrition could impact the patients’ COVID-19 prognosis. ( 1212. Ali AM, Kunugi H. Approaches to Nutritional Screening in Patients with Coronavirus Disease 2019 (COVID-19). Int J Environ Res Public Health. 2021;18(5):2772. Review. , 1717. Mechanick JI, Carbone S, Dickerson RN, Hernandez BJ, Hurt RT, Irving SY, Li DY, McCarthy MS, Mogensen KM, Gautier JB, Patel JJ, Prewitt TE, Rosenthal M, Warren M, Winkler MF, McKeever L; ASPEN COVID-19 Task Force on Nutrition Research. Clinical Nutrition Research and the COVID-19 Pandemic: a scoping review of the ASPEN COVID-19 Task Force on Nutrition Research. JPEN J Parenter Enteral Nutr. 2021;45(1):13-31. Review. ) Additionally, given the global prevalence of cancer and the high transmissibility of SARS-CoV-2, an understanding of the disease course of COVID-19 and factors influencing clinical outcomes in patients with cancer is urgently needed. ( 66. Kuderer NM, Choueiri TK, Shah DP, Shyr Y, Rubinstein SM, Rivera DR, Shete S, Hsu CY, Desai A, de Lima Lopes G Jr, Grivas P, Painter CA, Peters S, Thompson MA, Bakouny Z, Batist G, Bekaii-Saab T, Bilen MA, Bouganim N, Larroya MB, Castellano D, Del Prete SA, Doroshow DB, Egan PC, Elkrief A, Farmakiotis D, Flora D, Galsky MD, Glover MJ, Griffiths EA, Gulati AP, Gupta S, Hafez N, Halfdanarson TR, Hawley JE, Hsu E, Kasi A, Khaki AR, Lemmon CA, Lewis C, Logan B, Masters T, McKay RR, Mesa RA, Morgans AK, Mulcahy MF, Panagiotou OA, Peddi P, Pennell NA, Reynolds K, Rosen LR, Rosovsky R, Salazar M, Schmidt A, Shah SA, Shaya JA, Steinharter J, Stockerl-Goldstein KE, Subbiah S, Vinh DC, Wehbe FH, Weissmann LB, Wu JT, Wulff-Burchfield E, Xie Z, Yeh A, Yu PP, Zhou AY, Zubiri L, Mishra S, Lyman GH, Rini BI, Warner JL; COVID-19 and Cancer Consortium. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet. 2020;395(10241):1907-18. Erratum in: Lancet. 2020;396(10253):758. )
In the context, we hypothesize that, among patients with cancer who are diagnosed with COVID-19, mortality incidence differs between patients who are at nutritional risk and those who are not at nutritional risk.
OBJECTIVE
To verify whether the presence of related nutritional risk indicators prior to COVID-19 diagnosis is associated with poor survival in patients with cancer.
METHODS
Patients and study design
A hospital-based retrospective observational cohort study was conducted with data extracted from the electronic medical records of all the patients hospitalized for COVID-19 at the reference cancer institute between March 2020 and February 2021.
Inclusion criteria were: age ≥20 years; confirmed diagnosis of malignant neoplasm (active treatment or exclusive palliative care), regardless of tumor site and time of diagnosis; hospitalized for COVID-19, confirmed by a positive reverse-transcriptase polymerase chain reaction (RT-PCR) test for SARS-CoV-2. ( 11. World Health Organization (WHO). COVID-19 clinical management: living guidance, 25 January 2021. Geneva: WHO; 2021 [cited 2021 Mar 30]. Available from: https://apps.who.int/iris/handle/10665/338882
https://apps.who.int/iris/handle/10665/3...
) Patients without a positive RT-PCR test (n=45), who were not admitted to hospital during infection (n=180), and with missing nutritional risk data (n=148) were excluded ( Figure 1 ). None of the patients had received any dose of vaccine against COVID-19, as there was none available at the time of participant recruitment.
The study was approved by the Research Ethics Committee of the Instituto Nacional de Câncer (INCA), CAAE: 31053220.0.0000.5274; # 4.511.910. Informed consent was waived because data were extracted from medical records retrospectively (non-invasive observational study).
Demographic and clinical data were collected at hospital admission whenever a patient had a positive SARS-CoV-2 test result.
Patients were followed up from the date of hospital admission until 30 days after inclusion in the study. Outcomes were monitored up to March 31, 2021, the final date of follow-up.
Data collection
Nutritional risk
The main independent variable evaluated was the presence of nutritional risk (yes/no). Nutritional risk was defined as the presence of one of the following characteristics: body mass index (BMI) <20kg/m 2 , score Patient-Generated Subjective Global Assessment (PG-SGA) ≥9 points or global classification B (suspected malnutrition), ( 2525. Jager-Wittenaar H, Ottery FD. Assessing nutritional status in cancer: role of the Patient-Generated Subjective Global Assessment. Curr Opin Clin Nutr Metab Care. 2017;20(5):322-9. Review. ) albumin level <3.5g/dL, and C-reactive protein (CRP) level ≥10mg/L. ( 44. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48. , 2626. Cederholm T, Jensen GL, Correia MI, Gonzalez MC, Fukushima R, Higashiguchi T, Baptista G, Barazzoni R, Blaauw R, Coats A, Crivelli A, Evans DC, Gramlich L, Fuchs-Tarlovsky V, Keller H, Llido L, Malone A, Mogensen KM, Morley JE, Muscaritoli M, Nyulasi I, Pirlich M, Pisprasert V, de van der Schueren MA, Siltharm S, Singer P, Tappenden K, Velasco N, Waitzberg D, Yamwong P, Yu J, Van Gossum A, Compher C; GLIM Core Leadership Committee; GLIM Working Group. GLIM criteria for the diagnosis of malnutrition - a consensus report from the global clinical nutrition community. Clin Nutr. 2019;38(1):1-9. )
Assuming a mean delay of approximately one week between COVID-19 infection and a positive diagnosis, the nutritional risk data analyzed were from 7 to 60 days prior to the date of the patients’ inclusion (median: 16; interquartile range [IQR]: 9-30 days) and were available for 253 of the 401 patients selected for the study. There was no statistical difference between the patients included in the sample and the ones for whom nutritional risk data were missing: age (p=0.132), gender (p=0.354), primary tumor site (p=0.247) and Karnofsky Performance Status or ECOG-Performance Status (p=0.157).
Other covariates
The demographic data collected from the enrolled patients were: age (<60 or >60 years) and gender (male or female). The clinical characteristics included cancer diagnosis (site of primary cancer: gynecological, gastrointestinal tract, breast, head and neck, lung, bone and connective tissue, or other); tumor stage at the time of inclusion in the study (stages I and II [no metastasis] or stages III and IV [local or distant metastasis]); number of metastasis sites (<1 or >2); lung metastasis at the time of inclusion in the study (in patients without primary lung cancer) (yes or no); surgery and/or chemotherapy and/or radiation therapy within 60 days of admission (yes or no); and preexisting comorbidities ( diabetes mellitus , systemic arterial hypertension, cardiovascular disease or chronic obstructive pulmonary disease [yes or no]). Performance status data were obtained by administering the simple 6-item ECOG-PS scale that ranges from 0 (normal activity) to 5 (dead), ( 2727. Eastern Cooperative Oncology Group (ECOG-ACRIN). Cancer Research Group. ECOG Performance Status. Philadelphia (PA): ECOG-ACRIN; 2022 [cited 2021 Mar 13]. Available from: https://ecog-acrin.org/resources/ecog-performance-status
https://ecog-acrin.org/resources/ecog-pe...
, 2828. Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5(6):649-55. ) or the 11-point KPS scale, with scores ranging from 100 (normal activity) to 0 (dead). ( 2929. Karnofsky DA, Burchenal JH. The clinical evaluation of chemotherapeutic agents in cancer. In: Mac Leod CM, editor. Evaluation of chemotherapeutic agents. New York: Columbia Univ Press; 1949. p.199-205. ) These scales were converted and categorized as ECOG-PS score ≥3 or KPS score ≤40% (yes or no), as suggested by Ma et al. ( 3030. Ma C, Bandukwala S, Burman D, Bryson J, Seccareccia D, Banerjee S, et al. Interconversion of three measures of performance status: an empirical analysis. Eur J Cancer. 2010;46(18):3175-83. )
Outcome
The endpoint measure was all-cause mortality within 30 days of COVID-19 diagnosis. Survival was assessed longitudinally, counting from the date of the positive COVID-19 test until death. For the analyses, the survival times were censored on the patients who were alive after this endpoint.
Statistical analysis
Statistical analyses were performed using Stata 13.1 (Stata Corp., College Station, Texas, USA). Statistical significance was set at p<0.05.
The Kolmogorov-Smirnov test was used to assess the distribution of variables. Numerical variables were described as medians with iterquartile range (IQR) IQR (25 th and 75 th percentiles) and categorical variables were described as absolute (n) and relative frequencies (%). Proportions were compared using the χ 2 test, and medians were compared using the corresponding non-parametric test, the Mann-Whitney U test.
The Kaplan-Meier method and the log-rank test were used to compare survival according to groups. The Cox proportional hazard model was used to assess the predictive ability of nutritional risk, using hazard ratios (HRs) with 95% confidence interval (95%CI). All the factors with p<0.20 in the univariate analysis were included in the multivariate analysis. The final model was produced using the backward selection, and the variables with p value <0.05 were maintained.
Harrell’s C-statistic ( 3131. Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15(4):361-87. Review. ) with 95%CI was applied to assess the discriminatory power of nutritional risk in predicting 30-day mortality; 0.50 indicates the outcome as well as chance, 0.70 to <0.80: good discrimination, 0.80 to <0.90: excellent discrimination, 0.90 to <1.00: outstanding discrimination, and 1.00: perfect prediction. ( 3232. Hosmer DW, Hosmer T, Le Cessie S, Lemeshow S. A comparison of goodness-of-fit tests for the logistic regression model. Stat Med. 1997;16(9):965-80. Review. )
RESULTS
A total of 253 patients with cancer and COVID-19 were included in the analysis. The patients were predominantly older (≥60 years, 62.4%) and female (63.6%). Breast was the most prevalent tumor site (19.8%), followed by gastrointestinal tract (18.6%), and 82.6% of the patients were at stage III or IV ( Table 1 ).
The proportion of patients with PG-SGA score ≥9 points or classification B was 66.7%. In addition, 54.1% had hypoalbuminemia, 19.0% had BMI <20kg/m 2 , and 33.5% had CRP >10mg/L. Overall, 45.4% of the patients presented some characteristics related to nutritional risk ( Figure 2 ).
The prevalence of nutritional risk factors parameters among patients with cancer and COVID-19 diagnoses
The prevalence of nutritional risk varied according to the assessment criteria and the clinical and demographic characteristics. The median time from confirmed COVID-19 diagnosis to the study endpoints (death or discharge from hospital) was 11 days (IQR: 4-30). At analysis (March 31, 2021), 166 (65.6%) of the patients had died, all within 30 days of COVID-19 diagnosis. There was a higher proportion of deaths among the patients at nutritional risk than among the patients not at nutritional risk (p=0.001) ( Table 1 ). It is worth noting that, in our study, it was enough for patients to fulfill just one of the criteria used to identify nutritional risk, and that even though 85 patients fulfilled one of these criteria, 15 fulfilled two, 10 fulfilled three, and 5 fulfilled all four, there was no statistical difference in the proportion of deaths across these groups (data not shown).
Survival was significantly lower in patients at nutritional risk (8 days; IQR: 3-29) than in patients not at nutritional risk (16 days; IQR: 6-30) (log rank p<0.001) ( Figure 3A ). Additionally, according to the Kaplan-Meier curves, survival was also lower when each nutritional risk indicator was evaluated separately: BMI <20kg/m 2 (2 versus 16 days; log-rank p=0.008; Figure 3B ); PG-SGA score ≥9 points or classification B (7 versus 14 days; log-rank p=0.043; Figure 3C ); albumin <3.5g/dL and/or CRP ≥10mg/L (9 versus 14 days; log-rank p=0.016; Figure 3D ).
Survival curves of patients with cancer and COVID-19 diagnosis according to nutritional risk (A) and their indicators: BMI (B), PG-SGA score (C) and CRP or albumin level (D)
According to the Cox regression analysis adjusted for multiple covariates, the presence of nutritional risk in patients with both cancer and COVID-19 was associated with a higher risk of 30-day mortality (HR: 1.42; 95%CI: 1.03-1.94).
In this multivariate model, only nutritional risk and poor performance status by KPS/ECOG-PS remained a risk factor for 30-day mortality (HR: 2.41; 95%CI: 1.71-3.42). In addition, nutritional risk was found to have good predictive power for prognostic discrimination (C-statistic: 0.744; 95%CI: 0.696-0.765) ( Table 2 ).
DISCUSSION
The literature on the relationship between cancer-associated nutritional risk and COVID-19 outcomes is scant. In this study, patients at nutritional risk had significantly (almost 50%) higher of 30-day mortality than those not at nutritional risk. These findings suggest that patients with cancer at nutritional risk tend to have worse survival outcomes when infected with SARS-CoV-2.
In our results, prior nutritional risk in patients with cancer and COVID-19 varied according to: primary tumor site (higher prevalence in patients with bone and connective tissue (66.7%), gynecological (58.3%), and gastrointestinal tract (57.4%) cancer, all with p<0.050); disease stage (p=0.046); and performance status (p<0.001).
It is widely recognized that nutritional risk is common in patients with cancer, sometimes predating diagnosis, and previous evidence demonstrates that the prevalence of nutritional risk varies according to several factors. ( 2121. Muscaritoli M, Lucia S, Farcomeni A, Lorusso V, Saracino V, Barone C, Plastino F, Gori S, Magarotto R, Carteni G, Chiurazzi B, Pavese I, Marchetti L, Zagonel V, Bergo E, Tonini G, Imperatori M, Iacono C, Maiorana L, Pinto C, Rubino D, Cavanna L, Di Cicilia R, Gamucci T, Quadrini S, Palazzo S, Minardi S, Merlano M, Colucci G, Marchetti P; PreMiO Study Group. Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget. 2017;8(45):79884-96.
22. D’Almeida CA, Peres WA, de Pinho NB, Martucci RB, Rodrigues VD, Ramalho A. Prevalence of malnutrition in older hospitalized cancer patients: a multicenter and multiregional study. J Nutr Health Aging. 2020;24(2):166-71.
23. de Pinho NB, Martucci RB, Rodrigues VD, D’Almeida CA, Thuler LC, Saunders C, et al. High prevalence of malnutrition and nutrition impact symptoms in older patients with cancer: results of a Brazilian multicenter study. Cancer. 2020;126(1):156-64. - 2424. Wiegert EV, de Oliveira LC, Calixto-Lima L, Mota E Silva Lopes MS, Peres WA. Cancer cachexia: Comparing diagnostic criteria in patients with incurable cancer. Nutrition. 2020;79-80:110945. ) In a multicenter study of 1,952 patients making their first appointment with an oncologist, 42.4% were found to be at nutritional risk according to their Mini Nutritional Assessment score. ( 2121. Muscaritoli M, Lucia S, Farcomeni A, Lorusso V, Saracino V, Barone C, Plastino F, Gori S, Magarotto R, Carteni G, Chiurazzi B, Pavese I, Marchetti L, Zagonel V, Bergo E, Tonini G, Imperatori M, Iacono C, Maiorana L, Pinto C, Rubino D, Cavanna L, Di Cicilia R, Gamucci T, Quadrini S, Palazzo S, Minardi S, Merlano M, Colucci G, Marchetti P; PreMiO Study Group. Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget. 2017;8(45):79884-96. ) Oliveira et al. ( 3333. Oliveira LC, Abreu GT, Lima LC, Aredes MA, Wiegert EV. Quality of life and its relation with nutritional status in patients with incurable cancer in palliative care. Support Care Cancer. 2020;28(10):4971-8. ) found 85.4% prevalence of nutritional risk among 1,039 patients with advanced cancer in palliative care, using the PG-SGA short form. Other studies have found varying prevalence of nutritional risk among non-cancer patients hospitalized with COVID-19 using different screening methods. ( 1313. Li T, Zhang Y, Gong C, Wang J, Liu B, Shi L, et al. Prevalence of malnutrition and analysis of related factors in elderly patients with COVID-19 in Wuhan, China. Eur J Clin Nutr. 2020;74(6):871-5.
14. Silva DF, Lima SC, Sena-Evangelista KC, Marchioni DM, Cobucci RN, Andrade FB. Nutritional Risk Screening Tools for older adults with COVID-19: a systematic review. Nutrients. 2020;12(10):2956.
15. Bedock D, Bel Lassen P, Mathian A, Moreau P, Couffignal J, Ciangura C, et al. Prevalence and severity of malnutrition in hospitalized COVID-19 patients. Clin Nutr ESPEN. 2020;40:214-9. - 1616. Pironi L, Sasdelli AS, Ravaioli F, Baracco B, Battaiola C, Bocedi G, et al. Malnutrition and nutritional therapy in patients with SARS-CoV-2 disease. Clin Nutr. 2021;40(3):1330-7. )
Cancer has been found to be associated with a higher risk of death in patients with COVID-19. ( 55. Dai M, Liu D, Liu M, Zhou F, Li G, Chen Z, et al. Patients with cancer appear more vulnerable to SARS-CoV-2: a multi-center study during the COVID-19 outbreak. Cancer Discov. 2020;10(6):783-91.
6. Kuderer NM, Choueiri TK, Shah DP, Shyr Y, Rubinstein SM, Rivera DR, Shete S, Hsu CY, Desai A, de Lima Lopes G Jr, Grivas P, Painter CA, Peters S, Thompson MA, Bakouny Z, Batist G, Bekaii-Saab T, Bilen MA, Bouganim N, Larroya MB, Castellano D, Del Prete SA, Doroshow DB, Egan PC, Elkrief A, Farmakiotis D, Flora D, Galsky MD, Glover MJ, Griffiths EA, Gulati AP, Gupta S, Hafez N, Halfdanarson TR, Hawley JE, Hsu E, Kasi A, Khaki AR, Lemmon CA, Lewis C, Logan B, Masters T, McKay RR, Mesa RA, Morgans AK, Mulcahy MF, Panagiotou OA, Peddi P, Pennell NA, Reynolds K, Rosen LR, Rosovsky R, Salazar M, Schmidt A, Shah SA, Shaya JA, Steinharter J, Stockerl-Goldstein KE, Subbiah S, Vinh DC, Wehbe FH, Weissmann LB, Wu JT, Wulff-Burchfield E, Xie Z, Yeh A, Yu PP, Zhou AY, Zubiri L, Mishra S, Lyman GH, Rini BI, Warner JL; COVID-19 and Cancer Consortium. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet. 2020;395(10241):1907-18. Erratum in: Lancet. 2020;396(10253):758.
7. Miyashita H, Mikami T, Chopra N, Yamada T, Chernyavsky S, Rizk D, et al. Do Patients with cancer have a poorer prognosis of COVID-19? An experience in New York City. Ann Oncol. 2020;31(8):1088-9. - 88. Tian Y, Qiu X, Wang C, Zhao J, Jiang X, Niu W, et al. Cancer associates with risk and severe events of COVID-19: a systematic review and meta-analysis. Int J Cancer. 2021;148(2):363-74. ) A study conducted by Fernandes et al. ( 3434. Fernandes GA, Feriani D, França e Silva IL, Mendonça e Silva DR, Arantes PE, Canteras JD, et al. Differences in mortality of cancer patients with COVID-19 in a Brazilian cancer center. Semin Oncol. 2021;48(2):171-80. ) among 411 patients with cancer and COVID-19 showed that 12.4% died and patients receiving palliative care were more likely to die (HR: 17.66; 95%CI: 3.13-99.59). In evaluating a subset of 109 patients with cancer from a cohort of 3,060 patients with COVID-19, Liang et al. ( 2020. Liang J, Jin G, Liu T, Wen J, Li G, Chen L, et al. Clinical characteristics and risk factors for mortality in cancer patients with COVID-19. Front Med. 2021;15(2):264-74. ) observed that 23 (21.1%) of them died, with a median time from admission to death of 7.62 days (IQR: 4.44-17.25). In addition, patients with cancer were at a higher risk of mortality than patients without cancer. Melo et al., ( 3535. Melo AC, Thuler LC, Silva JL, Albuquerque LZ, Pecego AC, Rodrigues LO, da Conceição MS, Garrido MM, Quintella Mendes GL, Mendes Pereira AC, Soares MA, Viola JP; Brazilian National Cancer Institute COVID-19 Task Force. Cancer inpatients with COVID-19: a report from the Brazilian National Cancer Institute. PLoS One. 2020;15(10):e0241261. ) found 37.7% mortality in patients with cancer and COVID-19, and a significantly higher mortality risk in patients with higher serum CRP values (p=0.002). Pérez Camargo et al. ( 3636. Pérez Camargo DA, Vargas Gutiérrez G, Rivera Franco MM, Labana Ramírez A, Castro Herrera M, Urbalejo Ceniceros VI, et al. Nutritional status in patients with COVID-19 and cancer: the experience of the National Cancer Institute in Mexico. Nutr Hosp. 2021;38(6):1263-8. ) evaluated 121 cancer patients diagnosed with COVID-19, finding in the univariate analysis that hypoalbuminemia and nutritional impact symptoms were associated with lower survival. This is consistent with our finding that nutritional risk was associated with an increased risk of mortality. Our multivariate Cox analysis revealed that nutritional risk was an independent prognostic factor for 30-day mortality in cancer patients hospitalized for COVID-19 (HR: 1.42; 95%CI: 1.03-1.94), regardless of age, sex, tumor site, disease stage, comorbidities, or other recognized risk factors.
Additionally, our study found that nutritional risk had good discriminatory accuracy for predicting death (C-statistic: 0.744), albeit lower than that of the performance status scales (C-statistic: 0.745, data not shown). This was expected, considering that KPS and ECOG-PS are recognized as important scales for decision-making in cancer care and have good predictive accuracy for survival. ( 3737. Zhao X, Li Y, Ge Y, Shi Y, Lv P, Zhang J, et al. Evaluation of nutrition risk and its association with mortality risk in severely and critically ill COVID-19 patients. JPEN J Parenter Enteral Nutr. 2021;45(1):32-42.
38. Jang RW, Caraiscos VB, Swami N, Banerjee S, Mak E, Kaya E, et al. Simple prognostic model for patients with advanced cancer based on performance status. J Oncol Pract. 2014;10(5):e335-41.
39. Rosa KS, Cypriano RP, Albuquerque NM, Oliveira LC. Predictive factors of death on hospitalization in patients with advanced cancer in palliative care. Am J Hosp Palliat Care. 2021;38(10):1189-94. - 4040. Oliveira LC, da Costa Rosa KS, Borsatto AZ, Oliveira LA, Freitas R, Sampaio SG. Prognostic factors in patients with advanced cancer and COVID-19: a cohort from the Palliative Care Unit of the Brazilian National Cancer Institute. Support Care Cancer. 2021;29(10):6005-12. ) Therefore, even though nutritional risk preceded COVID-19 diagnosis, its predictive accuracy was similar to that of the performance status scales and other prognostic tools, such as the Palliative Prognostic Score (C-statistic: >0.79), the Palliative Prognostic Index (C-statistic: >0.75), ( 4141. Baba M, Maeda I, Morita T, Inoue S, Ikenaga M, Matsumoto Y, et al. Survival prediction for advanced cancer patients in the real world: a comparison of the Palliative Prognostic Score, Delirium-Palliative Prognostic Score, Palliative Prognostic Index and modified Prognosis in Palliative Care Study predictor model. Eur J Cancer. 2015;51(12):1618-29. ) the Alternative International Prognostic Score-E (C-statistic: 0.70), ( 4242. Morabito F, Tripepi G, Vigna E, Bossio S, D’Arrigo G, Martino EA, et al. Validation of the Alternative International Prognostic Score-E (AIPS-E): Analysis of binet stage A chronic lymphocytic leukemia patients enrolled into the O-CLL1-GISL protocol. Eur J Haematol. 2021;106(6):831-5. ) and the American Joint Committee on Cancer TNM Classification of Malignant Tumors (C-statistic: 0.74). ( 4343. Lin JX, Desiderio J, Lin JP, Wang W, Tu RH, Li P, et al. Multicenter Validation Study of the American Joint Commission on Cancer (8th Edition) for Gastric Cancer: Proposal for a Simplified and Improved TNM Staging System. J Cancer. 2020;11(12):3483-91. )
Published evidence about nutritional risk in patients with cancer and COVID-19 remains scant; however, a strong association has been found between lower survival and nutritional risk among non-cancer patients with COVID-19. ( 1313. Li T, Zhang Y, Gong C, Wang J, Liu B, Shi L, et al. Prevalence of malnutrition and analysis of related factors in elderly patients with COVID-19 in Wuhan, China. Eur J Clin Nutr. 2020;74(6):871-5. , 1818. Zhang P, He Z, Yu G, Peng D, Feng Y, Ling J, et al. The modified NUTRIC score can be used for nutritional risk assessment as well as prognosis prediction in critically ill COVID-19 patients. Clin Nutr. 2021;40(2):534-41. ) Nutritional risk and malnutrition are common in cancer, and can make patients more susceptible to severe respiratory tract infections. ( 4444. Briguglio M, Pregliasco FE, Lombardi G, Perazzo P, Banfi G. The malnutritional status of the host as a virulence factor for new coronavirus SARS-CoV-2. Front Med (Lausanne). 2020;7:146. , 4545. Barazzoni R, Bischoff SC, Breda J, Wickramasinghe K, Krznaric Z, Nitzan D, Pirlich M, Singer P; endorsed by the ESPEN Council. ESPEN expert statements and practical guidance for nutritional management of individuals with SARS-CoV-2 infection. Clin Nutr. 2020;39(6):1631-8. ) Changes in nutritional status in patients with cancer differ from those found in patients with diseases of non-oncological etiology, and these changes are multifactorial. They result from the pathophysiological alterations caused by tumor-host interactions, such as increased pro-inflammatory activity, alteration of neuroendocrine signaling, protein catabolism, chemosensory alterations, decreased food intake, and greater occurrence of symptoms of nutritional impact. ( 44. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48. , 4646. Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol. 2011;12(5):489-95. Review. ) The acute inflammatory process caused by infection concomitant with nutritional impairment in the host causes an increase in the pathogenicity of the infectious agent, resulting in worse clinical outcomes. ( 4444. Briguglio M, Pregliasco FE, Lombardi G, Perazzo P, Banfi G. The malnutritional status of the host as a virulence factor for new coronavirus SARS-CoV-2. Front Med (Lausanne). 2020;7:146. , 4545. Barazzoni R, Bischoff SC, Breda J, Wickramasinghe K, Krznaric Z, Nitzan D, Pirlich M, Singer P; endorsed by the ESPEN Council. ESPEN expert statements and practical guidance for nutritional management of individuals with SARS-CoV-2 infection. Clin Nutr. 2020;39(6):1631-8. ) This could be explained by the fact that patients with cancer are in a state of metabolic stress characterized by adverse outcomes and increased complications. ( 4444. Briguglio M, Pregliasco FE, Lombardi G, Perazzo P, Banfi G. The malnutritional status of the host as a virulence factor for new coronavirus SARS-CoV-2. Front Med (Lausanne). 2020;7:146. , 4545. Barazzoni R, Bischoff SC, Breda J, Wickramasinghe K, Krznaric Z, Nitzan D, Pirlich M, Singer P; endorsed by the ESPEN Council. ESPEN expert statements and practical guidance for nutritional management of individuals with SARS-CoV-2 infection. Clin Nutr. 2020;39(6):1631-8. ) Additionally, nutritional impact symptoms found in cancer, such as anorexia, anosmia, and weight loss, are also common with SARS-CoV-2 infection, potentially exacerbating the nutritional deficits already observed in patients with active malignancy. ( 4747. Tu H, Tu S, Gao S, Shao A, Sheng J. Current epidemiological and clinical features of COVID-19; a global perspective from China. J Infect. 2020;81(1):1-9. Review.
48. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497-506. Erratum in: Lancet. 2020 Jan 30. - 4949. Brugliera L, Spina A, Castellazzi P, Cimino P, Arcuri P, Negro A, et al. Nutritional management of COVID-19 patients in a rehabilitation unit. Eur J Clin Nutr. 2020;74(6):860-3. Review. )
The parameters used in our study to assess nutritional risk are recognized for this purpose, and their advantages and disadvantages should be considered, ( 44. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48. , 2121. Muscaritoli M, Lucia S, Farcomeni A, Lorusso V, Saracino V, Barone C, Plastino F, Gori S, Magarotto R, Carteni G, Chiurazzi B, Pavese I, Marchetti L, Zagonel V, Bergo E, Tonini G, Imperatori M, Iacono C, Maiorana L, Pinto C, Rubino D, Cavanna L, Di Cicilia R, Gamucci T, Quadrini S, Palazzo S, Minardi S, Merlano M, Colucci G, Marchetti P; PreMiO Study Group. Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget. 2017;8(45):79884-96.
22. D’Almeida CA, Peres WA, de Pinho NB, Martucci RB, Rodrigues VD, Ramalho A. Prevalence of malnutrition in older hospitalized cancer patients: a multicenter and multiregional study. J Nutr Health Aging. 2020;24(2):166-71.
23. de Pinho NB, Martucci RB, Rodrigues VD, D’Almeida CA, Thuler LC, Saunders C, et al. High prevalence of malnutrition and nutrition impact symptoms in older patients with cancer: results of a Brazilian multicenter study. Cancer. 2020;126(1):156-64.
24. Wiegert EV, de Oliveira LC, Calixto-Lima L, Mota E Silva Lopes MS, Peres WA. Cancer cachexia: Comparing diagnostic criteria in patients with incurable cancer. Nutrition. 2020;79-80:110945. - 2525. Jager-Wittenaar H, Ottery FD. Assessing nutritional status in cancer: role of the Patient-Generated Subjective Global Assessment. Curr Opin Clin Nutr Metab Care. 2017;20(5):322-9. Review. , 5050. Brasil. Ministério da Saúde. Instituro Nacional de Câncer José Alencar Gomes da Silva (INCA). Consenso Nacional de Nutrição Oncológica. 2a ed. Rio de Janeiro (RJ): INCA; 2015 [citado 2022 Set 19]. Disponível em: https://www.inca.gov.br/sites/ufu.sti.inca.local/files//media/document//consenso-nacional-de-nutricao-oncologica-2-edicao-2015.pdf
https://www.inca.gov.br/sites/ufu.sti.in...
) as should the different features of malnutrition. As these were recorded prior to COVID-19 diagnosis, they may have changed before hospitalization in parallel with the disease progression. In addition, during the pandemic, nutritional status could have been impaired by difficulty in accessing supportive care and acquiring food due to the restrictions imposed to curb the spread of the virus. ( 5151. Lobascio F, Caccialanza R, Monaco T, Cereda E, Secondino S, Masi S, et al. Providing nutritional care to cancer patients during the COVID-19 pandemic: an Italian perspective. Support Care Cancer. 2020;28(9):3987-9. )
Considering its convenience, low cost, and good ability to predict outcomes in patients with cancer, nutritional screening should be included as an integral part of the care approach for these patients, especially in the context of the COVID-19 pandemic. Because nutritional risk is a modifiable factor that can be reduced or controlled with early, individualized nutritional therapy after identifying nutritional risk could help prevent the disease from progressing and improve the prognosis for cancer patients infected with COVID-19. ( 1212. Ali AM, Kunugi H. Approaches to Nutritional Screening in Patients with Coronavirus Disease 2019 (COVID-19). Int J Environ Res Public Health. 2021;18(5):2772. Review. , 5151. Lobascio F, Caccialanza R, Monaco T, Cereda E, Secondino S, Masi S, et al. Providing nutritional care to cancer patients during the COVID-19 pandemic: an Italian perspective. Support Care Cancer. 2020;28(9):3987-9. ) This supports the idea that any nutritional derangements should be promptly and systematically managed in cancer patients with COVID-19, ( 5252. Caccialanza R, Laviano A, Lobascio F, Montagna E, Bruno R, Ludovisi S, et al. Early nutritional supplementation in non-critically ill patients hospitalized for the 2019 novel coronavirus disease (COVID-19): rationale and feasibility of a shared pragmatic protocol. Nutrition. 2020;74:110835. , 5353. Yárnoz-Esquíroz P, Chopitea A, Olazarán L, Aguas-Ayesa M, Silva C, Vilalta-Lacarra A, et al. Impact on the Nutritional Status and Inflammation of Patients with Cancer Hospitalized after the SARS-CoV-2 Lockdown. Nutrients. 2022;14(13):2754. ) and that nutritional care should be an integral part of care for these patients. However, future intervention trials are required to improve the current evidence.
Our findings cannot be considered conclusive due to an inherent bias caused by the study’s hospital-based retrospective nature and the fact that it did not include a control group of non-cancer patients with malnutrition and COVID-19, since it was carried out in a specialized cancer hospital. However, the data still highlight the importance of frequent nutritional screening to enable malnutrition in cancer patients to be detected and treated early in order to improve COVID-19 outcomes.
Another limitation of our study is that high CRP concentration is considered both a nutritional prognostic marker ( 44. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48. ) and an associated factor of mortality for cancer and COVID-19 patients. ( 3535. Melo AC, Thuler LC, Silva JL, Albuquerque LZ, Pecego AC, Rodrigues LO, da Conceição MS, Garrido MM, Quintella Mendes GL, Mendes Pereira AC, Soares MA, Viola JP; Brazilian National Cancer Institute COVID-19 Task Force. Cancer inpatients with COVID-19: a report from the Brazilian National Cancer Institute. PLoS One. 2020;15(10):e0241261. , 3838. Jang RW, Caraiscos VB, Swami N, Banerjee S, Mak E, Kaya E, et al. Simple prognostic model for patients with advanced cancer based on performance status. J Oncol Pract. 2014;10(5):e335-41. ) Although the CRP values considered in this study were evaluated before COVID-19 diagnosis, this marker is used to assess the magnitude (acute or chronic) of systemic inflammatory response, ( 55. Dai M, Liu D, Liu M, Zhou F, Li G, Chen Z, et al. Patients with cancer appear more vulnerable to SARS-CoV-2: a multi-center study during the COVID-19 outbreak. Cancer Discov. 2020;10(6):783-91. ) so its use could be considered a bias. Finally, our outcome assessment may be flawed because some of the discharged patients may have been readmitted elsewhere with severe illness and died after the follow-up period.
These results reinforce several important considerations for clinical care and emphasize the importance of nutritional care in patients with cancer. The prevention, screening, and treatment of nutritional risk should be included in the routine care of cancer patients with COVID-19.
CONCLUSION
This study demonstrates that the presence of prior nutritional risk is related to poor prognosis in patients with cancer and COVID-19. Since nutritional risk is a potentially modifiable factor, nutrition could be an important element for improving the clinical outcomes of these patients in the context of the pandemic.
REFERENCES
-
1World Health Organization (WHO). COVID-19 clinical management: living guidance, 25 January 2021. Geneva: WHO; 2021 [cited 2021 Mar 30]. Available from: https://apps.who.int/iris/handle/10665/338882
» https://apps.who.int/iris/handle/10665/338882 -
2Liang W, Guan W, Chen R, Wang W, Li J, Xu K, et al. Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China. Lancet Oncol. 2020;21(3):335-7.
-
3Petrilli CM, Jones SA, Yang J, Rajagopalan H, O’Donnell L, Chernyak Y, et al. Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study. BMJ. 2020;369:m1966.
-
4Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48.
-
5Dai M, Liu D, Liu M, Zhou F, Li G, Chen Z, et al. Patients with cancer appear more vulnerable to SARS-CoV-2: a multi-center study during the COVID-19 outbreak. Cancer Discov. 2020;10(6):783-91.
-
6Kuderer NM, Choueiri TK, Shah DP, Shyr Y, Rubinstein SM, Rivera DR, Shete S, Hsu CY, Desai A, de Lima Lopes G Jr, Grivas P, Painter CA, Peters S, Thompson MA, Bakouny Z, Batist G, Bekaii-Saab T, Bilen MA, Bouganim N, Larroya MB, Castellano D, Del Prete SA, Doroshow DB, Egan PC, Elkrief A, Farmakiotis D, Flora D, Galsky MD, Glover MJ, Griffiths EA, Gulati AP, Gupta S, Hafez N, Halfdanarson TR, Hawley JE, Hsu E, Kasi A, Khaki AR, Lemmon CA, Lewis C, Logan B, Masters T, McKay RR, Mesa RA, Morgans AK, Mulcahy MF, Panagiotou OA, Peddi P, Pennell NA, Reynolds K, Rosen LR, Rosovsky R, Salazar M, Schmidt A, Shah SA, Shaya JA, Steinharter J, Stockerl-Goldstein KE, Subbiah S, Vinh DC, Wehbe FH, Weissmann LB, Wu JT, Wulff-Burchfield E, Xie Z, Yeh A, Yu PP, Zhou AY, Zubiri L, Mishra S, Lyman GH, Rini BI, Warner JL; COVID-19 and Cancer Consortium. Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. Lancet. 2020;395(10241):1907-18. Erratum in: Lancet. 2020;396(10253):758.
-
7Miyashita H, Mikami T, Chopra N, Yamada T, Chernyavsky S, Rizk D, et al. Do Patients with cancer have a poorer prognosis of COVID-19? An experience in New York City. Ann Oncol. 2020;31(8):1088-9.
-
8Tian Y, Qiu X, Wang C, Zhao J, Jiang X, Niu W, et al. Cancer associates with risk and severe events of COVID-19: a systematic review and meta-analysis. Int J Cancer. 2021;148(2):363-74.
-
9Wei C, Liu Y, Li Y, Zhang Y, Zhong M, Meng X. Evaluation of the nutritional status in patients with COVID-19. J Clin Biochem Nutr. 2020;67(2):116-21.
-
10Wang R, He M, Yin W, Liao X, Wang B, Jin X, et al. The Prognostic Nutritional Index is associated with mortality of COVID-19 patients in Wuhan, China. J Clin Lab Anal. 2020;34(10):e23566.
-
11Haraj NE, El Aziz S, Chadli A, Dafir A, Mjabber A, Aissaoui O, et al. Nutritional status assessment in patients with Covid-19 after discharge from the intensive care unit. Clin Nutr ESPEN. 2021;41:423-8.
-
12Ali AM, Kunugi H. Approaches to Nutritional Screening in Patients with Coronavirus Disease 2019 (COVID-19). Int J Environ Res Public Health. 2021;18(5):2772. Review.
-
13Li T, Zhang Y, Gong C, Wang J, Liu B, Shi L, et al. Prevalence of malnutrition and analysis of related factors in elderly patients with COVID-19 in Wuhan, China. Eur J Clin Nutr. 2020;74(6):871-5.
-
14Silva DF, Lima SC, Sena-Evangelista KC, Marchioni DM, Cobucci RN, Andrade FB. Nutritional Risk Screening Tools for older adults with COVID-19: a systematic review. Nutrients. 2020;12(10):2956.
-
15Bedock D, Bel Lassen P, Mathian A, Moreau P, Couffignal J, Ciangura C, et al. Prevalence and severity of malnutrition in hospitalized COVID-19 patients. Clin Nutr ESPEN. 2020;40:214-9.
-
16Pironi L, Sasdelli AS, Ravaioli F, Baracco B, Battaiola C, Bocedi G, et al. Malnutrition and nutritional therapy in patients with SARS-CoV-2 disease. Clin Nutr. 2021;40(3):1330-7.
-
17Mechanick JI, Carbone S, Dickerson RN, Hernandez BJ, Hurt RT, Irving SY, Li DY, McCarthy MS, Mogensen KM, Gautier JB, Patel JJ, Prewitt TE, Rosenthal M, Warren M, Winkler MF, McKeever L; ASPEN COVID-19 Task Force on Nutrition Research. Clinical Nutrition Research and the COVID-19 Pandemic: a scoping review of the ASPEN COVID-19 Task Force on Nutrition Research. JPEN J Parenter Enteral Nutr. 2021;45(1):13-31. Review.
-
18Zhang P, He Z, Yu G, Peng D, Feng Y, Ling J, et al. The modified NUTRIC score can be used for nutritional risk assessment as well as prognosis prediction in critically ill COVID-19 patients. Clin Nutr. 2021;40(2):534-41.
-
19Allard L, Ouedraogo E, Molleville J, Bihan H, Giroux-Leprieur B, Sutton A, et al. Malnutrition: Percentage and association with prognosis in patients hospitalized for coronavirus disease 2019. Nutrients. 2020;12(12):3679.
-
20Liang J, Jin G, Liu T, Wen J, Li G, Chen L, et al. Clinical characteristics and risk factors for mortality in cancer patients with COVID-19. Front Med. 2021;15(2):264-74.
-
21Muscaritoli M, Lucia S, Farcomeni A, Lorusso V, Saracino V, Barone C, Plastino F, Gori S, Magarotto R, Carteni G, Chiurazzi B, Pavese I, Marchetti L, Zagonel V, Bergo E, Tonini G, Imperatori M, Iacono C, Maiorana L, Pinto C, Rubino D, Cavanna L, Di Cicilia R, Gamucci T, Quadrini S, Palazzo S, Minardi S, Merlano M, Colucci G, Marchetti P; PreMiO Study Group. Prevalence of malnutrition in patients at first medical oncology visit: the PreMiO study. Oncotarget. 2017;8(45):79884-96.
-
22D’Almeida CA, Peres WA, de Pinho NB, Martucci RB, Rodrigues VD, Ramalho A. Prevalence of malnutrition in older hospitalized cancer patients: a multicenter and multiregional study. J Nutr Health Aging. 2020;24(2):166-71.
-
23de Pinho NB, Martucci RB, Rodrigues VD, D’Almeida CA, Thuler LC, Saunders C, et al. High prevalence of malnutrition and nutrition impact symptoms in older patients with cancer: results of a Brazilian multicenter study. Cancer. 2020;126(1):156-64.
-
24Wiegert EV, de Oliveira LC, Calixto-Lima L, Mota E Silva Lopes MS, Peres WA. Cancer cachexia: Comparing diagnostic criteria in patients with incurable cancer. Nutrition. 2020;79-80:110945.
-
25Jager-Wittenaar H, Ottery FD. Assessing nutritional status in cancer: role of the Patient-Generated Subjective Global Assessment. Curr Opin Clin Nutr Metab Care. 2017;20(5):322-9. Review.
-
26Cederholm T, Jensen GL, Correia MI, Gonzalez MC, Fukushima R, Higashiguchi T, Baptista G, Barazzoni R, Blaauw R, Coats A, Crivelli A, Evans DC, Gramlich L, Fuchs-Tarlovsky V, Keller H, Llido L, Malone A, Mogensen KM, Morley JE, Muscaritoli M, Nyulasi I, Pirlich M, Pisprasert V, de van der Schueren MA, Siltharm S, Singer P, Tappenden K, Velasco N, Waitzberg D, Yamwong P, Yu J, Van Gossum A, Compher C; GLIM Core Leadership Committee; GLIM Working Group. GLIM criteria for the diagnosis of malnutrition - a consensus report from the global clinical nutrition community. Clin Nutr. 2019;38(1):1-9.
-
27Eastern Cooperative Oncology Group (ECOG-ACRIN). Cancer Research Group. ECOG Performance Status. Philadelphia (PA): ECOG-ACRIN; 2022 [cited 2021 Mar 13]. Available from: https://ecog-acrin.org/resources/ecog-performance-status
» https://ecog-acrin.org/resources/ecog-performance-status -
28Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol. 1982;5(6):649-55.
-
29Karnofsky DA, Burchenal JH. The clinical evaluation of chemotherapeutic agents in cancer. In: Mac Leod CM, editor. Evaluation of chemotherapeutic agents. New York: Columbia Univ Press; 1949. p.199-205.
-
30Ma C, Bandukwala S, Burman D, Bryson J, Seccareccia D, Banerjee S, et al. Interconversion of three measures of performance status: an empirical analysis. Eur J Cancer. 2010;46(18):3175-83.
-
31Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996;15(4):361-87. Review.
-
32Hosmer DW, Hosmer T, Le Cessie S, Lemeshow S. A comparison of goodness-of-fit tests for the logistic regression model. Stat Med. 1997;16(9):965-80. Review.
-
33Oliveira LC, Abreu GT, Lima LC, Aredes MA, Wiegert EV. Quality of life and its relation with nutritional status in patients with incurable cancer in palliative care. Support Care Cancer. 2020;28(10):4971-8.
-
34Fernandes GA, Feriani D, França e Silva IL, Mendonça e Silva DR, Arantes PE, Canteras JD, et al. Differences in mortality of cancer patients with COVID-19 in a Brazilian cancer center. Semin Oncol. 2021;48(2):171-80.
-
35Melo AC, Thuler LC, Silva JL, Albuquerque LZ, Pecego AC, Rodrigues LO, da Conceição MS, Garrido MM, Quintella Mendes GL, Mendes Pereira AC, Soares MA, Viola JP; Brazilian National Cancer Institute COVID-19 Task Force. Cancer inpatients with COVID-19: a report from the Brazilian National Cancer Institute. PLoS One. 2020;15(10):e0241261.
-
36Pérez Camargo DA, Vargas Gutiérrez G, Rivera Franco MM, Labana Ramírez A, Castro Herrera M, Urbalejo Ceniceros VI, et al. Nutritional status in patients with COVID-19 and cancer: the experience of the National Cancer Institute in Mexico. Nutr Hosp. 2021;38(6):1263-8.
-
37Zhao X, Li Y, Ge Y, Shi Y, Lv P, Zhang J, et al. Evaluation of nutrition risk and its association with mortality risk in severely and critically ill COVID-19 patients. JPEN J Parenter Enteral Nutr. 2021;45(1):32-42.
-
38Jang RW, Caraiscos VB, Swami N, Banerjee S, Mak E, Kaya E, et al. Simple prognostic model for patients with advanced cancer based on performance status. J Oncol Pract. 2014;10(5):e335-41.
-
39Rosa KS, Cypriano RP, Albuquerque NM, Oliveira LC. Predictive factors of death on hospitalization in patients with advanced cancer in palliative care. Am J Hosp Palliat Care. 2021;38(10):1189-94.
-
40Oliveira LC, da Costa Rosa KS, Borsatto AZ, Oliveira LA, Freitas R, Sampaio SG. Prognostic factors in patients with advanced cancer and COVID-19: a cohort from the Palliative Care Unit of the Brazilian National Cancer Institute. Support Care Cancer. 2021;29(10):6005-12.
-
41Baba M, Maeda I, Morita T, Inoue S, Ikenaga M, Matsumoto Y, et al. Survival prediction for advanced cancer patients in the real world: a comparison of the Palliative Prognostic Score, Delirium-Palliative Prognostic Score, Palliative Prognostic Index and modified Prognosis in Palliative Care Study predictor model. Eur J Cancer. 2015;51(12):1618-29.
-
42Morabito F, Tripepi G, Vigna E, Bossio S, D’Arrigo G, Martino EA, et al. Validation of the Alternative International Prognostic Score-E (AIPS-E): Analysis of binet stage A chronic lymphocytic leukemia patients enrolled into the O-CLL1-GISL protocol. Eur J Haematol. 2021;106(6):831-5.
-
43Lin JX, Desiderio J, Lin JP, Wang W, Tu RH, Li P, et al. Multicenter Validation Study of the American Joint Commission on Cancer (8th Edition) for Gastric Cancer: Proposal for a Simplified and Improved TNM Staging System. J Cancer. 2020;11(12):3483-91.
-
44Briguglio M, Pregliasco FE, Lombardi G, Perazzo P, Banfi G. The malnutritional status of the host as a virulence factor for new coronavirus SARS-CoV-2. Front Med (Lausanne). 2020;7:146.
-
45Barazzoni R, Bischoff SC, Breda J, Wickramasinghe K, Krznaric Z, Nitzan D, Pirlich M, Singer P; endorsed by the ESPEN Council. ESPEN expert statements and practical guidance for nutritional management of individuals with SARS-CoV-2 infection. Clin Nutr. 2020;39(6):1631-8.
-
46Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol. 2011;12(5):489-95. Review.
-
47Tu H, Tu S, Gao S, Shao A, Sheng J. Current epidemiological and clinical features of COVID-19; a global perspective from China. J Infect. 2020;81(1):1-9. Review.
-
48Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497-506. Erratum in: Lancet. 2020 Jan 30.
-
49Brugliera L, Spina A, Castellazzi P, Cimino P, Arcuri P, Negro A, et al. Nutritional management of COVID-19 patients in a rehabilitation unit. Eur J Clin Nutr. 2020;74(6):860-3. Review.
-
50Brasil. Ministério da Saúde. Instituro Nacional de Câncer José Alencar Gomes da Silva (INCA). Consenso Nacional de Nutrição Oncológica. 2a ed. Rio de Janeiro (RJ): INCA; 2015 [citado 2022 Set 19]. Disponível em: https://www.inca.gov.br/sites/ufu.sti.inca.local/files//media/document//consenso-nacional-de-nutricao-oncologica-2-edicao-2015.pdf
» https://www.inca.gov.br/sites/ufu.sti.inca.local/files//media/document//consenso-nacional-de-nutricao-oncologica-2-edicao-2015.pdf -
51Lobascio F, Caccialanza R, Monaco T, Cereda E, Secondino S, Masi S, et al. Providing nutritional care to cancer patients during the COVID-19 pandemic: an Italian perspective. Support Care Cancer. 2020;28(9):3987-9.
-
52Caccialanza R, Laviano A, Lobascio F, Montagna E, Bruno R, Ludovisi S, et al. Early nutritional supplementation in non-critically ill patients hospitalized for the 2019 novel coronavirus disease (COVID-19): rationale and feasibility of a shared pragmatic protocol. Nutrition. 2020;74:110835.
-
53Yárnoz-Esquíroz P, Chopitea A, Olazarán L, Aguas-Ayesa M, Silva C, Vilalta-Lacarra A, et al. Impact on the Nutritional Status and Inflammation of Patients with Cancer Hospitalized after the SARS-CoV-2 Lockdown. Nutrients. 2022;14(13):2754.
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In BriefWe conducted a retrospective observational cohort study among cancer patients hospitalized for COVID-19 between March 2020 and February 2021 to verify whether the presence of nutritional risk indicators prior to COVID-19 diagnosis is associated with poor survival in these patient
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Highlights• Patients at nutritional risk had a lower survival than those not at nutritional risk.• Nutritional risk had good discriminatory accuracy to predict death.• Nutritional screening should be included as an essential part of care for these patients.
Publication Dates
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Publication in this collection
20 Mar 2023 -
Date of issue
2023
History
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Received
13 May 2022 -
Accepted
30 Aug 2022