Prognostic factors in critically ill cancer patients admitted to the intensive care unit

Journal of Critical Care xxx (2014) xxx–xxx

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Journal of Critical Care

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Prognostic factors in critically ill cancer patients admitted to the intensivecare unit

Gulbin Aygencel, MD a,⁎, Melda Turkoglu, MD a, Gulsan Turkoz Sucak, MD b, Mustafa Benekli, MD c

a Gazi University Faculty of Medicine, Department of Internal Medicine, Division of Critical Care Medicine, Ankara, Turkeyb Gazi University Faculty of Medicine, Department of Internal Medicine, Division of Hematology, Ankara, Turkeyc Gazi University Faculty of Medicine, Department of Internal Medicine, Division of Medical Oncology, Ankara, Turkey

a b s t r a c ta r t i c l e i n f o

⁎ Corresponding author at: Gazi University FacultyInternal Medicine, Division of Critical Care Medicine, BeTel.: +90 312 2024216.

E-mail addresses: [email protected] (G. [email protected] (M. Turkoglu), aysucak@[email protected] (M. Benekli).

0883-9441/$ – see front matter © 2014 Elsevier Inc. Alhttp://dx.doi.org/10.1016/j.jcrc.2014.01.014

Please cite this article as: Aygencel G, et al(2014), http://dx.doi.org/10.1016/j.jcrc.201

Keywords:
ICU mortalityprognostic factorcancer patient
Objective: The objective of this study is to identify factors predicting intensive care unit (ICU) mortality incancer patients admitted to a medical ICU.Patients and methods:We conducted a retrospective study in 162 consecutive cancer patients admitted to themedical ICU of a 1000-bed university hospital between January 2009 and June 2012. Medical history, physical
and laboratory findings on admission, and therapeutic interventions during ICU staywere recorded. The studyend point was ICU mortality. Logistic regression analysis was performed to identify independent risk factorsfor ICU mortality.Results: The study cohort consisted of 104 (64.2%) patients with solid tumors and 58 patients (35.8%) withhematological malignancies. The major causes of ICU admission were sepsis/septic shock (66.7%) andrespiratory failure (63.6%), respectively. Overall ICU mortality rate was 55 % (n= 89). The ICU mortality rateswere similar in patients with hematological malignancies and solid tumors (57% vs 53.8%; P = .744). Fourvariables were independent predictors for ICU mortality in cancer patients: the remission status of theunderlying cancer on ICU admission (odds ratio [OR], 0.113; 95% confidence interval [CI], 0.027-0.48; P =.003), Acute Physiology and Chronic Health Evaluation II score (OR, 1.12; 95% CI, 1.032-1.215; P = .007),sepsis/septic shock during ICU stay (OR, 8.94; 95% CI, 2.28-35; P = .002), and vasopressor requirement (OR16.84; 95% CI, 3.98-71.24; P= .0001). Although Acute Physiology and Chronic Health Evaluation II score (OR,1.30; 95% CI, 1.054-1.61; P = .014), admission through emergency service (OR, 0.005; 95% CI, 0.00-0.69; P =.035), and vasopressor requirement during ICU stay (OR, 140.64; 95% CI, 3.59-5505.5; P = .008) wereindependent predictors for ICU mortality in patients with hematological malignancies, Sequential OrganFailure Assessment score (OR, 1.83; 95% CI, 1.29-2.6; P= .001), lactate dehydrogenase level on admission (OR,1.002; 95% CI, 1-1.005; P = .028), sepsis/septic shock during ICU stay (OR, 138.4; 95% CI, 12.54-1528.4; P =.0001), and complete or partial remission of the underlying cancer (OR, 0.026; 95% CI, 0.002-0.3; P = .004)were the independent risk factors in patients with solid tumors.Conclusion: Intensive care unit mortality rate was 55% in our cancer patients, which suggests that patientswith cancer can benefit from ICU admission. We also found that ICU mortality rates of patients withhematological malignancies and solid tumors were similar.
© 2014 Elsevier Inc. All rights reserved.

1. Introduction

The growing number of patients living with cancer leads to asimilar increase in the number of patients requiring intensive care.Despite the general opinion that admission of cancer patients tointensive care units (ICUs) is usually futile and costly based on someolder studies, ICU survival has been reported to be improved

of Medicine, Department ofsevler, 06510, Ankara, Turkey.

el),azi.edu.tr (G. Turkoz Sucak),

l rights reserved.

, Prognostic factors in critica4.01.014

significantly in recent studies [1–4]. Increased survival expectancyin critically ill cancer patients led conduction of studies thatinvestigate the prognostic factors that predict ICU outcome andguide ICU admission andmanagement strategies [1–8]. We, therefore,analyzed our data retrospectively to determine the characteristics andoutcomes of cancer patients admitted to our medical ICU and toidentify the risk factors associated with ICU mortality.

2. Patients and methods

2.1. Study design

This study is a retrospective, observational study conducted in the 9-bed medical ICU of the Gazi University Hospital, a 1000-bed university

lly ill cancer patients admitted to the intensive care unit, J Crit Care

http://dx.doi.org/10.1016/j.jcrc.2014.01.014

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2 G. Aygencel et al. / Journal of Critical Care xxx (2014) xxx–xxx

hospital in Ankara, Turkey. Every adult patient (≥18 years old) withhistologically proven cancerwho required ICU admissionwas evaluatedbetween January 1, 2009, and June 30, 2012. When ICU admission isconsidered in a cancer patient in our center, life expectancy should belonger than 3 months, and/or further treatment options to treat theunderlying cancer should be available. Only the first admission wasrecorded in patients withmultiple ICU admissions. Patients who stayedin the ICU for shorter than 24 hours were also excluded. This study wasapproved by the institutional review board.

A total of 162 consecutive cancer patients admitted to ICU during thestudy period were included in the study. The following information wasabstracted from the medical charts of the patients: age and sex;comorbidities; type of cancer; characteristics of the cancer includingpresence of metastases; current status of the underlying cancer (completeorpartial remission, relapsed, or progressive1 disease); treatmentmodalitythat includes surgery, chemotherapy, and radiation therapy; the patient'spreadmission performance status as determined by Eastern CooperativeOncology Group (ECOG2) scale; hematopoietic stem cell transplantation(HSCT) status and type of HSCT (autologous and allogeneic); cause of ICUadmission; source of admission (internal medicine, emergency service,etc); time fromhospital to ICU admission; blood chemistries and completeblood count on day 1; presence and site of infection on admission andduring ICU stay; severity of illness score using Acute Physiology andChronic Health Evaluation (APACHE) II score; organ dysfunctions usingSequential Organ Failure Assessment (SOFA) score; therapeutic interven-tions during the ICU stay (use of vasopressors, mechanical ventilation,dialysis, chemotherapy), length of ICU stay; and ICU mortality rate.

2.2. Statistical analysis

Data were analyzed using SPSS 13.5 for Windows (SPSS, Inc, Chicago,IL). Descriptive statistics were computed for all study variables. AKolmogorov-Smirnov testwas used, and histograms andnormal-quantileplots were examined to verify the normality of distribution of continuousvariables. Discrete variables are expressed as counts (percentage), andcontinuous variables, asmeans±SDormedian (interquartile range, 25%-75%). For demographics and clinical characteristics of the study groups,differences between groups were assessed using a χ2, Fisher exact test,Student t test, or Mann-Whitney U test, as appropriate. Multivariatelogistic regression analysis with ICU mortality as the dependent variablewas conducted in cancer patients. Only variables associatedwith a higherrisk of ICUmortality (P b .05) on a univariate basis were introduced in themultivariate model. P b .05 was considered statistically significant.

3. Results

3.1. Results in the whole study cohort

There were 1130 admissions during the study period, amongwhom 162 (14.3%) were cancer patients who met the eligibilitycriteria of the study. Median age was 61 (48-71.3) years, and mostpatients were male (58.6%). The most common causes of ICU

1 Cancer recurrence or relapse is defined as the return of cancer after treatment andafter a period during which the cancer cannot be detected. When cancer spreads orgets worse, it is called progression. When a treatment completely eliminates the tumorand the tumor cannot be seen on the tests or cannot be measured after a period, it iscalled a complete response or complete remission. A partial response or partialremission means the cancer partly responded to treatment. Treatment partly controlsthe tumor and reduces the tumor size.

2 Eastern Cooperative Oncology Group scale is used to assess how the disease affectsthe daily living abilities of the patient. They included the following: 0, fully active, ableto carry on all predisease performance without restriction; 1, restricted in physicallystrenuous activity but ambulatory and able to carry out work of a light or sedanterynature, for example, light house work, office work; 2, ambulatory and capable of allself-care but unable to carry out any work activities; 3, capable of only limited self-care, confined to bed or chair more than 50% of waking hours; and 4, completelydisabled, cannot carry on any self-care, totally confined to bed or chair.

Please cite this article as: Aygencel G, et al, Prognostic factors in critical(2014), http://dx.doi.org/10.1016/j.jcrc.2014.01.014

admission were sepsis/septic shock (66.7%) and respiratory failure(63.6%). The most common comorbidities of the patients werecardiovascular diseases, diabetes, and hypertension. Most patientswere admitted to our medical ICU from emergency service. Two ormore organ dysfunctions were found in 84 patients (52%) onadmission. Renal and pulmonary dysfunctions were the mostcommon organ dysfunctions. Most patients had thrombocytopenia(53.7%), whereas 46 patients had neutropenia. Sixty-eight patientsrequired mechanical ventilation on admission. A possibility of aninfectious etiology or isolation of a microorganism was seen in 147patients on ICU admission.

Fifty-eight patients (35.8%) in our cohort had hematologicalmalignancies, and 104 patients (64.2%) had solid tumors. Lymphomawas the most common solid tumor, whereas acute leukemia was themost common hematological malignancy. Colon, lung, and breastcancers were the other common solid tumors in our cohort (all typesof cancer in our study group are presented in Table 1). Fifty-fivepatients had relapsed or progressive cancer, whereas 54 patients werenewly diagnosed cancer patients. Performance status of the cancerpatients was well (ECOG, 0-2) in 117 patients according to ECOGperformance scale on ICU admission. One hundred fifteen patientshad been treated with chemotherapy, and 84 patients had cancertherapywithin amonth before ICU admission. Eighteen of the patientswere stem cell transplant recipients.

Renal replacement therapy was required in 53 patients (32.7%)during ICU stay. Mechanical ventilation (invasive or noninvasive) wasapplied to 109 patients. Intensive care unit–acquired nosocomialinfection was detected in 62 patients (38.3%). Of the cancer patients,73 (45%) survived, and 89 cancer patients (55%) died at the end oftheir ICU stay. Table 1 shows some baseline characteristics of thestudy population.

3.2. Results in hematological malignancies and solid tumors groups

Patients are categorized into 2 groups in terms of their type of cancer(patients with hematological malignancies and patients with solidtumors). Patients with solid tumors were older than the patients withhematological malignancies. Sequential Organ Failure Assessment scoreswere significantly higher in patients with hematological malignanciesthan in thosewith solid tumors. Patientswithhematologicalmalignancieshad longer duration of hospital stay before ICU admission. Comorbiditiesvaried among the groups, with a higher prevalence in patients with solidtumors. Anticancer treatment within a month before ICU admission wasmore common in patients with hematological malignancies. Thefrequency of infection on ICU admission was also more common inpatients with hematological malignancies. Episodes of bacteremia weremore frequent in patients with hematological malignancies comparedwith patients with solid tumors. The number of organ failure and renaldysfunction was more common in patients with hematological malig-nancies during ICU stay. Although neutropenia on and during admissionto ICU and thrombocytopenia were more common in patients withhematological malignancies, ICU mortality rate was similar in patientswith hematological malignancies and solid tumors. Table 1 shows somecharacteristics of the patients with hematological malignancies and solidtumors in our ICU.

3.3. Results in survivors and nonsurvivors

We subcategorized our cohort according to their outcome andreanalyzed: patients who survived (survivor—discharge or transfer)(73 patients, 45%) and who died (nonsurvivors) (89 patients, 55%).Acute Physiology and Chronic Health Evaluation II and SOFA scoreswere significantly lower, Glasgow Coma Scale (GCS) was significantlyhigher, and length of ICU stay and length of hospital stay before ICUadmission were significantly shorter in survivors when comparedwith nonsurvivors. Nonsurvivors had more progressive and relapsed

ly ill cancer patients admitted to the intensive care unit, J Crit Care


Table 1Some baseline characteristics of cancer patients in our ICU

Variable Cancer patients inICU (n = 162)

Patients with hematologicalmalignancies (n = 58)

Patients with solidtumors (n = 104)

P

Age (y) 61 (48-71.3) 52.5 (33-61.25) 66.5 (33-61.25) .0001Male sex 95 (59%) 40 (69%) 55 (53%) .067Length of hospital stay before ICU admission (d) 4 (1-16) 7 (1.75-26.25) 2 (1-11) .001Length of ICU stay (d) 5 (3-12) 4 (3-9.25) 5(3-14) .56Types of cancerSolid tumors 104 (64%)Non-Hodgkin lymphoma 26 (16%)Colon cancer 19 (12%)Breast cancer 12 (7%)Prostate cancer 8 (5%)Lung cancer 7 (4%)Urinary bladder cancer 7 (4%)Gynecologic cancers 6 (4%)Other solid tumorsa 19 (12%)Hematological malignancies 58 (36%)Acute myeloid leukemia 27 (16.7%)Multiple myeloma 13 (8%)Acute lymphoblastic leukemia 8 (5%)Chronic lymphocytic leukemia 6 (4%)Chronic myelogenous leukemia 4 (2%)

Characteristics of the cancer on ICU admissionNewly diagnosed 54 (33%) 21 (36%) 33 (32%) .604Complete or partial remission 37 (23%) 10 (17%) 27 (26%) .244Relapsed or progressive disease 55 (34%) 25 (43%) 30 (29%) .084End stage 16 (10%) 2 (3%) 14 (13%) .053

Patient's preadmissionperformance statusGood (ECOG 0-2) 117 (72.2%) 39 (67%) 78 (75%) .36Poor (ECOG 3 and 4) 45 (27.8%) 19 (33%) 26 (25%)

Cancer treatment statusChemotherapy 115 (71%) 45 (78%) 70 (67%) .207Radiation therapy 41 (25%) 7 (12%) 34 (33%) .004Surgery 44 (27%)Cancer therapy within the last month before ICU admission 84 (52%) 39 (67%) 45 (43%) .005

BMT recipient 18 (11%) 14 (24%) 4 (4%) .0001Allogeneic BMT 16 (10%) 12 (21%) 4 (4%) .001

ComorbiditiesChronic obstructive pulmonary disease 17 (10%) 2 (3%) 15 (14%) .033Diabetes mellitus 33 (20%) 4 (7%) 29 (28%) .001Hypertension 36 (22%) 4 (7%) 32 (31%) .0001Cardiovascular diseases 24 (15%) 5 (9%) 19 (18%) .11

Cause of ICU admissionSepsis/septic shock 108 (67%) 42 (72%) 66 (63%) .298Respiratory failure 103 (64%) 40 (69%) 63 (61%) .311Acute renal failure 51 (31%) 16 (28%) 35 (34%) .483

Source of admissionEmergency service 55 (34%) 9 (16%) 46 (44%) .0001

Morbidities on ICU admissionRenal dysfunction 75 (46%) 24 (41%) 51 (49%) .412Neutropenia 46 (28%) 37 (64%) 9 (9%) .0001Thrombocytopenia 87 (54%) 48 (83%) 39 (38%) .0001Requirement of mechanical ventilation (invasive or noninvasive) 68 (42%) 29 (50%) 39 (38%) .137Hepatic dysfunction 56 (35%) 17 (29%) 39 (38%) .308Vasopressors requirement 54 (33%) 23 (40%) 31 (30%) .226≥2 organ dysfunctions 84 (52%) 41 (71%) 43 (41%) .001Suspected or culture-proven infection 147 (91%) 55 (95%) 92 (88%) .26Bacterial infection 69 (43%) 32 (55%) 37 (36%) .02Fungal infection 21 (13%) 13 (22%) 8 (8%) .013Pulmonary infection 102 (63%) 39 (67%) 63 (61%) .498Bloodstream infection 28 (17%) 17 (29%) 11 (11%) .004On ICU admissionAPACHE II score 23 (18-29) 24 (18-32.5) 22 (17-28) .217GCS 14 (10-15) 14 (10-15) 14 (10-15) .6SOFA score 8 (5-10) 9 (6.25-12) 7 (4-10) .003Hemoglobin level (g/dL) 9.1 (8-10.6) 8.2 (6.8-9.45) 9.7 (8.5-11.2) .0001Leukocytes (/mm3) 8870 (3150-15950) 4300 (890-18800) 10180 (5400-15350) .014Thrombocytes (/mm3) 91000 (36000-192000) 43000 (21050-83800) 146500 (66750-232250) .0001Sodium (Na, mEq/L) 136 (135-140) 136 (133.5-140) 136 (132-141) .55ALT (IU/L) 21 (12-39.8) 16 (12-26) 26 (13-46) .01LDH (IU/L) 348 (246.5-779.25) 345 (239-830) 349 (246-697) .66C-reactive protein (mg/L) 149 (76.5-248.5) 180 (102.7-318) 133 (63.8-208) .035Procalcitonin (ng/mL) 2.3 (0.65-20) 5 (0.9-31) 1.9 (0.39-10.92) .048Calcium (mg/dL) 7.7 (7.1-8.3) 7.4 (6.8-7.85) 7.95 (7.32-8.5) .0001Albumin (g/dL) 2.6 (2.2-2.9) 2.5 (2.2-2.9) 2.6 (2.2-2.9) .54

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Please cite this article as: Aygencel G, et al, Prognostic factors in critically ill cancer patients admitted to the intensive care unit, J Crit Care(2014), http://dx.doi.org/10.1016/j.jcrc.2014.01.014


Table 1 (continued)

Variable Cancer patients inICU (n = 162)

Patients with hematologicalmalignancies (n = 58)

Patients with solidtumors (n = 104)

P

Creatinine (mg/dL) 1.1 (0.7-2.1) 0.9 (0.6-1.95) 1.2 (0.7-2.27) .087Glucose (mg/dL) 138 (120-185) 139 (119-181 135.5 (120.3-200.8) .82Morbidities during ICU staySepsis/septic shock 73 (45%) 26 (45%) 47 (45%) 1Neutropenia 27 (17%) 21 (36%) 6 (6%) .0001Hepatic dysfunction 24 (15%) 12 (21%) 12 (12%) .165Renal dysfunction 48 (30%) 24 (41%) 24 (23%) .019Renal replacement therapy 53 (33%) 22 (38%) 31 (30%) .3Requirement of mechanical ventilation 109 (67%) 42 (72%) 67 (64%) .383Chemotherapy in ICU 10 (6%) 10 (17%) 0 (0%) .0001Blood/blood products transfusion 96 (59%) 47 (81%) 49 (47%) .0001Central venous catheterization 88 (54%) 31 (53%) 57 (55%) .871Arterial catheterization 125 (77%) 49 (84%) 76 (73%) .119Suspected or culture-proven infection 62 (38%) 25 (43%) 37 (36%) .4Bacterial infection 57 (35%) 24 (41%) 33 (32%) .234Pulmonary infection 56 (35%) 21 (36%) 35 (34%) .863Steroid use 119 (73%) 47 (81%) 72 (69%) .137Vasopressor use 99 (61%) 37 (64%) 62 (60%) .619ResultsSurvived 73 (45%) 25 (43%) 48 (46%)Died 89 (55%) 33 (57%) 56 (54%) .744

Values are presented as median (interquartile range) or n (%). BMT indicates bone marrow transplantation; ALT, alanine aminotransferase.a Other solid tumors: renal cell cancer, nasopharyngeal cancer, laryngeal cancer, hepatocellular carcinoma, esophageal cancer, and glial brain tumors.


cancer and worse performance status. Respiratory failure and sepsis/septic shock on admission were significantly more common innonsurvivors. Being thrombocytopenic, on mechanical ventilation,having infection were significantly more frequent in nonsurvivors.Platelet count was found to be significantly higher in survivors. Someinflammatory markers such as procalcitonin and C-reactive proteinwere lower in survivors. Nosocomial infections and acute renal failurewere significantly more common, and renal replacement therapy wasrequired more often in nonsurvivors during ICU stay. Requirement forinvasive monitoring and administration of steroids was significantlymore frequent during ICU stay in the nonsurvivor group. Requirementfor tracheostomy and blood/blood product transfusion was alsosignificantly more common in nonsurvivors. Table 2 shows somecharacteristics of the survivor and nonsurvivor cancer patients in ICU.

3.4. Results of multivariate analysis in our study group

Length of hospital stay before ICU admission, length of ICU stay,status of the underlying cancer, performance status, causes of ICUadmission, source of ICU admission, some comorbidities and infectionson ICU admission, APACHE II score, GCS, SOFA score, some laboratoryabnormalities (inflammatory markers, in particular), and some mor-bidities during ICU stay (septic shock, renal replacement therapy,requirementof vasopressors and steroid, etc) are the variables thatwerefound to be significantly associated with increased ICU mortality incancer patients in univariate analysis. However, only 3 parameters,namely, APACHE II score on admission (odds ratio [OR], 1.12; 95%confidence interval [CI], 1.032-1.215; P=.007), sepsis/septic shock (OR,8.94, 95% CI: 2.283-35.002; P= .002), and requirement of vasopressorsduring ICU stay (OR, 16.839; 95% CI, 3.98-71.235; P = .0001), wereindependently associatedwithhigher ICUmortality. Complete or partialremission of the underlying cancer on admission to ICU was the onlyprotective factor, with a markedly decreased risk of death (OR, 0.113;95% CI, 0.027-0.483; P = .003) (Table 4).

3.5. Results of multivariate analysis in our study subgroups

We also evaluated dependent and independent risk factorsassociated with ICU mortality in patients with hematologicalmalignancies and patients with solid tumors separately. Univariateanalysis revealed that length of hospital stay before ICU, length of ICU


stay, status of the underlying disease, performance status, source ofICU admission, some morbidities and infections on ICU admission,APACHE II score, GCS, SOFA score, and some morbidities during ICUstay (septic shock, renal replacement therapy, requirement ofvasopressors and steroid, etc) were significantly associated with ICUmortality in patients with hematological malignancies (Table 3). Only2 parameters, namely, APACHE II score on admission (OR, 1.303; 95%CI, 1.054-1.609; P = .014) and requirement of vasopressors duringICU stay (OR, 140.635; 95% CI, 3.592-5505.482; P = .008), wereindependently associated with higher ICU mortality in multivariateanalysis. Admission from emergency service was the only protectivefactor, with a markedly decreased risk of death (OR, 0.005; 95% CI,0.000-0.691; P = .035) (Table 4).

Length of hospital stay before ICU admission, length of ICU stay,cancer status, some morbidities and infections on ICU admission,some laboratory abnormalities (lactate dehydrogenase [LDH], inflam-matory markers, etc), APACHE II score, GCS, SOFA score, and somemorbidities during ICU stay (septic shock, mechanical ventilation,nosocomial infections, blood/blood product transfusion, requirementof vasopressor and steroid, etc) were significantly associated with ICUmortality in patients with solid tumors in univariate analysis(Table 3). Only 3 parameters, namely, SOFA score (OR, 1.831; 95%CI, 1.289-2.601; P= .001), LDH level on admission (OR, 1.002; 95% CI,1-1.005; P = .028), and sepsis/septic shock during ICU stay (OR,138.406; 95% CI, 12.534-1528.4; P = .0001), were independentlyassociated with higher ICU mortality in multivariate analysis;complete or partial remission of the underlying cancer on ICUadmission was the only protective factor, with a markedly decreasedrisk of death (OR, 0.026; 95% CI, 0.002-0.304; P = .004) (Table 4).

Our results indicate that the severity of critical illness (APACHE IIscore), presence of organ dysfunctions (SOFA score), development ofsome morbidities during ICU stay (sepsis/septic shock in particular),and the status of the underlying cancer (limited or progressive)predicted the ICU mortality in our cancer patients.

5. Discussion

There is growing number of ICU admissions of cancer patients inparallel to the increase in patients living with cancer. Patients withcancer are more severely ill than the patients without cancer,resulting in higher ICU and hospital mortality rates. Similarly, our



Table 2Some characteristics of the survivor and nonsurvivor cancer patients in our ICU

Variable Survivor (n = 73) Nonsurvivor (n = 89) P

Age (y) 62 (49-70) 61 (47.5-72) .814Male sex 44 (60%) 51 (57%) .75Length of hospital stay before ICU admission (d) 2 (1-6) 8 (2-22.5) .0001Length of ICU stay (d) 4 (3-6) 7 (3-16) .002Characteristics of the cancer on ICU admissionNewly diagnosed 24 (33%) 30 (34%) 1Complete or partial remission 27 (37%) 10 (11%) .0001Relapsed or progressive disease 16 (22%) 39 (44%) .004End stage 6 (8%) 10 (11%) .603

Patient's preadmission performance statusGood (ECOG 0-2) 59 (81%) 58 (65%)Poor (ECOG 3 and 4) 14 (19%) 31 (35%) .034

Cancer treatment statusChemotherapy 49 (67%) 66 (74%) .385Radiation therapy 19 (26%) 22 (25%) .858Cancer therapy within the last month before ICU admission 33 (45%) 51 (57%) .155

BMT recipient 7 (10%) 11 (12%) .624Allogeneic BMT 6 (8%) 10 (11%) .603

ComorbiditiesChronic obstructive pulmonary disease 7 (10%) 10 (11%) .801Diabetes mellitus 17 (23%) 16 (18%) .437Hypertension 20 (27%) 16 (18%) .185Cardiovascular diseases 9 (12%) 15 (17%) .508

Cause of ICU admissionSepsis/septic shock 40 (55%) 68 (76%) .004Acute respiratory failure 39 (53%) 64 (72%) .021Acute renal failure 19 (26%) 32 (36%) .234

Source of admissionEmergency service 34 (47%) 21 (24%) .003

Morbidities on ICU admissionSepsis/septic shock 37 (51%) 58 (65%) .078Renal dysfunction 32 (44%) 43 (48%) .636Neutropenia 17 (23%) 29 (33%) .22Thrombocytopenia 29 (40%) 58 (65%) .002Requirement of mechanical ventilation (IMV or NIMV) 21 (29%) 47 (53%) .002Hepatic dysfunction 22 (30%) 34 (38%) .321Requirement of vasopressors treatment 19 (26%) 35 (39%) .094≥2 organ dysfunctions 24 (33%) 60 (67%) .0001Suspected or culture-proven infection 61 (84%) 86 (97%) .006Bacterial infection 21 (29%) 48 (54%) .001Fungal infection 4 (5%) 17 (19%) .01Pulmonary infection 41 (56%) 61 (69%) .141Bloodstream infection 7 (10%) 21 (24%) .022Urinary tract infection 10 (14%) 27 (30%) .014On ICU admissionAPACHE II score 18 (14-22.5) 27.5 (22-34) .0001GCS 15 (14-15) 12.5 (7-15) .0001SOFA score 6 (3-8) 9 (7-13) .0001Hemoglobin level (g/dL) 9.3 (8.05-11.05) 9.1 (8-10) .239Leukocytes (/mm3) 9140 (5275-14100) 7800 (2310-16775) .268Thrombocytes (/mm3) 130000 (59600-225500) 66000 (29950-160750) .001Sodium (Na, mEq/L) 136 (132-140) 137 (134-142) .036AST (IU/L) 26 (17.3-45) 35 (22.3-75) .035LDH (IU/L) 312 (210.5-507) 475 (268-909) .007C-reactive protein 121.5 (51-218) 168 (109-284) .026Procalcitonin 1.45 (0.28-4.9) 4.5 (1-26) .003Calcium (mg/dL) 8 (7.25-8.5) 7.7 (6.9-8.1) .03Total protein (g/dL) 5.5 (4.8-6) 5.1 (4.4-5.8) .029Albumin (g/dL) 2.7 (2.4-3) 2.4 (2.1-2.8) .003Creatinine (mg/dL) 1 (0.7-1.9) 1.15 (0.7-2.48) .611Glucose (mg/dL) 135 (118.3-172) 138 (123-201) .423

Morbidities during ICU staySepsis/septic shock 7 (10%) 66 (74%) .0001Neutropenia 6 (8%) 21 (24%) .011Hepatic dysfunction 1 (1%) 23 (26%) .0001Renal dysfunction 5 (7%) 43 (48%) .0001Renal replacement therapy 13 (18%) 40 (45%) .0001Requirement of mechanical ventilation (IMV or NIMV) 34 (47%) 75 (84%) .0001Chemotherapy in ICU 4 (5%) 6 (7%) 1Blood/blood product transfusion 29 (40%) 67 (75%) .0001Central venous catheterization 19 (26%) 69 (78%) .0001Arterial catheterization 44 (60%) 81 (91%) .0001Tracheostomy 1 (1%) 17 (19%) .0001Suspected or culture-proven infection 12 (16%) 50 (56%) .0001





Table 2 (continued)

Variable Survivor (n = 73) Nonsurvivor (n = 89) P

Bacterial infection 10 (14%) 47 (53%) .0001Fungal infection 2 (3%) 18 (20%) .001Pulmonary infection 11 (15%) 45 (51%) .0001Urinary tract infect 3 (4%) 18 (20%) .002Bloodstream infection 1 (1%) 19 (21%) .0001Steroid use 38 (52%) 81 (91%) .0001Vasopressor use 15 (21%) 84 (94%) .0001Types of cancerSolid tumors 48 (66%) 56 (63%)Hematological malignancies 25 (34%) 33 (37%)

Values are presented as median (interquartile range) or n (%). IMV indicates invasive mechanical ventilation; NIMV, noninvasive mechanical ventilation.


ICU mortality rate in cancer patients was 55% and higher than theoverall mortality of 32%. Previous studies have reported ICU mortalitybetween 10% and 70% in cancer patients. This large interstudyvariation in the mortality rates might be explained by the variationin the composition of underlying disease, admission and dischargecriteria, treatment decisions, and the implementation of end-of-lifedecisions [1–8]. The poor prognosis of patients with hematologicalmalignancies who require ICU admission has been well documented,with ICU mortality rates up to 60%, increasing up to 80% whenmechanical ventilation is required [9,10], whereas surgical admissionis reported to be associated with better outcome in patients with solidtumors [1,11]. Although some studies claim higher ICU mortality ratein hematological malignancies [9,10,12], we did not confirm thisresult in our study. Intensive care unit mortality rates were similar inpatients with solid tumors and hematological malignancies (53.8% vs57%; P = .744), which might be explained by some features of thepresented cohort. First of all, lymphomas were categorized within thesolid tumors. Colon and breast cancers, which have a relatively betterprognosis, consisted themajority of solid tumor group. Mortality ratescould have been different when the lymphomas are removed fromthis subcategory. Another explanation is the high rate of patients withadvanced cancer, with the rate of 43% in the solid tumor group, whichmight have caused overestimation of the mortality rate in this groupof patients. Site and number of metastases, which have a significantimpact onmortality in advanced cancer patients, were not recorded inour cohort and might be a limitation of the current study.

Intensive caremortality couldbe significantly improved in critically illcancer patients with rational patient selection during admission. As ageneral rule, patientswith goodperformance status,whoare at the initialphase of their malignant disease with available life-extending treatmentoptions, should routinely be admitted to the ICU. Reliable objectivecriteria in cancer patients that can be assessed rapidly at the bedside todecide ICU admission are often lacking. In most of the studies, classiccriteria such as the characteristics of the underlying malignancy are nolonger reliable for assessingpotential benefits of ICUadmission [1–8]. Theclinical judgment of physicians is inaccurate in up to 25% of casesaccording to a previous French study [13]. Severity of the acute illness onICU admission is the main determinant of short-term mortality innoncancer critically ill patients. Severity scores and organ failure scorescanbeuseful inpredicting the outcomeof cancerpatients admitted to theICU and thus help the medical decision making [14–17]. We demon-strated that one of the severity scores (APACHE II) in all cancer patientcohort and organ failure score (SOFA) in patients with solid tumorswereindependent risk factors for ICU mortality. Some studies in cancerpatients have shownseverity andorgan failure scores (suchasAPACHE II,Simplified Acute Physiology Score II, SOFA, etc) on admission to be avaluable prognostic factor for ICUmortality, whereas some other studieshave not [14–17]. Some studies have reported that daily assessments oforgan failures and the courseof theorgan failurewith timeduring the ICUstay showed good discrimination in cancer patients [14,16].

Up to 80% of cancer patients are admitted to the ICU because ofsepsis/septic shock or acute respiratory failure. In other words, severe


infections and organ failures are themain reasons for ICU admission incancer patients [3–5,8]. Similarly, sepsis/septic shock (67%) andrespiratory failure (64%) were the leading causes of ICU admission,whereas respiratory system (63%) was the leading site of infections inour study. Acute kidney injury is known to be among the frequentorgan failures on ICU admission and approximately one third ofcancer patients have acute kidney injury, half of whom require renalreplacement therapy [11,12,18,19]. Nevertheless, 31.5% of our cancerpatients were admitted to our ICU with acute renal failure, and 32.7%of them required renal replacement therapy during ICU stay.

The main objectives of the current study were to determine theoutcome of our cancer patients admitted to ICU over a 3.5-year periodand to identify factors influencing ICU mortality. The ICU mortalityrate was 55% and was negatively influenced by high APACHE II scoreon admission, vasopressor use, and development of septic shockduring ICU stay in multivariate analysis. We also confirmed thatpresence of organ failure on ICU admission predicts poor ICU outcomein patients with solid tumors.

Achievement of complete or partial remission had significantlybetter ICU outcome in our cohort. Although several previous studiesdeny that response to chemotherapy, stage of malignancy, and othercharacteristics of the cancer have little or no impact on short-termsurvival, some other reports, in accordance with ours, claim that somecharacteristics of the underlying cancer, such as its extent or phaseinfluenced the ICU mortality [4,6,9,20].

Some studies have reported that patient level of functioning beforethe admission to ICU influenced the ICU mortality and morbidities[3,5,20,21]. We confirmed these results in our study. Poor performancestatus predicted poor ICU outcome; however, this result was not anindependent risk factor for ICU mortality in multivariate analysis.

Different studies have showed various independent risk factors forICU mortality in cancer patients. Some of the previously defined riskfactors are older age, male sex, progressive underlying malignancy,respiratory insufficiency, high severity of illness scores (such asAPACHE II and III and Simplified Acute Physiology Score II), thenumber and the severity of organ failures (especially multiorganfailure), requirement for invasive mechanical ventilation, renaldysfunction and requirement of renal replacement therapy, hepaticdysfunction, neutropenia, allogenic HSCT, presence of graft-versus-host disease, sepsis on admission and during ICU stay, infections(especially invasive fungal infection or bacteremia), use of vasopres-sors, length of hospital stay before ICU admission, source of admission,performance status, administration of chemotherapy in ICU, and somelaboratory abnormalities (including anemia, thrombocytopenia, neu-tropenia, high bilirubin and creatinine levels, low albumin levels, etc)[1–29]. Several variables were shown to be related with ICU mortalityin univariate analysis of our data (length of hospital stay before ICUadmission, length of ICU stay, relapsed or progressive cancer,admitted with sepsis/septic shock, illness severity score and organfailure score, thrombocytopenia, some laboratory abnormalities inaspartate aminotransferase (AST), LDH, albumin, inflammatorymarkers, organ dysfunctions during ICU stay, infection during ICU



Table 3Some characteristics of the survivor and nonsurvivor hematological malignancies and solid tumors patients in our ICU

Variable Patients with hematological malignancies Patients with solid tumors

Survivor(n = 25)

Nonsurvivor(n = 33)

P Survivor(n = 48)

Nonsurvivor(n = 56)

P

Age (y) 53 (37.5-63.5) 52 (28-61) .55 64.5 (57-74.8) 66 (57-74.8) .904Male sex 20 (80%) 20 (61%) .155 24 (50%) 31 (55%) .694Length of hospital stay before ICU admission (d) 3 (1-9.5) 19 (5.5-30) .001 1.5 (0-4.8) 6 (1-16) .001Length of ICU stay (d) 3 (3-6) 7 (4-12) .027 4.5 (3-6) 7 (3-16.8) .025Characteristics of the cancer on ICU admissionNewly diagnosed 10 (40%) 11 (33%) .783 14 (29%) 19 (34%) .675Complete or partial remission 9 (36%) 1 (3%) .001 18 (38%) 9 (16%) .015Relapsed or progressive disease 4 (16%) 21 (64%) .0001 12 (25%) 18 (32%) .516End stage 2 (8%) 0 (0%) .063 4 (8%) 10 (18%) .249

Patient's preadmission performance statusGood (ECOG 0-2)Poor (ECOG 3 and 4) 4 (16%) 15 (45%) .024 10 (21%) 16 (29%) .496

Cancer treatment statusChemotherapy 20 (80%) 25 (76%) .76 29 (60%) 41 (73%) .209Radiation therapy 3 (12%) 4 (12%) .989 16 (33%) 18 (32%) 1Cancer therapy within the last monthbefore ICU admission

16 (64%) 23 (70%) .779 17 (35%) 28 (50%) .166

BMT recipient 6 (24%) 8 (24%) 1 1 (2.1%) 3 (5.4%) .374Allogeneic BMT 5 (20%) 7 (21%) 1 1 (2%) 3 (5%) .374

ComorbiditiesChronic obstructive pulmonary disease 0 (0%) 2 (6%) .129 7 (15%) 8 (14%) 1Diabetes mellitus 3 (12%) 1 (3%) .179 14 (29%) 15 (27%) .829Hypertension 1 (4%) 3 (9%) .436 19 (40%) 13 (23%) .09Cardiovascular diseases 3 (12%) 2 (6.1%) .427 6 (13%) 13 (23%) .206

Cause of ICU admissionSepsis/septic shock 16 (64%) 26 (79%) .247 24 (50%) 42 (75%) .014Acute respiratory failure 17 (68%) 23 (70%) 1 22 (46%) 41 (73%) .005Acute renal failure 4 (16%) 12 (36%) .138 15 (31%) 20 (36%) .681Neurologic disorders 3 (12%) 15 (45%) .009

Source of admissionEmergency service 8 (32%) 1 (3%) .002 26 (54%) 20 (36%) .078

Morbidities on ICU admissionSepsis/septic shock 15 (60%) 23 (70%) .578 22 (46%) 35 (63%) .114Renal dysfunction 9 (36%) 15 (45%) .592 23 (48%) 28 (50%) .847Neutropenia 14 (56%) 23 (70%) .408 3 (6%) 6 (11%) .414Thrombocytopenia 17 (68%) 31 (94%) .009 12 (25%) 27 (48%) .016Requirement of mechanical ventilation(IMV or NIMV)

6 (24%) 23 (70%) .001 15 (31%) 24 (43%) .310

Hepatic dysfunction 6 (24%) 11 (33%) .564 16 (33%) 23 (41%) .543Requirement of vasopressors treatment 8 (32%) 15 (45%) .417 11 (23%) 20 (36%) .198≥2 organ dysfunctions 15 (60%) 26 (79%) .151 9 (19%) 34 (61%) .0001Suspected or culture-proven infection 23 (92%) 32 (97%) .572 38 (79%) 54 (96%) .011Bacterial infection 9 (36%) 23 (70%) .016 12 (25%) 25 (45%) .042Fungal infection 3 (12%) 10 (30%) .122 1 (2%) 7 (13%) .034Pulmonary infection 17 (68%) 22 (67%) 1 24 (50%) 39 (70%) .047Bloodstream infection 5 (20%) 12 (36%) .247 2 (4%) 9 (16%) .060Urinary tract infection 2 (8%) 7 (21%) .155 8 (17%) 20 (36%) .045On ICU admissionAPACHE II score 18 (12.5-21.5) 30 (24-38.5) .0001 18.5 (14.25-23.75) 25 (21-32) .0001GCS 15 (14.5-15) 10 (4.5-14.5) .0001 15 (14-15) 13 (7-15) .0001SOFA score 8 (5-9) 10.5(7.3-13.8) .001 5 (3-7) 9 (6-12) .0001Hemoglobin level (g/dL) 8.4 (6.9-9.75) 8.2 (6.5-9.4) .568 10 (8.45-11.65) 9.5 (8.53-10.7) .215Leukocytes (/mm3) 8800 (1625-20300) 2960 (695-16825) .143 9930 (6242-13575) 10300 (4300-16775) .907Thrombocytes (/mm3) 55200 (28500-135450) 37650 (18000-65750) .038 166500 (97850-249750) 114500 (35375-210725) .016Sodium (Na, mEq/L) 136 (134.5-138.5) 137.5(135-141.5) .131 135 (131.25-140) 136.5 (133-143) .113AST (IU/L) 32 (16-43) 29(16.3-69.8) .711 24 (17-45) 38 (24.25-80.25) .019LDH (IU/L) 334 (201-682) 418.5 (263-1026) .446 308 (223.5-417) 501 (265.5-875.5) .004C-reactive protein 154 (92-266.3) 205 (106-327) .39 89 (36.25-198.25) 149.5 (111-223.5) .026Procalcitonin 3.7 (0.6-23) 15.5 (0.9-73.5) .212 0.9 (0.245-3.5) 3.9 (1.15-20) .003Calcium (mg/dL) 7.5 (7.2-8) 7.4 (6.63-7.78) .363 8.15 (7.5-8.8) 7.8 (7.125-8.3) .018Total protein (g/dL) 5.5 (4.7-6.4) 4.75 (4.3-5.6) .032 5.6 (4.9-6) 5.4 (4.6-5.83) .28Albumin (g/dL) 2.5 (2.3-2.9) 2.4 (2.2-2.98) .378 2.8 (2.4-3.1) 2.4 (2-2.78) .002Creatinine (mg/dL) 0.9 (0.65-1.65) 0.9 (0.6-2.08) .917 1.2 (0.7-2.125) 1.2 (0.8-2.6) .509Glucose (mg/dL) 142 (120-177) 138 (117-200) .792 134 (118-172) 139.5 (123-201) .455

Morbidities during ICU staySepsis/septic shock 3 (12%) 23 (70%) .0001 4 (8%) 43 (77%) .0001Neutropenia 5 (20%) 16 (46%) .031 1 (2%) 5 (9%) .117Hepatic dysfunction 0 (0%) 12 (36%) .0001 1 (2%) 11 (20%) .005Renal dysfunction 2 (8%) 22 (67%) .0001 3 (6%) 21 (38%) .0001Renal replacement therapy 3 (12%) 19 (58%) .0001 10 (21%) 21 (38%) .086





Table 3 (continued)

Variable Patients with hematological malignancies Patients with solid tumors

Survivor(n = 25)

Nonsurvivor(n = 33)

P Survivor(n = 48)

Nonsurvivor(n = 56)

P

Requirement of mechanical ventilation(IMV or NIMV)

13 (52%) 29 (88%) .003 21 (44%) 46 (82%) .0001

Chemotherapy in ICU 4 (16%) 6 (18%) .827Blood/blood product transfusion 15 (60%) 32 (97%) .0001 14 (29%) 35 (63%) .001Central venous catheterization 6 (24%) 25 (76%) .0001 13 (27%) 44 (79%) .0001Arterial catheterization 19 (76%) 30 (91%) .121 25 (52%) 51 (91%) .0001Tracheostomy 1 (4%) 7 (21%) .045 0 (0%) 10 (18%) .0001Suspected or culture-proven infection 7 (28%) 18 (55%) .062 5 (10%) 32 (57%) .0001Bacterial infection 6 (24%) 18 (55%) .031 4 (8%) 29 (52%) .0001Fungal infection 0 (0%) 5 (15%) .014 2 (4%) 13 (23%) .01Pulmonary infection 6 (24%) 15 (45%) .107 5 (10%) 30 (54%) .0001Urinary tract infection 2 (8%) 3 (9%) .883 1 (2%) 15 (27%) .001Bloodstream infection 1 (4%) 9 (27%) .012 0 (0%) 10 (18%) .0001Steroid use 16 (64%) 31 (94%) .006 22 (46%) 50 (89%) .0001Vasopressor use 6 (24%) 31 (94%) .0001 9 (19%) 53 (95%) .0001

Values are presented as median (interquartile range) or n (%).


stay, sepsis/septic shock during ICU stay, etc). However, only 3independent parameters were identified to be associated with higherICU mortality rate in multivariate analysis. These were APACHE IIscore, requirement of vasopressors, and sepsis/septic shock duringICU stay in all cancer patients. In addition, complete or partialremission of the underlying cancerwas identified as a good prognosticfactor. Although some studies evaluated the independent risk factorsfor mortality in cancer groups in general, some other studiesevaluated risk factors for cancer subgroups specifically [9–12,19–21]. We, therefore, analyzed our data in all the cohort and categorizedas subgroup of patients with solid and hematological malignancies.Acute Physiology and Chronic Health Evaluation II score andrequirement of vasopressors during ICU stay were independent riskfactors for mortality in patients with hematological malignancies,whereas SOFA score, LDH level, and sepsis/septic shock during ICUstay were the independent risk factors for ICUmortality in solid tumorpatients. Admission from emergency department for patients withhematological malignancies and complete or partial remission statusfor patients with solid tumors were good prognostic factors.

Delayed ICU admission is a very well-known risk factor for highermortality rates in noncancer patients. Furthermore, some studies havereported that late ICU admission of cancer patients may be associatedwith poor survival [21,28,29]. We believe that some factors such asrenal dysfunction or respiratory failure could have been modified ormanaged easily by earlier admission to ICU, whereas some otherfactors such as progressive underlying cancer are among the ones thatare unmodifiable. We, therefore, suggest that at least the subgroup of

Table 4Independent risk factors for ICU mortality in cancer patients and their subgroups inmultivariate analysis

Variable OR (95% CI) P

All cancer patientsAPACHE II score 1.12 (1.032-1.215) .007Sepsis/septic shock during ICU stay 8.94 (2.283-35.002) .002Vasopressor use during ICU stay 16.839 (3.98-71.235) .0001Complete or partial remission of theunderlying cancer on ICU admission

0.113 (0.027-0.483) .003

Hematological malignanciesAPACHE II score 1.303 (1.054-1.609) .014Vasopressor use during ICU stay 140.635 (3.592-5505.482) .008Admission from emergency services 0.005 (0.000-0.691) .035Solid tumorsSOFA score 1.831 (1.289-2.601) .001LDH level on admission 1.002 (1-1.005) .028Sepsis/septic shock during ICU stay 138.406 (12.534-1528.4) .0001Complete or partial remission of theunderlying cancer on ICU admission

0.026 (0.002-0.304) .004


cancer patients already inpatient could be saved by earlier evaluationand intervention by the ICU team when they have less severe disease.Earlier ICU admission rather than refusal due to poor outcome duringadmission seems to be a more promising and rational approach,which could be investigated in prospective trials.

The retrospective nature and being a single-center study are themajor limitations of the current report. Furthermore, the relativelysmall sample size leads us to refrain from drawing solid conclusions. Itis also rather difficult to compare crude mortality in different studiesbecause of variations in the underlying disease composition, ICUadmission, and discharge criteria and treatment decision criteria. Ourlocal treatment decisions may not necessarily be applicable to allinstitutions. Putting admission criteria for cancer patients at thebeginning, categorizing lymphomas in solid tumor group, absence ofsite, and number of metastases in cancer patients were the otherlimitations of our study. Finally, we did not collect data on long-termoutcomes or quality of life after discharge from ICU in our cohort,which might have increased the impact of the study.

In conclusion, our study indicates that a reasonable number ofcancer patients might survive their ICU stay. We attribute this 45%survival rate to better selection during ICU admission. AcutePhysiology and Chronic Health Evaluation II score, the status ofunderlying cancer, and requirement of vasopressors can be used asselection criteria on admission to ICU. Earlier ICU intervention andadmission of the at-risk patients might further improve the ICUoutcome of cancer patients. The role of earlier ICU evaluation inimproving ICU outcome seems to be an attractive topic for furtherprospective multicenter trials.

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