Content of this journal is licensed under a Abstract
Aim:
The objective of this study was to retrospectively assess the correlation of malnutrition with mortality and morbidity according to Global Initiative on Malnutrition criteria in patients with the diagnosis of lung cancer hospitalized in the palliative care unit.
Method:
The sample of the study consisted of the data of 705 patients with lung cancer, who were hospitalized in the palliative care unit in a training and research hospital between January 2018 and January 2020. All the patients’ demographic characteristics, disease-related data, laboratory values, Global Initiative on Malnutrition scores, mortality in the last 3 months, and recurrent hospitalizations in the last 3 months were recorded from the patient records and automation system.
Results:
According to the Global Initiative on Malnutrition criteria, 64 (9.2%) of the patients had malnutrition. There was a negative correlation between the ages and the admission albumin levels of patients with malnutrition who passed away in the last 3 months.
Conclusion:
No correlation was found between malnutrition and duration of mortality according to Global Initiative on Malnutrition criteria. Moreover, a difference was found between C-reactive protein and albumin levels of the patients according to the degree of malnutrition. It is recommended that nurses should start nutritional assessments of patients immediately when the patient is admitted to hospital.
Keywords: Lung cancer, malnutrition, morbidity, mortality, palliative care
Introduction
Malnutrition is an important health problem that can be caused primarily by malnutrition or secondarily by some diseases. Anorexia-induced malnutrition due to the disease and/or its treatment and the associated metabolic stress may be the underlying causes of secondary malnutrition. Although the pathophysiology of malnutrition is not exactly known, long-term inadequate nutrient intake, increased need, absorption disorders, inflammatory, and hypermetabolic or hypercatabolic conditions may cause malnutrition (Cederholm et al., 2017; Serón-Arbeloa et al., 2022). Malnutrition is associated with increased risk of infection, increased muscle loss, delayed wound healing, longer hospital stay, and higher mortality and morbidity (Cederholm et al., 2017; Serón-Arbeloa et al., 2022; Soeters et al., 2017).
Cancer patients are at high risk of malnutrition due to both the disease and their treatment processes. It is estimated that 10–20% of deaths of cancer patients can be attributed to malnutrition rather than the malignancy itself (Arends et al., 2017).
Patients with lung cancer are at risk for malnutrition, sarcopenia, and cancer cachexia. This risk increases as the stage of cancer increases (Jain et al., 2020). In advanced lung cancer, the activity of the molecular mechanisms responsible for proteolysis and lipolysis increases and food intake decreases, and early satiety and weight loss, muscle and fat mass loss, anemia, and a cachexia period with hypoalbuminemia are observed (Arends et al., 2017; Argilés, 2005). Despite these, the increased malnutrition in patients with advanced lung cancer leads to negative consequences such as decreased chance and effectiveness of treatment, impaired quality of life of the patient, increased healthcare costs, and low survival rates (Jain et al., 2020).
Although there is treatment opportunity for malnutrition, sarcopenia, and cancer cachexia in recent years, they are often insufficiently diagnosed and therefore not treated. Therefore, early intervention is important to detect these poor prognostic conditions early and improve outcomes (Arends et al., 2017; Argilés, 2005; Jain et al., 2020).
One of the most important elements of palliative treatment is the evaluation and support of the patient’s nutrition (Bozzetti, 2020). Adequate and balanced nutritional support is required for properly maintaining body functions. In the evaluation of nutritional status, methods that combine subjective and objective parameters, can be applied to the patient at regular intervals, and are sensitive in determining malnutrition should be used. Today, there is no gold standard method used to evaluate nutritional status (Bozzetti, 2020; Cotogni et al., 2021). Tools such as Subjective Global Assessment (SGA), Mini-Nutritional Assessment (MNA), Nutrition Risk Screening-2002 (NRS-2002), and Malnutrition Universal Screening Tool (MUST) can be used to determine nutritional risk (Demirel & Atasoy, 2018).
Screening scales such as NRS-2002 are approved screening criteria used for a long term in general clinical practices or malnutrition risk screenings. Many nutrition societies established the Global Initiative on Malnutrition (GLIM) for a common view and published the international GLIM malnutrition diagnostic criteria with a consensus report published in 2019. Global Initiative on Malnutrition offers a two-step approach to the diagnosis of malnutrition (Cederholm et al., 2019; Sanz-Paris et al., 2021). The first of these approaches is to screen using an approved screening tool such as NRS-2002 to determine the risk status and to determine the risk of malnutrition; the second approach is make evaluation to determine the diagnosis and degree of malnutrition (Cederholm et al., 2019). The aim of this study was to retrospectively evaluate the correlation between malnutrition and mortality and morbidity according to the GLIM criteria in patients with the diagnosis of lung cancer hospitalized in the palliative care unit and present it to the literature.
Research Questions
What is the morbidity status of patients with the diagnosis of lung cancer hospitalized in the palliative care unit according to their malnutrition levels according to GLIM criteria?
What is the mortality status of patients with the diagnosis of lung cancer hospitalized in the palliative care unit according to their malnutrition levels according to GLIM criteria?
Is there a correlation between malnutrition according to GLIM criteria and morbidity in patients with the diagnosis of lung cancer hospitalized in the palliative care unit?
Is there a correlation between malnutrition according to GLIM criteria and mortality in patients with the diagnosis of lung cancer hospitalized in the palliative care unit?
Method
Study Design
The data of this retrospective descriptive study were obtained from the hospital records and automation system.
Sample
The sample of the study consisted of the data of 705 patients with lung cancer, who were hospitalized in the palliative care unit in a training and research hospital in Istanbul, Turkey, between January 2018 and January 2020. All patients diagnosed with lung cancer over the age of 18 in the palliative care unit were included in the study.
Data Collection Tools
All patients’ demographic characteristics [age, gender, body mass index (BMI), height, weight, weight loss, and comorbidities], laboratory values (creatinine, C-reactive protein, and albumin), NRS-2002 scores, mortalities in the last 3 months, and recurrent hospitalizations in the last 3 months were recorded.
Data Collection
A two-step approach was used for the diagnosis of malnutrition. In the first stage, the patient’s nutritional risk is assessed. Tools such as SGA, MNA, NRS-2002, and MUST can be used to determine nutritional risk (Demirel & Atasoy, 2018). Nutrition Risk Screening-2002 was used in the evaluation of nutritional risk scores in the hospital where the study was conducted. In the first step, the NRS-2002 scores of the patients recorded in the system were obtained. In the second step, evaluation was made to diagnose malnutrition. According to GLIM, the diagnostic criteria of malnutrition are evaluated under two main headings such as phenotypic and etiological criteria. While the phenotypic criteria are weight loss, low BMI, and low muscle mass, the etiological criteria are low food intake or digestion. Chronic disease/inflammation criteria are screened in patients, and a patient meeting one phenotypic criterion and one etiological criterion is diagnosed with malnutrition (Cederholm et al., 2019). All the patients in the sample met the etiological criteria because they had lung cancer. Body mass index values were used in the evaluation of phenotypic criteria.
Statistical Analysis
The analyses of the study were performed using the Statistical Package for the Social Sciences 26.00 for Windows software (IBM SPSS Corp., Armonk, NY, USA). Percentage distribution, mean, standard deviation, and median values were presented in descriptive statistics. The Chi-square test will be used to determine the difference between categorical variables. In order to determine the difference between the mean scores of continuous variables, parametric tests (t-test, one-way ANOVA) will be used for normally distributed ones, and non-parametric tests (Mann–Whitney U test and Kruskal–Wallis test) will be used for non-normally distributed ones. Correlation analysis was used to analyze the correlation between patients’ demographic data and laboratory findings, length of hospital stay, mortalities in the last 3 months, and recurrent hospitalizations in the last 3 months.
Ethical Considerations
The study was conducted in accordance with the Declaration of Helsinki once approval was obtained from the Acıbadem University and Acıbadem Healthcare Institutions Medical Research Ethics Committee (dated 31.12.2020 and numbered 2020-27/29).
Results
The mean age of the patients was 66.52 ± 10.56 years, and 578 (82%) were male. Of the patients, 217 (30.8%) were hospitalized with the diagnosis of adenocarcinoma and 672 (95.3%) were in stage 4. The number of participants with comorbid diseases was 390 (55.3%) (Table 1).
Table 1.
Sociodemographic and Disease-Related Characteristics of the Patients (N = 705)
| Mean | SD | |
|---|---|---|
| Age | 66.52 | 10.56 |
| NRS-2002 score | 2.77 | 0.07 |
| Height, m | 1.66 | 2.90 |
| Weight, kg | 66.52 | 10.56 |
| Admission creatinine | 1.41 | 8.49 |
| Admission CRP | 93.46 | 84.18 |
| Admission albumin | 30.39 | 18.59 |
| n | % | |
| Gender | ||
| Female | 127 | 18.0 |
| Male | 578 | 82.0 |
| Cancer type | ||
| Small cell lung cancer | 125 | 17.7 |
| Adenocarcinoma | 217 | 30.8 |
| Squamosis | 132 | 18.7 |
| Other | 102 | 14.5 |
| Stage | ||
| Stage 2–3 | 33 | 4.7 |
| Stage 4 | 672 | 95.3 |
| Comorbidity | ||
| Yes | 390 | 55.3 |
| No | 315 | 44.7 |
| Malnutrition | ||
| No malnutrition (>20 kg/m2) | 624 | 88.5 |
| Moderate malnutrition (18.5–20 kg/m2) | 33 | 4.7 |
| Severe malnutrition (<20.0 kg/m2) | 31 | 2.4 |
| Unstated | 17 | 2.4 |
| Mortality within 3 months | ||
| Yes | 506 | 71.8 |
| No | 199 | 28.2 |
| Recurrent hospitalizations palliative care unit repeated admission within 3 months prior to GLIM assessment | ||
| Yes | 120 | 17.0 |
| No | 585 | 83.0 |
| The number of palliative care unit repeated hospitalizations before the last hospitalization | ||
| One | 91 | 75.8 |
| Two | 24 | 20.0 |
| Three | 4 | 3.3 |
| Four | 1 | .8 |
Note: CRP = C-reactive protein; GLIM = Global Initiative on Malnutrition; NRS = Nutrition Risk Screening-2002; SD = standard deviation.
According to the GLIM criteria, 64 (9.2%) of the patients suffered from malnutrition. There was a significant difference between admission creatinine (t = –2.050; p = 0.041) and admission CRPs (t = –2.515; p = 0.012) of patients with and without malnutrition according to the GLIM criteria (Table 2).
Table 2.
Disease Characteristics of the Patients in Terms of Malnutrition Status of GLIM Criteria
| According to GLIM Criteria | Mean | SD | t | p | |
|---|---|---|---|---|---|
| Admission creatinine | No malnutrition | 1.19 | 7.09 | –2.050 | 0.041 * |
| Malnutrition | 3.59 | 17.39 | |||
| Admission CRP | No malnutrition | 90.39 | 84.47 | –2.515 | 0.012 * |
| Malnutrition | 120.97 | 80.97 | |||
| Admission albumin | No malnutrition | 30.83 | 19.53 | 1.733 | 0.084 |
| Malnutrition | 26.40 | 5.88 | |||
| Length of stay in hospital | No malnutrition | 12.72 | 11.81 | –.582 | 0.561 |
| Malnutrition | 13.63 | 12.21 | |||
| Survival times of patients after GLIM assessment | No malnutrition | 63.76 | 93.03 | .614 | 0.540 |
| Malnutrition | 55.77 | 103.41 | |||
| Died in the last 3 months after GLIM assessment | No malnutrition | 35.43 | 49.81 | 1.098 | 0.273 |
| Malnutrition | 27.29 | 52.69 |
* p < 0.05
Note: CRP = C-reactive protein; GLIM = Global Initiative on Malnutrition; SD = standard deviation.
There was no statistically significant difference between the survival times of patients with and without malnutrition according to the GLIM criteria after GLIM assessment (t = 0.614; p = 0.540). In the GLIM assessment, there was a negative correlation between the ages of patients with malnutrition who died in the last 3 months and their admission albumin levels (r = –0.309; p = 0.037) and a positive (r = 1.000; p = 0.000) correlation between admission creatinine levels and the number of recurrent hospitalizations in the last 3 months (Table 3).
Table 3.
The Correlation Between Characteristics of Patients with Malnutrition Who Passed Away in the Last 3 Months in the GLIM Assessment (n = 51)
| Age | BMI | Admission Creatinine | Admission CRP | Admission Albumin | The Last Period of Stay in the Hospital | Survival Times of Patients After GLIM Assessment | The Number of Recurrent Hospitalizations in the Last 3 Months | ||
|---|---|---|---|---|---|---|---|---|---|
| Age | r | 1 | .059 | .036 | .146 | –.309 | –.125 | .187 | .517 |
| p | .679 | .814 | .362 | .037* | .383 | .188 | .234 | ||
| BMI | r | .059 | 1 | .194 | –.158 | .185 | –.006 | –.253 | .562 |
| p | .679 | .197 | .325 | .218 | .965 | .073 | .189 | ||
| Admission creatinine | r | .036 | .194 | 1 | –.289 | .017 | –.046 | .102 | 1.000 |
| p | .814 | .197 | .067 | .913 | .761 | .500 | .000 * | ||
| Admission CRP | r | .146 | –.158 | –.289 | 1 | –.257 | –.185 | –.033 | –.694 |
| p | .362 | .325 | .067 | .105 | .248 | .837 | .083 | ||
| Admission albumin | r | –.309 * | .185 | .017 | –.257 | 1 | .084 | .027 | .017 |
| p | .037 | .218 | .913 | .105 | .578 | .857 | .971 | ||
| The last period of stay in the hospital | r | –.125 | –.006 | –.046 | –.185 | .084 | 1 | .102 | –.196 |
| p | .383 | .965 | .761 | .248 | .578 | .477 | .674 | ||
| Survival times of patients after GLIM assessment | r | .187 | –.253 | .102 | –.033 | .027 | .102 | 1 | .221 |
| p | .188 | .073 | .500 | .837 | .857 | .477 | .633 | ||
| The number of recurrent hospitalizations in the last 3 months | r | .517 | .562 | 1.000 | –.694 | .017 | –.196 | .221 | 1 |
| p | .234 | .189 | .000 * | .083 | .971 | .674 | .633 | ||
Note: BMI = body mass index; CRP = C-reactive protein; GLIM = Global Initiative on Malnutrition.
There was a statistically significant difference between admission CPR levels (W = 10.434; p = 0.015) and admission albumin levels (W = 9.630; p = 0.022) according to malnutrition degree in patients who passed away within 3 months after GLIM assessment (Table 4).
Table 4.
Disease Characteristics of the Patients Who Passed Away Within 3 Months After GLIM Assessment According to Malnutrition Degrees (n = 459)
| Malnutrition According to the GLIM Criteria | Mean | SD | KW | p | |
|---|---|---|---|---|---|
| Admission creatinine | No malnutrition | 1.32 | 8.44 | 5.127 | .163 |
| Moderate malnutrition | 7.64 | 27.67 | |||
| Severe malnutrition | 0.83 | 0.309 | |||
| Admission CRP | No malnutrition | 99.28 | 87.07 | 10.434 | .015 * |
| Moderate malnutrition | 124.57 | 96.48 | |||
| Severe malnutrition | 143.20 | 53.32 | |||
| Admission albumin | No malnutrition | 29.74 | 14.42 | 9.630 | .022 * |
| Moderate malnutrition | 27.26 | 4.81 | |||
| Severe malnutrition | 24.36 | 8.12 | |||
| The last period of stay in the hospital | No malnutrition | 12.62 | 10.85 | 1.362 | .715 |
| Moderate malnutrition | 12.16 | 11.23 | |||
| Severe malnutrition | 12.99 | 15.77 | |||
| Survival times of patients after GLIM assessment | No malnutrition | 35.43 | 49.81 | 8.214 | .042 |
| Moderate malnutrition | 17.44 | 16.11 | |||
| Severe malnutrition | 36.76 | 21.32 |
Note: KW = Kruskall-Wallis Test; CRP = C-reactive protein; GLIM = Global Initiative on Malnutrition; SD = standard deviation.
There was no significant correlation between malnutrition status and mortality of the patients according to the GLIM criteria (χ 2 = 2.391; p = 0.122). There was no significant correlation between malnutrition status and comorbidities of the patients according to the GLIM criteria (χ 2 = 0.008; p = 0.927) (Table 5).
Table 5.
The Correlation Between Malnutrition Status and Mortality and Morbidity of the Patients
| Malnutrition | χ 2 | p | |||
|---|---|---|---|---|---|
| No | Yes | ||||
| Died in the last 3 months after GLIM assessment | Yes | 440 | 51 | 2.391 | .122 |
| No | 184 | 13 | |||
| Comorbidity | Yes | 345 | 35 | 0.008 | .927 |
| No | 279 | 29 | |||
| Cancer type | Small cell lung cancer | 117 | 7 | 5.871 | .209 |
| Adenocarcinoma | 193 | 22 | |||
| Squamosis | 115 | 12 | |||
| Other | 83 | 14 | |||
| The number of recurrent hospitalizations in the last three months | Yes | 111 | 8 | 1.135 | .287 |
| No | 513 | 56 | |||
Note = GLIM = Global Initiative on Malnutrition.
Discussion
This study aimed to retrospectively evaluate the correlation of malnutrition with mortality and morbidity according to the GLIM criteria in patients with the diagnosis of lung cancer hospitalized in the palliative care unit and present it to the literature.
In a study conducted with 124 cancer patients at different stages, 77% (n = 96) of the patients got an NRS-2002 score of 3 points or higher (Demirel & Atasoy, 2018). In a study conducted with 82 cancer patients at Gaziantep University, the NRS-2002 score was found to be 2.22 ± 0.72 (Sancar Bekircan & Ünlü, 2022). The result of the present study is compatible with the results of previous studies. In the present study, the NRS mean score of palliative care patients with lung cancer was 2.77 ± 0.7. According to the GLIM criteria, 64 (9.2%) of the palliative care patients had malnutrition. Another study conducted with 336 people aged 65 and over reported that the prevalence of malnutrition was 17.6% according to the GLIM criteria and 5.65% according to the European Society for Clinical Nutrition and Metabolism (ESPEN) consensus (Beaudart et al., 2019). In another study conducted with hospitalized elderly patients, their malnutrition rate was 25.8% (Yilmaz et al., 2020). A study conducted with cancer patients reported that the highest incidence of malnutrition was seen 7 weeks after the start of treatment for all GLIM combinations. The malnutrition rate was 32.4% in the combination of phenotypic and etiological criteria in the last 6 months. (Einarsson et al., 2020).
In another study with cancer patients, according to the GLIM criteria, malnutrition was detected in 72.2–80% patients (Contreras-Bolívar et al., 2019). Considering that the mean age of the patients in the sample group was over 65, it can be asserted that the malnutrition rates of the palliative care patients were higher than the other elderly.
Cancer increases the risk of malnutrition in patients. The degree of malnutrition varies according to the type of disease, stage, treatment applied, age, gender, and consumption. In this patient group, the risk of malnutrition should be identified early and nutritional support should be started early. Since the risk of malnutrition is high in lung cancer patients, it can be said that the low malnutrition rates of the patients in the sample group in the present study may be associated with the earlier initiation of nutritional support.
There was a significant difference between the admission CRPs of patients with and without malnutrition according to the GLIM criteria. In addition, there was a difference between admission CPR levels of patients, who passed away within 3 months after GLIM assessment, according to malnutrition degrees.
Inflammation is an etiological criterion in the GLIM classification and is widely accepted for both screening and nutritional assessment. Markers such as serum albumin or CRP used in the Glasgow prognostic score are useful for detecting inflammation in cancer patients (Nozoe et al., 2014). In a previous study, the assessments made according to the GLIM criteria indicated that albumin and prealbumin values were significantly lower and CRP was higher in patients with malnutrition than in patients eating a normal diet. Moreover, in-hospital mortality and 6-month mortality were significantly higher in these patients. In the same study, rehospitalizations also tended to be higher in patients with malnutrition, although this was not statistically significant (Contreras-Bolívar et al., 2019). Contreras-Bolivar’s study and the present study revealed that inflammation, which is one of the etiological factors of the GLIM criteria, is also associated with mortality.
In the present study, there was no significant correlation between malnutrition status and mortality of the patients according to the GLIM criteria. In another study with ambulatory cancer patients, severe malnutrition according to the GLIM criteria was associated with increased mortality risk (De Groot et al., 2020); this was not the case for moderate malnutrition according to GLIM or for moderate or severe malnutrition (GLIM) when adding handgrip strength <10th percentile of reference values. Recent studies have reported that malnutrition according to the GLIM criteria with the addition of hand grip strength in hospitalized cancer patients is associated with higher mortality, specifically a two- threefold increase in mortality (Contreras-Bolívar et al., 2019; Yilmaz et al., 2020). In the present study, the GLIM criteria with the addition of hand grip strength were not analyzed. Moreover, in the assessment of the presence of malnutrition, only BMI value from the GLIM criteria’s phenotypic criteria and the presence of chronic disease from the etiological criteria were considered as malnutrition. Combinations with the other criteria were not have been lower.
Study Limitations
The study was done retrospectively, and the data constituted archival information. Errors may have been made during the recording of the data. Despite this limitation, our study is one of the limited numbers of studies on this subject and evaluated many parameters at the same time.
Conclusion and Recommendations
As a result of the study, it was found that there was no difference between the presence of malnutrition according to the GLIM criteria and mortality status in palliative care patients with lung cancer. Despite this, there was a difference between CRP and albumin levels, which support the presence of inflammation, which is one of the etiological factors of GLIM, according to the malnutrition degree of the patients who passed away within 3 months after GLIM assessment. Furthermore, there was a difference between the presence of malnutrition and the CRP mean values of the patients. The malnutrition status of the patients was not correlated with their comorbidities, cancer types, and recurrent hospitalizations. Nutrition has an important role to play in supportive and palliative care, from diagnosis through to end-of-life care. In addition, our study showed a relationship between some markers of malnutrition and end-of-life time of patients. Therefore, it is recommended that nurses should start nutritional assessments of patients immediately when the patient is admitted to palliative care and should be performed at regular intervals. In addition, malnutrition diagnosed in the early period should be intervened immediately in cooperation with the physician and dietician. It is recommended to use a prospective study design in future studies. In addition, it is recommended that reduced muscle mass (reduced calf circumference, reduced mid-arm circumference, declined muscle strength, and fat-free mass index) measurements be evaluated in future studies to measure the nutritional status of patients.
Footnotes
Ethics Committee Approval: Ethics committee approval was received for this study from the Acıbadem University and Acıbadem Healthcare Institutions Medical Research Ethics Committee (2020-27/29).
Informed Consent: Written informed consent was obtained from all participants who participated in this study.
Peer-review: Externally peer-reviewed.
Author Contributions: Concept - M.H.İ, Ö.O., V.K.; Design - M.H.İ, Ö.O., V.K.; Supervision - Ö.O.; Materials - M.H.İ, V.K.; Data Collection and/or Processing - M.H.İ, Ö.O.; Analysis and/or Interpretation - M.H.İ, V.K.; Literature Review - M.H.İ.; Writing - M.H.İ, Ö.O., V.K.; Critical Review - Ö.O., V.K.
Declaration of Interests: The authors have no conflict of interest to declare.
Funding: The authors declared that this study has received no financial support.
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