Patients after allogeneic hematopoietic SCT (HSCT) are at risk of malnutrition. To assess the impact of malnutrition after allogeneic HSCT on transplant outcomes, we conducted a retrospective study. Adult patients who received allogeneic HSCT from 2000 to 2009 for standard-risk leukemia and achieved disease-free survival up to 3 months after allogeneic HSCT were included. From participating centers, 145 patients were enrolled. Median age was 46 years (19–68). Patients were classified based on weight loss during 3 months after allogeneic HSCT as follows: normal group (weight loss <5%, n=53), mild malnutrition group (5%⩽weight loss<10%, n=47), severe malnutrition group (10% ⩽weight loss, n=45). The cumulative incidences of 2-year nonrelapse mortality (NRM) were 3.8% in the normal group, 8.5% in the mild malnutrition group and 27.3% in the severe malnutrition group. The probabilities of a 2-year OS were 73.2% in the normal group, 74.5% in the mild malnutrition group and 55.3% in the severe malnutrition group. In multivariate analysis, severe malnutrition was associated with an increased risk of NRM and a worse OS. In conclusion, weight loss ⩾10% was associated with a worse clinical outcome. Prospective studies that identify patients at risk of malnutrition and intervention by a nutritional support team are warranted.
Allogeneic hematopoietic SCT (HSCT) is an integral treatment modality for hematological malignancies. The rate of early death after allogeneic HSCT has significantly decreased in last decades.1 Therefore, the importance of the management of survivors at the outpatient clinic is increasing. Although it might include the management by a nutritional support team, the impact of malnutrition at the outpatient clinic on the subsequent clinical outcome is not yet well established.
It was reported that discharged patients who survived the early period after allogeneic HSCT frequently experienced nutritional problems related to GVHD.2, 3, 4 Lenssen et al. have reported that long-term survivors experienced weight loss, especially after 100 days post-transplant.2 One major cause of weight loss was insufficient caloric intake. Previous studies showed that patients often experienced nausea and vomiting and needed parenteral nutrition.5 We also see patients who are unable to manage sufficient oral intake to maintain adequate nutritional status immediately post discharge from the transplant unit. Not all patients are diagnosed as acute GVHD of gut by endoscopy.6 Even though oral caloric intake often recovers spontaneously, time taken for recovery is usually long and patients often experience significant weight loss.7,8
Even though several studies assessed the impact of body mass index (BMI) before allogeneic HSCT,9, 10, 11 there are limited data about the nutritional status of outpatients after allogeneic HSCT because the practice of screening of nutritional status is still rarely performed. Nutritional screening aims to identify patients who are malnourished or at risk of malnutrition.12,13 Patients identified through screening require referral to a dietitian for nutritional assessment. Nutritional screening to identify patients at risk is important because early intervention is necessary in order to improve the outcome by nutritional support. Although malnutrition in general negatively influences prognosis,14, 15, 16, 17 the impact of weight loss after allogeneic HSCT on the subsequent clinical outcome has not yet been assessed. In this study, we aimed to determine the prevalence of weight loss and assess the impact of weight loss on the clinical outcome after allogeneic HSCT. If weight loss after allogeneic HSCT negatively influences prognosis, nutritional support with exercise might help to reduce the consequences of poor nutrition and improve clinical outcomes.
Patients and methods
This study was approved by the Institutional Review Board of National Cancer Center, Tokyo, Japan. The patients in this analysis were aged 18 years or older and had received a first allogeneic HSCT from 2000–2009. We included patients with standard-risk leukemia—AML or ALL in first or second remission, or CML in first chronic phase. The stem cell source was PBSC or BM. We included patients who achieved a disease-free survival for at least 90 days after allogeneic HSCT. All patients who met these eligibility criteria were included in this study. During the study period, there was no consensus practice guideline of nutritional support in participating centers. There was no consensus regarding adjustment of the conditioning regimen dose for patients with obesity, which will likely vary among the transplant centers, even though in this cohort only 3 patients were obese (BMI >30 kg/m2) at allogeneic HSCT.
The study endpoints included the prevalence of patients with weight loss, and clinical outcomes including nonrelapse mortality (NRM), OS and relapse after day 90 post-transplant. In this study, patients were classfied into three groups based on weight loss during 3 months after allogeneic HSCT as follows: normal (weight loss<5%), mild malnutrition (5%⩽weight loss<10%), severe malnutrition (10% ⩽weight loss). OS was defined as time to death from any cause. NRM was defined as death from any cause or death in continuous CR. Relapse was defined as the time to onset of hematologic recurrence.
A descriptive statistical analysis was performed to assess the patients’ characteristics. Medians and ranges are provided for continuous variables and percentages are shown for categorical variables. In the comparison of three groups, statistical correction by Bonferroni’s method was used. The patients' characteristics were compared using the Chi-square test for categorical variables. The probability of OS was calculated by the Kaplan–Meier method. A Cox proportional-hazards regression model was used to analyze OS. The cumulative incidences of NRM and GVHD were evaluated using the Fine and Grey model for univariate and multivariate analyses. In the competing risk models for GVHD, relapse and death before these events were defined as competing risks. In the competing risk models for NRM, relapse was defined as a competing risk. Factors that were associated with a two-sided P-value of <0.10 in the univariate analysis were included in a multivariate analysis. We used a backward-stepwise selection algorithm and retained only the statistically significant variables in the final model. A two-sided P-value of <0.05 was considered statistically significant. The variables evaluated in these analyses were as follows: BMI at day 90 (BMI <18.5 kg/m2 vs BMI ⩾18.5 kg/m2), sex (female vs male), patient’s age at HSCT (continuous), disease (AML vs ALL vs CML), stem cell source (related vs unrelated, BM vs PBSC), GVHD prophylaxis (CYA-based vs tacrolimus-based), conditioning regimen (myeloablative vs reduced-intensity), transplant year (2000–2004 vs 2005–2009) and the presence of grade II–IV acute GVHD. We also assessed serum albumin level (⩾3.0 mg/dL vs <3.0 mg/dL) and serum C-reactive protein (CRP) level (⩾0.27 mg/dL vs <0.27 mg/dL). In terms of serum albumin level, 3.0 mg/dL was chosen as a threshold as reported previously.18 In terms of serum CRP level, 0.2 mg/dL was chosen as a mean value of CRP at day 90 was 0.27 mg/dL. All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Shimotsuke-shi, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, version 2.13.0).19 More precisely, it is a modified version of R commander (version 1.6–3) that was designed to add statistical functions that are frequently used in biostatistics.
The patient characteristics are shown in Table 1. All patients had a good performance status before transplant (ECOG performance status 0 or 1). In this cohort, 101 patients (69.7%) received a myeloablative conditioning regimen. In a myeloablative conditioning regimen, TBI-based (n=61), BU plus CY-based (n=37) and other regimens (fludarabine plus melphalan) were used. In a reduced-intensity conditioning regimen (n=44), all patients received purine analog plus BU-based regimen. The median age was 33 years (range, 19–68). The median follow-up of surviving patients was 2992 days after allogeneic HSCT. The trend of mean body weight after allogeneic HSCT was shown in Figure 1a. Patients were classified into three groups based on weight loss during 3 months after allogeneic HSCT as follows: normal group (weight loss <5%, n=53), mild malnutrition group (5%⩽weight loss<10%, n=47), severe malnutrition group (10%⩽weight loss, n=45). Compared to the normal group, the mild malnutrition group and severe malnutrition group had more patients with prior grade II–IV acute GVHD, more patients with systemic steroids and more patients who received a BMT (Table 1). Patients in the severe malnutrition group tended to have more stage 2–4 gut acute GVHD (n=9, 20%) than other groups. Although the mean dose of steroid at day 90 in the severe malnutrition group was significantly higher than that in the normal group, there was no significant difference between the mild malnutrition group and the severe malnutrition group (prednisolone-equivalent dose at day 90, 5 mg/day in the normal group, 7 mg/day in the mild malnutrition group and 14 mg/day in the severe malnutrition group).
The cumulative incidences of chronic GVHD after day 90 were 64.2% in the normal group, 59.6% in the mild malnutrition group and 60.9% in the severe malnutrition group, respectively (P=0.72, Figure 1b). There was no statistically significant difference in the incidence of chronic GVHD among the three groups. The cumulative incidences of extensive chronic GVHD after day 90 were 52.8% in the normal group, 40.4% in the mild malnutrition group and 56.2% in the severe malnutrition group, respectively (P=0.17, Figure 1c). There was no statistically significant difference among the three groups.
The cumulative incidences of a 2-year NRM after day 90 were 3.8% in the normal group, 8.5% in the mild malnutrition group and 27.3% in the severe malnutrition group, respectively (P<0.01, Figure 1d). Low BMI at day 90 (BMI<18.5 kg/m2) was not a significant variable. In a multivariate analysis, the presence of severe malnutrition was associated with an increased risk of NRM (HR 4.05, 95% confidence interval (CI) 1.54–10.7, P<0.01, Table 2). The cumulative incidences of a 2-year relapse after day 90 were 26.4% in the normal group, 25.5% in the mild malnutrition group and 20.5% in the severe malnutrition group, respectively (P=0.76). The probabilities of a 2-year OS after day 90 were 73.2% in the normal group, 74.5% in the mild malnutrition group and 55.3% in the severe malnutrition group, respectively (P=0.17). In a multivariate analysis, the presence of severe malnutrition was associated with a worse OS (HR 2.04, 95%CI 1.12–3.71, P=0.02, Table 2).
In terms of biochemical indices, mean serum albumin level at day 90 was 3.96 g/mL in the normal group, 4.00 g/mL in the mild malnutrition group and 3.73 g/mL in the severe malnutrition group, respectively. Serum albumin level in the severe malnutrition group was significantly lower than that in the mild malnutrition group (P=0.03). Mean serum total protein level at day 90 was 6.39 g/mL in the normal group, 6.36 g/mL in the mild malnutrition group and 6.02 g/mL in the severe malnutrition group, respectively. Serum total protein level in the severe malnutrition group was significantly lower than that in the normal group (P=0.03). Mean CRP level at day 90 was 0.22 mg/dL in the normal group, 0.21 mg/dL in the mild malnutrition group and 0.39 mg/dL in the severe malnutrition group, respectively. There was no statistically significant difference among the three groups. There was no statistically significant difference in terms of other biochemical indices including aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, γ-glutamyltransferase, total bilirubin, creatinine and fasting glucose level (data not shown). We assessed the impact of low albumin level (<3.0 g/mL) and high CRP level (⩾0.27 mg/dL) on the clinical outcome as a post-hoc analysis. In terms of NRM after day 90, both low albumin level at day 90 and high CRP level were associated with an increased risk of NRM after day 90 (P<0.01 and P=0.021, respectively) in univariate analyses. In a multivariate analysis, only low albumin level remained a significant prognostic factor for NRM, independently of weight loss in 3 months (HR 4.58, 95%CI 1.06–19.8, P=0.042). In terms of OS after day 90, both low albumin level at day 90 and high CRP level were associated with a worse OS (P=0.044 and P=0.033) in univariate analyses. In a multivariate analysis, only low albumin level remained a significant prognostic factor for OS, independently of weight loss in 3 months (HR 3.05, 95%CI 1.18–7.85, P=0.021).
Causes of death in the normal group were chronic GVHD-related (n=3), bleeding (n=1) and secondary cancer (n=1). Causes of death in the mild malnutrition group were chronic GVHD-related (n=2), primary breast cancer (n=1), secondary cancer (n=1) and unknown (n=1). Causes of death in the severe malnutrition group were acute GVHD-related (n=2), chronic GVHD-related (n=8), secondary cancer (n=2) and unknown (n=1).
In this study, for the first time we have demonstrated that the presence of severe malnutrition in 3 months defined by weight loss after allogeneic HSCT was associated with a poor subsequent clinical outcome due to an increased risk of NRM mainly relating to GVHD. Although several studies have previously shown that a fraction of patients after allogeneic HSCT lost body weight, no study has assessed the impact of weight loss on the subsequent clinical outcome. We assessed both BMI and weight loss as a tool for nutritional screening and found that only weight loss has a significant impact on the clinical outcome, which is consistent with the general consensus that the change of body weight reflects the nutritional status more precisely than the actual body weight.12
We found that a significant proportion of patients lost body weight in the 3 months after allogeneic HSCT. Almost one-third of patients lost body weight ⩾10% in 3 months. Although no standardized nutritional screening tool has been designed specifically for use in patients after allogeneic HSCT, weight loss is in general regarded as an integral part of nutritional screening in most nutritional screening tool.12,13,20 For instance, the Nutritional Risk Screening (NRS 2002) is a tool developed by ESPEN (European Society for Clinical Nutrition and Metabolism) working group in 2002.12,13 NRS 2002 included weight loss as the main factor in initial and final screening. Following the Malnutrition Universal Screening Tool for adults written in ESPEN guidelines for nutrition screening,12 patients who lost body weight ⩾10% in 3–6 months are regarded as severely malnourished.12,13 The presence of such severe malnutrition in the 3 months after allogeneic HSCT was associated with a poor clinical outcome in this study, which suggests the clinical implication of severe malnutrition after allogeneic HSCT. Although weight loss is included in the criteria of chronic GVHD by National Institutes of Health consensus, no definition of weight loss has been determined due to the lack of data.21 In our study, the major cause of death in the severe malnutrition group was chronic GVHD-related, in particular infectious diseases in patients with chronic GVHD. As expected, patients with significant weight loss must be vulnerable to infectious diseases after allogeneic HSCT. Our data suggest that it is reasonable to use weight loss ⩾10% in 3 months to identify patients at risk of NRM relating to chronic GVHD as in other fields.12
If weight loss after allogeneic HSCT is associated with a worse OS, it is reasonable to try to identify patients at risk and intervene to improve the nutritional status. In other fields, a prospective, controlled trial with 212 hospitalized patients showed an increase in nutrition intake and a shorter length of hospital stay in patients who received nutritional intervention, which supported the idea that nutritional intervention in patients at nutritional risk improved the clinical outcome.22 Another prospective, controlled trial in patients with colorectal cancer demonstrated that nutritional intervention contributed to an increase of nutritional intake and maintenance of nutritional status.23,24 When applying a periodic nutritional assessment of all patients after allogeneic HSCT, it might be possible to identify patients at risk for malnutrition to start early with nutritional support and to achieve a clinical benefit as reported.25 Such intervention should be prospectively examined in patients at nutritional risk after allogeneic HSCT. In addition, exercise is an important part of intervention to keep the muscle weight as previously reported.26,27 In particular, inactivity was reported to amplify the catabolic response of skeletal muscle to steroid.28,29 Therefore, effective programs including nutritional support and exercise to prevent the catabolism in patients who receive systemic steroid must be developed.
Reduced food intake is a major factor for the deterioration of nutritional status. We can assume that such reduced food intake is caused by anorexia and other gastrointestinal symptoms. It has been reported that a significant proportion of patients who are discharged to the outpatient setting are unable to sustain adequate oral intake.5,8,30 Charuhas et al. reported that patients in the hydration solution group lost more weight compared with the supplemental PN group in the outpatient clinic.8 Therefore, if patients have eating difficulties and do not receive supplemental nutrition, they will easily lose body weight. At an earlier phase after allogeneic HSCT, some studies showed that the insufficient caloric intake was associated with a significant weight loss.31,32 At a later phase in the outpatient clinic, it was often difficult to conduct a routine checkup of nutritional status after allogeneic HSCT, in particular in small centers or in developing countries. However, as our study showed, nutritional status after discharge is important and nutritional support team has to follow the nutritional status in the outpatient setting as well as in the inpatient setting.
In terms of biochemical indices, serum albumin and total protein level in the severe malnutrition group were significantly lower than those in other groups. However, we would like to emphasize that the absolute difference in biochemical indices among the three groups in our study was minimal (around 0.3 g/mL in both serum albumin and total protein level). Therefore, it must be inappropriate to determine the nutritional status solely by the level of these biochemical indices as recommended.33 In a post-hoc analysis, we found that low albumin level at day 90 was a significant prognostic factor of adverse outcome after day 90, independently of weight loss. This finding is consistent with a report from Kharfan-Dabaja and colleagues.18 Therefore, low albumin level, which reflects the level of inflammation, might be useful to assume the risk of NRM.
The limitation of this study should be clarified. The high mortality rate found in patients with severe weight loss is consistent with previous studies in other fields. However, severe weight loss is expected to reflect the poor general condition caused by the persistent inflammation or use of steroid and so on. Therefore, it is statistically difficult to distinguish the effects of malnutrition on the clinical outcome from other causes, even if we performed multivariate analyses. However, we might be able to say that the presence of malnutrition is a surrogate marker of poor general condition which is associated with a worse OS. More research is required before the data can be interpreted to conclude that malnutrition per se is responsible for increased mortality as in other fields.
Another important point is that this study included patients who received allogeneic HSCT from 2000–2009. Therefore, the practice in allogeneic HSCT changed significantly during the period, which affected the overall clinical outcome, even though time period was not a significant variable. Such change in clinical practice might explain why the NRM rate in patients with AML and ALL were substantially lower than that in those with CML, because patients with CML received allogeneic HSCT in the earlier time period. However, due to the lack of data about cytogenetics in patients with AML and ALL, we were not able to estimate the disease risk of patients with AML and ALL.34
In conclusion, we have shown that the prevalence of significant weight loss (>10% in 3 months) was high after allogeneic HSCT and the presence of such significant weight loss was associated with a poor clinical outcome. Future studies that prospectively try to identify patients at risk of weight loss and prevent weight loss are warranted. In addition, future studies should investigate the changes in body composition to assess the impact of loss of fat-free mass, mainly due to muscle atrophy.
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We thank the medical, nursing, data-processing, laboratory and clinical staffs at the participating centers for their important contributions to this study and their dedicated care of the patients.
The authors declare no conflict of interest.
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Fuji, S., Mori, T., Khattry, N. et al. Severe weight loss in 3 months after allogeneic hematopoietic SCT was associated with an increased risk of subsequent non-relapse mortality. Bone Marrow Transplant 50, 100–105 (2015) doi:10.1038/bmt.2014.228
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