https://orcid.org/0000-0001-5695-6907
Abstract
Malnutrion among children with childhood cancer in low and middle income countries (LMICs) is prevelant. While national nutrition programs focus on children under 5 years, childhood cancer can occur regardless of their age. Through a single-center retrospective cohort in Lilongwe, Malawi, we aim to characterize the burden of age-related malnutrition among children diagnosed with cancer in Lilongwe, Malawi, and evaluate them for any associations with mortality. Four hundred and sixty-three children (63.5% ≥5 years and 58.3% males) were identified.The majority of children (63.3%) were malnourished; 23.1% had moderate acute malnutrition (MAM) and 40.2% had severe acute malnutrition (SAM). Malnutrition was more common in children ≥5 years (70.0%) compared to children <5 years (51.8%); p < 0.0001. Age <5 years (HR 1.6; 95%CI 1.1-2.3, p = 0.016) and presence of sever acute malnutrition (HR 1.6, 95%CI 1.1-2.3, p = 0.012) were both associated with increased mortality risk. Acute malnutrition was highly prevalent among children with cancer above 5 years of age. This age group is not prioritized among malnutrition programs in LMICs, hence there is a direct need to include children with cancer regardless of age in national nutrition guidelines in LMICs to give them acces to adequate nutritional support.
Background
Nearly 90% of all childhood cancer cases worldwide occur in low-and-middle-income countries (LMICs) (Citation1, Citation2). Specifically, greater than 100,000 children in Sub-Saharan Africa are estimated to develop cancer annually (Citation3). Unlike high-income countries where survival is estimated at 80%, in LMICs, survival rates do not exceed 20% (Citation1, Citation4–9).
Children with cancer are at an increased risk for malnutrition for many reasons including diminished intake, enhanced losses, and increased needs (Citation10). Additionally, increased metabolic rates, as well as circulating peptides and cytokines can lead to anorexia and cachexia, increased fat and protein breakdown, and increased gluconeogenesis (Citation11). Malnutrition is also often exacerbated during treatment due to further challenges arising from the side effects of chemotherapy, such as taste changes, anorexia, mucositis, nausea, vomiting, and diarrhea (Citation12, Citation13). Children with both cancer and malnutrition have been noted to have prolonged neutropenia, changes in pharmacokinetics, and possible inferior event-free survival (Citation14–18). Studies have shown varied prevalence of malnutrition at the time of cancer diagnosis—up to 15% in high-income countries (Citation19, Citation20) and up to 77% in LMICs, depending on the diagnosis (Citation15, Citation16, Citation20–23).
Apart from the concurrent disease, malnutrition poses a significant health risk including an increased risk of death compared to their well-nourished counterparts (Citation24–26). Worldwide, nearly half of all deaths in children under 5 years of age are attributed to malnutrition (Citation26, Citation27). As a result, nutrition guidelines in most LMICs focus on children under 5, due to the increased risk of morbidity and mortality in this age group (Citation27, Citation28). Children who are older than 5 years but have significant comorbidities like cancer are typically not stratified as a high risk group in most national nutrition guidelines (Citation27–29).
This study aims to describe the burden of malnutrition among children with cancer, stratified by age, and evaluates its association with mortality in a resource-limited setting. Such information has the potential to influence policy making in LMICs regarding the incorporation of all children with cancer, regardless of their age, into national nutritional programmes.
Methods
Study Design, Setting, and Data Collection
This was a single-center, retrospective cohort study of children aged less than 19 years, who were diagnosed with cancer at the Pediatric Hematology-Oncology Unit at Kamuzu Central Hospital in Lilongwe, Malawi. Patients were included if they were newly diagnosed between January 2016 and December 2018 and had documented anthropometric measures (weight, height, and Mid-Upper Arm Circumference (MUAC)) at the time of diagnosis. These anthropometric measures were obtained as part of routine clinical care by trained members of the clinical team. Cancer diagnoses were grouped into three categories: (1) Leukemias (acute lymphoblastic leukemia, acute myeloid leukemia, and chronic myeloid leukemia), (2) Lymphomas (Hodgkin and non-Hodgkin lymphomas), and (3) Solid cancers (Wilms tumor, retinoblastoma, sarcomas, neuroblastoma, and other rare non-hematological cancers). Patients with secondary cancers were excluded. Physical charts and database entries were reviewed to obtain this information.
Definition of Malnutrition
Malnutrition was defined and classified according to both World Health Organization (WHO) and Guidelines for Community-Based Management of Acute Malnutrition (CMAM) in Malawi (Citation28–30). This included children aged < 5 years with regards to moderate acute malnutrition (MAM), weight for height (W/H) or weight for age (W/A) ≤-2 SD but > −3 SD and/or MUAC > 11.5 cm but < 12.5 cm and for severe acute malnutrition (SAM), W/H or W/A ≤ −3 SD and/or MUAC ≤ 11.5 cm. For children aged 5–9, MAM was defined as W/A or Body Mass Index (BMI) ≤ −2 SD but > -3SD and/or MUAC > 13 but < 15.5 cm and for SAM, W/A or BMI ≤ −3 SD and/or MUAC ≤13 cm. For children ≥ 10 years, MAM was defined as BMI ≤ −2 SD but > -3SD and/or MUAC > 16 but ≤18.5 cm and for SAM, BMI ≤ -3SD and/or MUAC ≤16 cm. In cases where there was discordance between the different anthropometric measure, we used the anthropometric measure that identified worse malnutrition. Patients with MAM or SAM were defined as having acute malnutrition.
Nutrition Support
Nutrition support was provided by the nutrition unit based on the national standards in conformity with United Nations Children’s Fund (UNICEF) and WHO recommendations incorporated into the Malawian nutrition guideline for children (Citation28). Patients with SAM received nutritified milk such as F-75 and F-100 and Ready-to-Use-Therapeutic-Food (RUTF). RUTF was continued for patients during admission with MAM through donations made to the department (Citation21). In addition to the twice daily hospital meals, once a day fortified porridge along with extra milk, eggs, and vegetables were also provided through donations.
Statistical Analysis
Patient characteristics were summarized using descriptive statistics. A bivariate analysis using X2 test was conducted to compare the difference between categorical variables (Citation31). A one year overall survival, calculated from the date of enrollment into the to death was estimated using Kaplan-Meier methods (Citation31). Patients were censored at the time of their last visit and those transferred to other health facilities or did not follow up after a minimum of 3 mo, from the date of diagnosis were included to the last follow-up date (Citation32) Univariate and Multivariate Cox proportional hazards method were used to test for significance of covariates on risk of mortality by calculating hazard ratios. Only covariates with p-values ≤ 0.5 on univariate analysis were included in the multivariate analysis. All analyses were made at 95% confidence intervals (CI) and a p-value < 0.05 was considered statistically significant. All statistical analyses were performed using Stata® (STATA Corp. LP, Texas, USA) version 14.
Ethical Statement
Ethical approval for use of institutional retrospective data for research was granted by the National Health Science Research Commission of Malawi: approval number 740 and Baylor College of Medicine Houston, Texas: ID H-27755.
Results
Baseline Characteristics of Patients
Out of 599 patients with primary cancer diagnoses in the stipulated period, 135 (22.5%) were excluded either due to missing files (n = 57) or because they lacked documentation of anthropometric measurements at the time of diagnosis (n = 79). A total of 463 patients were included in this analysis. The median age at diagnosis was 6 years (IQR 3–10 years). The majority of the patients (63.5%) were ≥ 5 years of age (63.5%). Males comprised 58.3% of patients in the cohort. The most common diagnoses were solid tumors (48.0%, n = 222), followed by lymphomas (34.5%, n = 160) and leukemias (17.5%, n = 81). Patient demographics and characteristics are displayed in .
Table 1. Baseline characteristics of children with cancer in Malawi stratified according to nutritional status.
Nutritional Status
Anthropometry
The following anthropometric measures were available to evaluate nutrition status: MUAC (73.4%, n = 340), W/A in children (81.9%, n = 378), W/H and/or BMI (63.0%, n = 292). A diagnosis of acute malnutrition (MAM & SAM) based on W/A alone was found in 27.5% (n = 104/378) of the children,and W/H and/or BMI 30.5% (n = 89/292) or MUAC alone in 70.6% (240/340) respectively. Results are outlined in .
Table 2. Anthropometry results Abbreviations: MAM: Moderate acute malnutrition, SAM: Severe acute malnutrition, MUAC; mid-upper arm circumference, BMI: Body Mass index.
Prevalence of Acute Malnutrition
Acute malnutrition was identified in 63.3% (n = 293) of patients; 23.1% (n = 107) and 40.2% (n = 186) had MAM and SAM, respectively. Additionally, it was present among 67.9% (55/81) of patients with leukemia, 68.1% (109/160) of patients with lymphoma, and 58.1% (129/222) of patients with solid malignancies; p = 0.09 (). Children ≥ 5 years presented more often with acute malnutrition in respectively 70.0% (206/294) compared to 51.5% (87/169) for children < 5 years of age; p < 0.0001. The distribution for children with MAM was 27.2% (46/169) for children <5 years and 20.7% (61/294) for children > 5 years; p = 0.12. For children with SAM aged < 5 years, this was 24.2% (41/169), vs. 49.3% (145/294) for those ≥ 5 years of age; p < 0.001 ().
Mortality and Factors Associated with Mortality
During the 1-year follow-up period, 162 (35.0%) patients died. The median time to death was 102 day (IQR: 19–212). A total of 30 patients (6.4%) did not follow-up (LTFU) and 5 patients (1.1%) were transferred to other health facilities. The 1-year OS was 53% (95%CI 47%–58%) for the entire cohort. In a multivariate analysis, age < 5 years (HR 1.6; 95%CI 1.1–2.3, p = 0.016) and SAM (HR 1.6, 95%CI 1.1–2.3, p = 0.012) were associated with increased risk of mortality ().
Discussion
We demonstrate a high prevalence of malnutrition among pediatric patients newly diagnosed with cancers in Malawi. The majority (63%) of children were malnourished at the time of cancer diagnosis. Children aged 5 years or older had a higher prevalence of malnutrition, including SAM. Children aged less than 5 years was associated with higher mortality, in addition to SAM.
In LMICs, children under 5 years are at higher risk for malnutrition and have an increased mortality risk from treatable causes such as pneumonia and malaria (Citation40). Hence, national and international nutrition guidelines, based on WHO recommendations, for children in LMIC primarily focus on nutritional interventions for children under the age of 5 (Citation24–26, Citation28). Notably, in our cohort, there was a higher proportion of acute malnutrition in children older than 5 years. This was of great significance as these children are not prioritized in malnutrition guidelines in many LMICs and thefore nutrition support can not always been given. Secondly, guidelines include products such as F75, F100 and Ready-to Use Therapeutic Food (RUTF). These products are developed for children < 5 years of age in LMIC’s and might not be suitable for older children, as for example big amounts of F75,100 or RUTF need to be taken to adres an adequate nutritional and calorical intake. This observation necessitates advocacy for the incorporation of a robust nutritional assessment and intervention scheme in national health guidelines for pediatric oncology programs, regardless of a child’s age. Arguably, the same protections should be extended to older children with other chronic illnesses besides cancer, who are similarly at risk for malnutrition.
Table 3. Univariate and multivariate analysis of factors associated with overall survival among children with cancer in Malawi. Reference variables in this regression model were Male gender, Age under 5 years, Leukemia and No malnutrition. Abbreviations: MAM: Moderate acute malnutrition, SAM: Severe acute malnutrition, HR: Hazard Ratio, CI: Confidence Interval. * No malnutrition is the comparison group.
The prevalence of malnutrition at our center was greater than other published literature from other sites in southern Malawi (34–55%) (Citation14, Citation21, Citation32, Citation33). This may be explained by a higher predisposition of malnutrition due to food insecurity in the northern and central region compared to the southern region (Citation34). Similarly, data from other African countries have equally reported a high burden of malnutrition in cohorts of children with various cancers, regardless of the diagnosis (Citation22, Citation35–37). There is a tendency toward higher rates of malnutrition among patients with advanced diseases across all cancer types, which has also been reported in high‐income countries and thought to be attributed to the disease burden (Citation38). Unfortunately, in our cohort, this data was not consistently available due to inherent inavailability of imaging modalities such as computed tomography or in the case of leukemias, risk-stratification based on cytogenetics. However it is likely that preexisting suboptimal nutrition status and advanced disease presentation contributed to the high burden of malnutrition in our cohort (Citation39).
Cancer-associated malnutrition is unique in its complexity as it is driven by both reduced intake and excessive catabolic changes arising from high tumor burden and biology (Citation10, Citation11). Hence, specific attention should be provided on training of healthcare workers who care for pediatric oncology patients in LMICs and on best practices to ensure that nutritional needs are adequately addressed. As we demonstrated in our cohort, there was a clear under-detection of acute malnutrition if solely relying on the use of weight for age, weight for height or BMI alone without MUAC. In children with cancer, the use of weight as an anthropometric tool can often be misleading as it may erroneously reflect tumor mass. Furthermore, in these patients, a reduction of weight with therapy may not necessarily be indicative of failure of nutritional interventions (Citation41). Hence, experts have argued that the use of MUAC, arm muscle area, or triceps skinfold thickness to assess malnutrition may provide a more accurate assessment, particularly in LMICs, where the majority of patients present with advanced or bulky disease (Citation22, Citation33). Although we used MUAC in over 70% of the cases, in this scenario, the use of MUAC alone would have been optimal. Future prospective studies must take this into account. MUAC for children under 5 years of age is widely accepted as a validated tool (Citation29). MUAC z-score in children above five is less studied but validated for mortality (Citation30, Citation42). As a result, they are implemented in the WHO Integrated Management of Adolescent and Adult Illness (IMAI) guidelines and required by several national guidelines in LMICs, like in Malawi (Citation28, Citation30). The differences in MUAC validation among children above and below 5 years of age show the direct need for additional research with regards to optimal nutritional assessment in children above 5 years of age with severe malnutrition and cancer.
Our retrospective analysis has a number of limitations. A significant percentage of patients (22.7%) had to be excluded due to missing files and/or lack of anthropometric measurements and it can be argued that antropometrics were more likely to be recorded if they were suboptimal, however it is unknown whether these excluded patients would represent a similar distribution pattern of malnutrition as those who were included in the study. Secondly, while the same measurement assessment tools were consistently used by Malawian trained medical docters, a trained nutrionist consistently taking measurements was only available in the last year of the study period, and potential inter-observer errors might have occurred. Additionally, the different diagnoses were not stratified based on stage or risk groups and/or tumor burden – factors that may likely inform mortality regardless of nutritional status. Future prospective study is needed to minimize these biases and further examine the effect of targeted nutritional supplementation on treatment-related morbidity and mortality in this specific population. Nonetheless, our characterization of the significant burden of acute malnutrition among childhood cancer, demonstrating significant risk to all age groups provides critical data to motivate changes in national and international malnutrition guidelines – specifically so that children above 5 years with childhood cancer and chronic conditions are also supported.
Conclusion
There is a significant burden of malnutrition in children with cancer in low-resource settings, regardless of age. Adoption of coordinated nutrition assessments, interventions, and monitoring regardless of age are critical in pediatric oncology units across LMICs. Malnutrition guideluines in LMICs currently focus on children under the age of 5. National and international nutritional policies and guidelines in LMICs should be framed to be inclusive of pediatric oncology patients regardless of age to have access to nutritional support. Additional prospective investigations are of extreme importance to inform best practices for nutritional rehabilitation and treatment modifications in malnourished patients with cancer in LMICs.
Author Responsibilities
The authors’ responsibilities were as follows – WW, IM, SM, KW,GM, AS, and MH were involved in data collection; GM, AS, and MH were involved in data cleaning, performed the data analysis, and wrote the manuscript; WW, IM, SM, KW, PM, and NO revised the manuscript; NO and MH had primary responsibility for final content; and all authors read and approved the final manuscript.
Acknowledgments
The authors wish to thank the patients and the clinical, nursing, and administrative team at Kamuzu Central Hospital, Pediatric Hematology Oncology Unit, and the Texas Children’s Hospital Global Hematology Oncology Pedatric Excellence (HOPE) program for funding the operations of this unit.
Conflict of Interest
The authors declare that there is no conflict of interest.
Funding
The author(s) reported there is no funding associated with the work featured in this article.
Correction Statement
This article has been republished with minor changes. These changes do not impact the academic content of the article.
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