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The Role of Reticulocyte Hemoglobin Content in Diagnosing Iron Deficiency in Childhood Cancer
CC BY 4.0 · Indian J Med Paediatr Oncol 2024; 45(05): 396-401
DOI: DOI: 10.1055/s-0044-1779047
Abstract
Background The prevalence of iron deficiency (ID) and iron deficiency anemia (IDA) in children with cancer is not well studied. The detection of ID and IDA using sensitive laboratory tools may facilitate early diagnosis and treatment in this cohort. In this regard, reticulocyte hemoglobin (Ret-He) content serves as a cost-effective measurement that remains unaffected by inflammation, unlike the ferritin test.
Aim The objective of this study is to analyze the role of Ret-He as a diagnostic tool to identify functional and absolute ID and IDA in children with cancer.
Methods We conducted a cross-sectional study in children aged 0 to 18 years. Blood samples were collected to compare Ret-He values with iron status, reflected by hemoglobin (Hb), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), serum iron (SI), total iron binding capacity (TIBC), and ferritin and transferrin saturation. The overall discriminative power of Ret-He in detecting ID and IDA was assessed using receiver operating characteristic analysis.
Results Of the 135 children included in the study, 58 (43.0%) had anemia. Among them, 20 (14.8%) had IDA (8 [5.9%] absolute and 12 [8.9%] functional), while 25 (18.5%) had ID (16 [11.9%] absolute and 9 [6.7%] functional). The Ret-He value was significantly related to iron status (p ≤ 0.002). Ret-He was also shown to have a significant correlation with the abovementioned hematological parameters (p = 0.000), except TIBC. Multivariate analysis revealed a significant relationship between Hb (p = 0.051), MCH (p = 0.000), and MCHC (p = 0.001) and Ret-He. Ret-He values of 33.7, 32.7, 32.4 and 28.6 pg were established as optimal cut-off values to identify functional ID, absolute ID, functional IDA, and absolute IDA, respectively.
Conclusion Ret-He is a reliable diagnostic tool for absolute and functional IDA in children with cancer.
Keywords
absolute ID - absolute IDA - childhood cancer - functional ID - functional IDA - hemoglobin - Ret-HePatient Consent
Patient consent was obtained from every subject.
Supplementary Material
Publication History
Article published online:
21 March 2024
© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
Thieme Medical and Scientific Publishers Pvt. Ltd.
A-12, 2nd Floor, Sector 2, Noida-201301 UP, India
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Abstract
Background The prevalence of iron deficiency (ID) and iron deficiency anemia (IDA) in children with cancer is not well studied. The detection of ID and IDA using sensitive laboratory tools may facilitate early diagnosis and treatment in this cohort. In this regard, reticulocyte hemoglobin (Ret-He) content serves as a cost-effective measurement that remains unaffected by inflammation, unlike the ferritin test.
Aim The objective of this study is to analyze the role of Ret-He as a diagnostic tool to identify functional and absolute ID and IDA in children with cancer.
Methods We conducted a cross-sectional study in children aged 0 to 18 years. Blood samples were collected to compare Ret-He values with iron status, reflected by hemoglobin (Hb), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), serum iron (SI), total iron binding capacity (TIBC), and ferritin and transferrin saturation. The overall discriminative power of Ret-He in detecting ID and IDA was assessed using receiver operating characteristic analysis.
Results Of the 135 children included in the study, 58 (43.0%) had anemia. Among them, 20 (14.8%) had IDA (8 [5.9%] absolute and 12 [8.9%] functional), while 25 (18.5%) had ID (16 [11.9%] absolute and 9 [6.7%] functional). The Ret-He value was significantly related to iron status (p ≤ 0.002). Ret-He was also shown to have a significant correlation with the abovementioned hematological parameters (p = 0.000), except TIBC. Multivariate analysis revealed a significant relationship between Hb (p = 0.051), MCH (p = 0.000), and MCHC (p = 0.001) and Ret-He. Ret-He values of 33.7, 32.7, 32.4 and 28.6 pg were established as optimal cut-off values to identify functional ID, absolute ID, functional IDA, and absolute IDA, respectively.
Conclusion Ret-He is a reliable diagnostic tool for absolute and functional IDA in children with cancer.
Keywords
absolute ID - absolute IDA - childhood cancer - functional ID - functional IDA - hemoglobin - Ret-He
Introduction
Children suffering from chronic diseases, such as cancer, are more susceptible to both iron deficiency (ID) and iron deficiency anemia (IDA). A study conducted by the European Cancer Anemia Survey (ECAS) revealed that 39%- of children with cancer were anemic at the study's onset. This value increased to 67%- after chemotherapy. Moreover, 42%- were identified as iron deficient.[1] [2]
Anemia in cancer patients can arise from factors like malnutrition, malabsorption, chronic inflammation, bleeding, therapy-induced myelosuppression, bone marrow infiltration, hemolysis, hypersplenism, and ID. The disrupted iron homeostasis and metabolism in cancer patients are primarily due to chronic inflammation, which leads to iron sequestration in macrophages, causing limited iron availability for red blood cell production in the bone marrow.[3] [4]
IDA can adversely affect physical performance, leading to general weakness and fatigue and potentially reducing the effectiveness of chemotherapy/radiotherapy against tumors.[3] Thus, the early detection of ID is crucial to address it with simple treatments like iron supplementation or erythropoietin and limit the need for packed red cell transfusion in cancer patients.
Although the gold-standard diagnostic tool for ID is bone marrow staining with Prussian blue, this method is invasive and expensive.[5] In 2010, the American Academy of Pediatrics (AAP) stated that ID can be diagnosed by evaluating ferritin and c-reactive protein levels or measuring reticulocyte hemoglobin (Ret-He), with low hemoglobin levels indicating IDA.[6] However, ferritin is an acute-phase protein that can increase under inflammatory conditions, including malignancy. The European Society for Medical Oncology (ESMO) guidelines define ID in cancer patients as ferritin levels <100 href="https://www.thieme-connect.com/products/ejournals/html/10.1055/s-0044-1779047#JR23561160-3" xss=removed>3] [5]
In recent years, the potential of Ret-He content as an early marker for ID has been highlighted. Reticulocytes are immature erythrocytes released from the bone marrow that can reflect the erythropoiesis status over the preceding 3 to 4 days.[7] [8] Unlike ferritin, Ret-He is not influenced by inflammation as it is not an acute-phase protein.[6] [9] The hemoglobin content in reticulocytes can be assessed through measures such as Ret-He content (CHr or Ret-He), both utilizing flow cytometry and reported in picograms.[8] [10] [11] The Ret-He laboratory test can be performed alongside routine blood tests without the need for additional blood samples.[9] [12]
Research to determine the optimal Ret-He cut-off values for ID and IDA in pediatrics, particularly pediatric cancer patients is ongoing.[12] [13] [14] In this study, we investigated the diagnostic value of Ret-He in identifying ID and IDA in children with cancer to facilitate the simple detection of these conditions.
Materials and Methods
Subjects
A cross-sectional study was conducted in Cipto Mangunkusumo Hospital from March to June 2021. Hospitalized and outpatient children aged 0 to 18 years with cancer were selected as participants. Patients with a history of iron therapy or blood transfusion in the past month were excluded. Written consent and assent were obtained from the subjects' parents or legal guardians and adolescent patients.
Inclusion and Exclusion Criteria
The inclusion criteria for this study comprised children between the ages of 0 and 18 years with cancer who were either hospitalized or received outpatient treatment. Patients who received iron therapy or blood transfusion within the past month were excluded. No oral iron therapy was initiated for IDA patients.
Laboratory Methods
Venous blood samples (6 mL) were obtained from the subjects. Iron parameters, including hemoglobin (Hb), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), reticulocyte hemoglobin (Ret-He), ferritin, serum iron (SI), and total iron binding capacity (TIBC), were measured via standard techniques. TS was calculated using the formula SI/TIBC × 100. All parameters were analyzed in the Clinical Pathology Laboratory of Cipto Mangunkusumo Hospital.
Iron Status Definition
The World Health Organization defines anemia as a low Hb value according to age: Hb <11 href="https://www.thieme-connect.com/products/ejournals/html/10.1055/s-0044-1779047#BR23561160-15" xss=removed>15] In this study, ESMO criteria were used to evaluate iron status in children: (1) absolute IDA with low Hb and ferritin <100 href="https://www.thieme-connect.com/products/ejournals/html/10.1055/s-0044-1779047#JR23561160-16" xss=removed>16]
Primary and Secondary Outcomes
The primary outcome of this study was the establishment of optimal Ret-He cut-off values for different types of absolute and functional ID or IDA, with their respective sensitivities, specificities, and predictive values. The secondary outcome was the evaluation of iron status in children with cancer, including the prevalence of ID and IDA. Laboratory indices, such as Hb, MCV, MCH, MCHC, SI, ferritin and TS, and their relationship with Ret-He, were also analyzed.
Statistical Analysis
The correlation between iron status and Ret-He was determined with analysis of variance (ANOVA) or the Kruskal–Wallis test, depending on the data distribution. Normality was assessed using the Kolmogorov–Smirnoff test. ANOVA with Tukey's post-hoc analysis was performed. Ret-He was also compared with other laboratory parameters through correlation analysis using the Pearson and nonparametric Spearman methods. Significant variables were subsequently subjected to multivariate analysis using linear regression. The overall discriminative power of Ret-He to detect iron depletion, ID, and IDA was assessed using receiver operating characteristic (ROC) analysis. Cut-off values were determined for each iron status using Youden's index, where (sensitivity + specificity) –1 had the highest value. A p-value of <0>
Ethics
The Ethics Committee of the Faculty of Medicine, University of Indonesia, Cipto Mangunkusumo Hospital, approved this study (No. KET-1010/UN2.F1/ETIK/PPM.00.02/2020) on September 14, 2020. This study did not involve any animals. All the research methods involving humans were performed according to the ethical guidelines established by the responsible committee overseeing human experimentation at the institutional and national levels. They also complied with the 1975 Helsinki Declaration, updated in 2013.
Results
A total of 146 children were initially included in this study. Eleven subjects had incomplete data and were excluded; thus, the final study population comprised 135 children ([Supp. Fig. 1]). The characteristics of these subjects are shown in [Table 1].
|
Characteristics |
Frequency (n) |
Percentage (%) |
|---|---|---|
|
Gender |
||
|
Male |
75 |
55.6 |
|
Female |
60 |
44.4 |
|
Age (years), mean ± SD, median (IQR) |
8.4 ± 4.7 |
7 (8) |
|
Cancer type |
||
|
ALL |
74 |
54.8 |
|
AML |
7 |
5.2 |
|
CML |
9 |
6.7 |
|
Lymphoma |
6 |
4.4 |
|
Solid cancer |
39 |
28.9 |
|
Normal (n = 52) |
Functional ID (n = 9) |
Absolute ID (n = 16) |
Functional IDA (n = 12) |
Absolute IDA (n = 8) |
p-Value |
|
|---|---|---|---|---|---|---|
|
Hb |
13.00 ± 0.96 |
12.33 ± 0.86 |
12.58 ± 1.45 |
10.09 ± 1.16 |
10.44 ± 1.37 |
<0> |
|
MCV |
85.48 (75–96) |
80.39 (75–87) |
77.43 (60–85) |
84.03 (78–97) |
80.05 (71–85) |
0.000 |
|
MCH |
29.85 (25–34) |
27.80 (25–30) |
27.40 (19–30) |
27.90 (26–33) |
27.60 (20–29) |
<0> |
|
MCHC |
34.75 ± 1.30 |
34.29 ± 0.93 |
34.05 ± 1.28 |
33.93 ± 1.17 |
32.64 ± 2.19 |
0.001 |
|
Ret-He |
34 (26–38) |
32.5 (27–36) |
31.2 (20–35) |
31.50 (17–36) |
30 (19–36) |
<0 href="#FN23561160-4" class="alt">a] |
|
Ferritin |
709.55 (113–96,773) |
191.03 (111–5,039) |
38.35 (11–95) |
716.79 (187–3,483) |
14.68 (1–81) |
0.79 |
|
SI |
93.5 (40–291) |
39 (9–54) |
73.5 (24–132) |
29.5 (10–52) |
45 (19–82) |
<0 href="#FN23561160-4" class="alt">a] |
|
TS |
40 (21–92) |
17 (9–18) |
23 (10–40) |
15 (5–20) |
14.5 (6–26) |
<0 href="#FN23561160-4">a] |
|
TIBC |
238 (101–258,000) |
231 (103–326) |
315 (247–389) |
214.5 (168–310) |
330 (193–382) |
0.93 |
|
Parameters |
Correlation coefficient |
Sig. (2-tailed) |
|---|---|---|
|
Hb[a] |
0.431 |
0.000 |
|
MCV |
0.474 |
0.000 |
|
MCH |
0.627 |
0.000 |
|
MCHC[a] |
0.668 |
0.000 |
|
SI |
0.489 |
0.000 |
|
TIBC |
−0.76 |
0.460 |
|
Transferrin |
0.540 |
0.000 |
|
Ferritin |
0.443 |
0.000 |
|
Unstandardized coefficients |
Standardized coefficients |
t |
Sig. |
|||
|---|---|---|---|---|---|---|
|
B |
Standard error |
Beta |
||||
|
Ret-He |
Hb |
0.392 |
0.198 |
0.154 |
1.983 |
0.051 |
|
MCV |
0.009 |
0.030 |
0.025 |
0.313 |
0.755 |
|
|
MCH |
0.642 |
0.166 |
0.427 |
3.878 |
0.000 |
|
|
MCHC |
0.841 |
0.243 |
0.315 |
3.466 |
0.001 |
|
|
SI |
0.007 |
0.11 |
0.101 |
0.599 |
0.551 |
|
|
TIBC |
−7.131E − 007 |
0.000 |
−0.005 |
−0.072 |
0.943 |
|
|
Transferrin |
−0.006 |
0.028 |
−0.040 |
−0.231 |
0.818 |
|
|
Ferritin |
−1.703E − 005 |
0.000 |
−0.043 |
−0.637 |
0.526 |
|
|
Parameter |
AUC |
Cut-off |
Sensitivity |
Specificity |
p-Value |
|||
|---|---|---|---|---|---|---|---|---|
|
Functional ID |
||||||||
|
72.4% |
33.7[a] |
88.9 |
55.8 |
0.033 (0.54 − 0.91) |
||||
|
33.65 − 34.65 |
88.9 |
32.7 − 55.8 |
||||||
|
28.4 − 30.25 |
22 − 33 |
90.4 − 98.1 |
||||||
|
Absolute ID |
||||||||
|
77.8% |
32.7[a] |
81.3 |
73.1 |
0.001 (0.65 − 0.91) |
||||
|
33.4 − 34.05 |
81.3 − 87.5 |
44.2 − 57.7 |
||||||
|
27.85 − 30.25 |
31.3 − 37.5 |
90.4 − 98.1 |
||||||
|
Functional IDA |
||||||||
|
69.7% |
32.4[a] |
66.7 |
75.0 |
0.034 (0.50 − 0.89) |
||||
|
34.55 − 35.25 |
83.3 |
21.2 − 36.5 |
||||||
|
27.85 − 30.25 |
25 − 41.7 |
90.4 − 98.1 |
||||||
|
Absolute IDA |
||||||||
|
73.1% |
28.6[a] |
50.0 |
98.1 |
0.037 (0.50 − 0.97) |
||||
|
35 − 35.25 |
87.5 |
21.2 − 26.9 |
||||||
|
27.25 − 30.25 |
37.5 − 50 |
90.4 − 98.1 |
||||||
- Ludwig H, Van Belle S, Barrett-Lee P. et al. The European Cancer Anaemia Survey (ECAS): a large, multinational, prospective survey defining the prevalence, incidence, and treatment of anaemia in cancer patients. Eur J Cancer 2004; 40 (15) 2293-2306
- Ludwig H, Müldür E, Endler G, Hübl W. Prevalence of iron deficiency across different tumors and its association with poor performance status, disease status and anemia. Ann Oncol 2013; 24 (07) 1886-1892
- Abiri B, Vafa M. Iron deficiency and anemia in cancer patients: the role of iron treatment in anemic cancer patients. Nutr Cancer 2019; 0 (00) 1-9
- Naoum FA. Iron deficiency in cancer patients. Rev Bras Hematol Hemoter 2016; 38 (04) 325-330
- Uçar MA, Falay M, Dağdas S, Ceran F, Urlu SM, Özet G. The importance of RET-He in the diagnosis of iron deficiency and iron deficiency anemia and the evaluation of response to oral iron therapy. J Med Biochem 2019; 38 (04) 496-502
- Baker RD, Greer FR, Bhatia JJS. et al; Committee on Nutrition American Academy of Pediatrics. Diagnosis and prevention of iron deficiency and iron-deficiency anemia in infants and young children (0–3 years of age). Pediatrics 2010; 126 (05) 1040-1050
- Peerschke EIB, Pessin MS, Maslak P. Using the hemoglobin content of reticulocytes (RET-He) to evaluate anemia in patients with cancer. Am J Clin Pathol 2014; 142 (04) 506-512
- Elghetany MT, Schexneider KI. Erythrocytic disorder. In: McPherson RA, Pincus MR. ed. Henry's Clinical Diagnosis and Management by Laboratory Methods. 23rd ed. Missouri:: Elsevier; 2017: 562
- Toki Y, Ikuta K, Kawahara Y. et al. Reticulocyte hemoglobin equivalent as a potential marker for diagnosis of iron deficiency. Int J Hematol 2017; 106 (01) 116-125
- Thomas L, Franck S, Messinger M, Linssen J, Thomé M, Thomas C. Reticulocyte hemoglobin measurement–comparison of two methods in the diagnosis of iron-restricted erythropoiesis. Clin Chem Lab Med 2005; 43 (11) 1193-1202
- Brugnara C, Schiller B, Moran J. Reticulocyte hemoglobin equivalent (Ret He) and assessment of iron-deficient states. Clin Lab Haematol 2006; 28 (05) 303-308
- Andriastuti M, Adiwidjaja M, Satari HI. Diagnosis of iron deficiency and iron deficiency anemia with reticulocyte hemoglobin content among children aged 6–18 years. Iran J Blood Cancer 2019; 11 (04) 127-132
- Lorenz L, Arand J, Büchner K. et al. Reticulocyte haemoglobin content as a marker of iron deficiency. Arch Dis Child Fetal Neonatal Ed 2015; 100 (03) F198-F202
- Rungngu SLP, Wahani A, Mantik MFJ. Reticulocyte hemoglobin equivalent for diagnosing iron deficiency anemia in children. Paediatr Indones 2016; 56 (02) 90
- World Health Organization. Iron deficiency anaemia: assessment, prevention and control, a guide for program managers. Geneva: World Health Organization; 2001: 1-114
- Aapro M, Beguin Y, Bokemeyer C. et al. Management of anaemia and iron deficiency in patients with cancer: ESMO Clinical Practice Guidelines. Ann Oncol 2018; 29 (February): 96-110
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References
Address for correspondence
Publication History
Article published online:
21 March 2024
© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)
Thieme Medical and Scientific Publishers Pvt. Ltd.
A-12, 2nd Floor, Sector 2, Noida-201301 UP, India
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- Ludwig H, Van Belle S, Barrett-Lee P. et al. The European Cancer Anaemia Survey (ECAS): a large, multinational, prospective survey defining the prevalence, incidence, and treatment of anaemia in cancer patients. Eur J Cancer 2004; 40 (15) 2293-2306
- Ludwig H, Müldür E, Endler G, Hübl W. Prevalence of iron deficiency across different tumors and its association with poor performance status, disease status and anemia. Ann Oncol 2013; 24 (07) 1886-1892
- Abiri B, Vafa M. Iron deficiency and anemia in cancer patients: the role of iron treatment in anemic cancer patients. Nutr Cancer 2019; 0 (00) 1-9
- Naoum FA. Iron deficiency in cancer patients. Rev Bras Hematol Hemoter 2016; 38 (04) 325-330
- Uçar MA, Falay M, Dağdas S, Ceran F, Urlu SM, Özet G. The importance of RET-He in the diagnosis of iron deficiency and iron deficiency anemia and the evaluation of response to oral iron therapy. J Med Biochem 2019; 38 (04) 496-502
- Baker RD, Greer FR, Bhatia JJS. et al; Committee on Nutrition American Academy of Pediatrics. Diagnosis and prevention of iron deficiency and iron-deficiency anemia in infants and young children (0–3 years of age). Pediatrics 2010; 126 (05) 1040-1050
- Peerschke EIB, Pessin MS, Maslak P. Using the hemoglobin content of reticulocytes (RET-He) to evaluate anemia in patients with cancer. Am J Clin Pathol 2014; 142 (04) 506-512
- Elghetany MT, Schexneider KI. Erythrocytic disorder. In: McPherson RA, Pincus MR. ed. Henry's Clinical Diagnosis and Management by Laboratory Methods. 23rd ed. Missouri:: Elsevier; 2017: 562
- Toki Y, Ikuta K, Kawahara Y. et al. Reticulocyte hemoglobin equivalent as a potential marker for diagnosis of iron deficiency. Int J Hematol 2017; 106 (01) 116-125
- Thomas L, Franck S, Messinger M, Linssen J, Thomé M, Thomas C. Reticulocyte hemoglobin measurement–comparison of two methods in the diagnosis of iron-restricted erythropoiesis. Clin Chem Lab Med 2005; 43 (11) 1193-1202
- Brugnara C, Schiller B, Moran J. Reticulocyte hemoglobin equivalent (Ret He) and assessment of iron-deficient states. Clin Lab Haematol 2006; 28 (05) 303-308
- Andriastuti M, Adiwidjaja M, Satari HI. Diagnosis of iron deficiency and iron deficiency anemia with reticulocyte hemoglobin content among children aged 6–18 years. Iran J Blood Cancer 2019; 11 (04) 127-132
- Lorenz L, Arand J, Büchner K. et al. Reticulocyte haemoglobin content as a marker of iron deficiency. Arch Dis Child Fetal Neonatal Ed 2015; 100 (03) F198-F202
- Rungngu SLP, Wahani A, Mantik MFJ. Reticulocyte hemoglobin equivalent for diagnosing iron deficiency anemia in children. Paediatr Indones 2016; 56 (02) 90
- World Health Organization. Iron deficiency anaemia: assessment, prevention and control, a guide for program managers. Geneva: World Health Organization; 2001: 1-114
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