Undernutrition in Nepalese children: a biochemical and haematological study

REGULAR ARTICLE

Undernutrition in Nepalese children: a biochemical and haematologicalstudyArijit Ghosh1,*, Sutanu Dutta Chowdhury2, Tusharkanti Ghosh ([email protected])2

1.Department of Clinical Physiology, Nepal Medical College, Kathmandu, Nepal2.Department of Physiology, University of Calcutta, Kolkata, West Bengal, India

KeywordsNutritional status, Serum albumin, Serum ferritin,Serum iron, Undernutrition

CorrespondenceTushar K. Ghosh, Department of Physiology, Univer-sity of Calcutta, Kolkata 700009, West Bengal, India.Tel: 91 033 2350 8386 Extn. 220 |Fax: 91-033-2351-9755 |Email: [email protected]

Received25 September 2011; revised 30 November 2011;accepted 20 January 2012

DOI:10.1111/j.1651-2227.2012.02613.x

*Present address: Department of Endocrinology andMetabolism, Medical University of Graz, Austria.

ABSTRACTAim: This study was undertaken to assess the nutritional status of 6–10 years old

Nepalese children by measuring some haematological and biochemical parameters.Methods: Nutritional status was assessed by height-for-age z-score. Total count of

red blood corpuscles (TC of RBC), packed cell volume, haemoglobin concentration, mean

corpuscular volume (MCV), mean corpuscular haemoglobin (MCH) and mean corpuscular

haemoglobin concentration were measured. Biochemical parameters such as serum iron,

total iron-binding capacity (TIBC), serum ferritin, serum transferrin, transferrin saturation

(TS) and serum albumin were also measured. Serum folate and vitamin B12 were mea-

sured in well-nourished and undernourished children.Results: TC of RBC, serum iron, serum ferritin, TS and serum albumin of stunted chil-

dren were significantly lower (p < 0.05) than that of well-nourished children. MCV, MCH,

TIBC and serum transferrin of stunted children were significantly higher (p < 0.05) than

that of well-nourished children. Serum folate and vitamin B12 values of stunted children

were significantly lower (p < 0.001) than that of well-nourished children.Conclusion: A mild iron deficiency was found in stunted Nepalese children. The

serum ferritin has been identified as a sensitive marker for measurement of iron status in

surveyed children. A deficiency of serum protein, serum folate and vitamin B12 was also

found in the undernourished Nepalese children.

INTRODUCTIONUndernutrition has been found to be a serious health prob-lem in Nepalese children. The study carried out two dec-ades ago in Terai region revealed a higher percentage(65%) of stunting in Nepalese children (1). Another investi-gation among Nepalese children aged 5–12 years demon-strated their poor nutritional status (2). Survey report onglobal child undernutrition stated that undernutrition isone of the major health problems in Nepal and more than40% children are suffering from undernutrition (3). Inrecent times, the nutritional status of Nepalese children hasbeen measured on the basis of their height and weight mea-surements, and a high prevalence of undernutrition hasbeen reported (4).

Biochemical tests provide the most objective and quanti-tative data on nutritional status. It has been opined thatnutritional inadequacy is first indicated by biochemicalchanges, then impairments occur in cell or organ and finallyclinical malnutrition is established (5). Measurement of ironstatus has been recognized as a stronger biochemical toolfor nutritional assessment. It is employed to detect the nutri-tional anaemia, most prevalent undernutritional problemamong worldwide preschool and school aged children (5).A number of parameters such as RBC count, haemoglobinconcentration (Hb%) and packed cell volume (PCV) aregenerally used as early indicators for describing differenttypes of nutritional anaemia (5). Researchers most

Abbreviations

ANOVA, One-way analysis of variance; Hb%, haemoglobin con-centration; MCH, mean corpuscular haemoglobin; MCHC, meancorpuscular haemoglobin concentration; MCV, mean corpuscu-lar volume; PCV, packed cell volume; RBC, red blood cell; SEM,standard error of mean; TC, total count; TIBC, total iron-bindingcapacity; TS, transferrin saturation.

Key notes• A mild iron deficiency was found in stunted Nepalese

children. The serum ferritin has been identified as asensitive marker for measurement of iron status in sur-veyed children. A deficiency of serum protein, serumfolate and vitamin B12 were also found in the under-nourished Nepalese children.

Acta Pædiatrica ISSN 0803–5253

ª2012 The Author(s)/Acta Pædiatrica ª2012 Foundation Acta Pædiatrica 2012 101, pp. 671–676 671

commonly assess the serum ferritin, total iron-bindingcapacity (TIBC), serum transferrin and transferrin satura-tion (TS) as confirmatory tests for diagnosis of iron-defi-ciency and iron-deficiency anaemia (6,7). In addition to theiron status, both folate and vitamin B12 measurements havebeen found as to be highly sensitive, but less specific, fornutritional assessment (8). Serum albumin has been used asan important parameter for assessing protein nutritionalstatus (9). Relationship between undernutrition and above-mentioned biochemical parameters has also been reportedin Indian children (10) and in SriLankan children (11). Inthis regard, the data from Nepal are scanty and scarce.Martorell et al. (1984) examined the low level of haemoglo-bin percentage in Nepalese children of Terai region (1).Recently, Mishra et al. (2009) (12) demonstrated signifi-cantly lower total protein and serum albumin level in under-nourished preschool children compared to well-nourishedpreschool children of Nepal. Therefore, the purpose of thisstudy was to assess the nutritional status of 6–10 years oldNepalese children by measuring some haematological andbiochemical parameters.

MATERIALS AND METHODSStudy populationA total of 192 (98 boys and 94 girls) primary school childrenof Nepali origin (aged 6–10 years) from four randomlyselected government and private schools in the Kathmanduvalley of Nepal were used for the study. Age of the childrenwas verified from the school records as well as from theparents ⁄ guardians. Children with any systemic disease,infection or with major surgical operations that could influ-ence their biochemical or haematological parameters wereexcluded from participating in the study. Approval for thisstudy was granted by the Ethical Committee of Nepal Medi-cal College, Kathmandu, Nepal.

Nutritional statusHeight of each subject was measured using anthropometricrods (Globe Surgical, Kathmandu, Nepal) following thestandard technique (5) by two trained observers. Chronicundernutrition in terms of stunting was calculated by Z-score using World Health Organization height-for-age ref-erence values (13).

Haematological and biochemical measurementsAbout 5 mL venous blood samples were obtained from eachchild for haematological and biochemical screening tests,following a 12-h overnight fast. EDTA – containing vacu-tainers – was used for the collection of whole blood samplesthat were analysed for haematological examination. Theremaining blood was collected in vacutainers with no addedanticoagulant and kept at room temperature for 30 minthen incubated at 37�C for another 30 min, as this desig-nated for serum separation. After separation of serum bycentrifugation, 1 mL aliquots were pipetted into plastic ep-pendorf tubes and stored at )80�C for biochemical assess-ments.

TC of RBC, PCV and Hb concentrationTotal count of RBC was measured in haemocytometer andPCV was calculated by standard method (14). Haemoglobinconcentration was determined by Cyanmethemoglobinmethod (15). Mean corpuscular volume (MCV), mean cor-puscular haemoglobin (MCH) and mean corpuscular hae-moglobin concentration (MCHC) were calculated.

Serum iron and TIBCSerum iron and TIBC were measured using Iron & TIBC kit(Crest Biosystems: IRT010 & IRT011, Goa, India) by Ferro-zine method (16).

Serum ferritin, serum transferrin and TSSerum ferritin was measured using DiaMetra kit (DK0039,Milano, Italy) by immunoenzymatic determination (17).Transferrin value was determined indirectly by multiplyingTIBC with 0.7 (18). Transferrin saturation was calculated bydividing serum iron with TIBC and multiplied by 100 (5).

Folic acid and vitamin B12

Folic acid and vitamin B12 were measured using commer-cially available immunoassay kit (Beckman Coulter, South-field, MI, USA: Ref. 33000) by chemiluminescence assaymethod (19,20).

Stages of iron depletionThe stage-I of iron depletion, referred to as iron deficientstores, was recognized by a serum ferritin level below12 lg ⁄ L. The stage-II of iron depletion, referred as iron defi-ciency erythropoiesis, was recognized by serum ferritin levelbelow 12 lg ⁄ L and TS level below 15%. The stage-III ofiron depletion, referred to as iron-deficiency anaemia, wasrecognized by serum ferritin level below 12 lg ⁄ L, TS levelbelow 15% and haemoglobin level below 12 g ⁄ dL (5).

Statistical analysisDescriptive statistics of height-for-age, haematological andbiochemical parameters were expressed as mean ± stan-dard error of mean (SEM). ANOVA was conducted totest for differences in biochemical and haematologicalparameters between normal statured and stunted groupsfollowed by Bonferroni post hoc test. Student’s t-test wasperformed separately to find out the difference in serumfolic acid, vitamin B12 and serum albumin between nor-mal statured (>)1 z-score) and stunted (<)1 z-score) chil-dren. Multiple forward regression analysis was used toexamine the association between nutritional status anddifferent biochemical parameters using five incrementalmodels. The statistical analyses were performed using theSPSS 10.0.

RESULTSNutritional statusThere was no significant difference in mean height betweenboys and girls in all age groups (Table S1). About 82% ofNepalese children were found to be stunted in this study

Undernutrition of Nepalese children Ghosh et al.

672 ª2012 The Author(s)/Acta Pædiatrica ª2012 Foundation Acta Pædiatrica 2012 101, pp. 671–676

and more than 18% boys and 17% girls among them werefound to be severe stunted (Table S2).

Haematological parametersTotal count of RBC of different grades of stunted childrenwas significantly lower (p < 0.001) than normal staturedchildren. Values of MCV and MCH were significantlyhigher (p < 0.01) in different grades of stunted children thanthat of normal statured children (Table S3).

Biochemical parametersMean values of serum iron and TS of stunted children weresignificantly lower (p < 0.05) than that of normal staturedchildren. In contrast, mean values of TIBC and transferrinwere significantly higher (p < 0.05) in both moderate andsevere stunted children than that of normal statured chil-dren. However, the mean values of serum ferritin of differ-ent grades stunted boys were found to be significantly lower(p < 0.001) than that of normal statured boys (Table S4).

Stages of iron depletionAbout 60.94% (55.11% boys and 67.15% girls), 22.92%(18.37% boys and 28.58% girls) and 5.21% (8.17% boys and1.43% girls) of Nepalese children were suffering from stage-I, stage-II and stage-III of iron depletion, respectively(Table S5).

Serum vitamin B12 and folic acidFigures 1 and 2 showed that stunted (<)1 SD) children hadsignificantly lower (p < 0.001) vitamin B12 and folic acidvalues compared with normal statured (>)1 SD) children.

Serum albuminThe serum albumin level of stunted children was signifi-cantly lower (p < 0.001) than that of normal statured chil-dren (Fig. 3).

Regression analysesIt has been found that serum ferritin and serum albuminhave strong significant association (p < 0.001) to the nutri-tional status (Table S4).

DISCUSSIONIn this study, the nutritional status as measured by height-for-age z-score indicates that about 82% (81.6% boys and83% girls) Nepalese children have been suffering from dif-ferent grades of stunting (<)1 z-score). Similar magnitude ofstunting in Nepalese children was reported by otherresearchers (1,4). The haematological and biochemicalparameters were analysed according to the nutritional sta-tus of the subject from height-for-age z-score.

The measurement of Hb concentration in whole blood ismost widely used as a screening test for anaemia. Regressionstudy suggests that Hb concentration in surveyed childrendoes not seem to have any significant association with theirnutritional status as determined by z-score values of height-

*902.26 + 98.94

290.65 + 41.02

0

200

400

600

800

1000

1200

Nutritional status

Vit B

12 (p

g/m

L)

Normal statured (>–1 z-score) Stunted (<–1 z-score)

Figure 1 The mean and standard error of mean values of vitamin B12 (pg ⁄ mL)for normal statured (n = 12) and stunted (n = 16) Nepalese children(*p < 0.001).

*17.38 + 1.77

6.7 + 0.32

0

5

10

15

20

25

Nutritional status

Folic

aci

d (n

g/m

L)

Normal statured (>–1 z-score) Stunted (<–1 z-score)

Figure 2 The mean and standard error of mean values of folic acid (mg ⁄ mL)for normal statured (n = 12) and stunted (n = 16) Nepalese children(*p < 0.001).

4.63 + 0.08*4.71 + 0.05***4.29 + 0.314.24 + 0.32

2

2.5

3

3.5

4

4.5

5

GirlsBoys

Seru

m a

lbum

in (g

m/L

)

Normal stature (>–1 z-score) Stunted (<–1 z-score)

Figure 3 Comparison of serum albumin (gm ⁄ L) between normal statured andstunted Nepalese children (*p < 0.05, ***p < 0.001).

Ghosh et al. Undernutrition of Nepalese children


for-age. In some cases, PCV has also been considered as auseful parameter along with Hb level for defining anaemiaand iron-deficiency anaemia (5). According to the WHOcriteria (21), a child having Hb level below 12 g ⁄ dL alongwith PCV value below 32% should be considered as anae-mic. The present investigation did not find any child asanaemic according to these criteria (result not shown).Although Hb and PCV values are useful for defining anae-mia, these are changed at the last stage of iron deficiencyand hence are not considered as good indicators of earlyiron deficiency (5).

Anaemia may result from iron deficiency. The risk ofiron deficiency increases as the body’s iron stores aredepleted. Stages of iron depletion lead to the progressionof magnitude and severity of undernutrition in a subject.Serum ferritin, TS and Hb are used to identify the irondeficiency status. In mild iron deficiency (stage-I irondepletion), the serum ferritin level is decreased, while inmoderate iron deficiency (stage-II iron depletion), boththe serum ferritin level and TS are affected. Only in irondeficiency of stage-III, Hb level is affected along withserum ferritin level and TS. In stunted children, both theserum ferritn and TS levels are decreased compared tothe surveyed children having normal stature. Althoughthe serum ferritin level and TS in stunted children are inthe normal range (serum ferritin: 18–250 ng ⁄ mL and TS:20–50%), it is in the lower border of the normal range.Moreover, the levels are significantly lower than that ofnormal statured children. The mild iron deficiency of thestunted children is also supported by higher serum trans-ferrin and TIBC. Probably, these changes are indicating aregulatory mechanism to maintain the iron homeostasisin the body. Thus, biochemical parameters indicate a mildiron deficiency in stunted children. Olney et al. (2007)reported that a major percentage (53.4%) of Zanzibarichildren suffered from iron-deficiency anaemia (22).Recently, a higher percentage of iron-deficiency anaemiawas found in rural Indian children (72.2%) (23). InNepal, Martorell et al. (1) reported a higher percentage ofiron-deficiency anaemia (60%) in Nepalese children ofTerai region. The prevalence of iron-deficiency anaemiain the present study was not severe like that of otherstudies.

The mean values of TC of RBC in stunted children weresignificantly lower than that of normal statured children.This lower TC of RBC probably is not because of iron defi-ciency. In iron-deficiency anaemia, MCV is decreased whilein observed stunted children, MCV is increased. A defi-ciency of vitamin B12 and ⁄ or folic acid may cause a lowerRBC count along with higher MCV. The results of this studyprobably indicate that lower level of vitamin B12 and folicacid in stunted children compared with normal staturedgroup may cause a change in TC of RBC and MCV valuescompared with normal statured group. The primary causeof folate deficiency may be due to low intake of green leafyvegetables in stunted children as the green leafy vegetablesare expensive in Kathmandu valley. Villamore et al. (24)reported that vitamin B12 of children is positively associated

with socioeconomic factors like the amount of money spenton food per person per day at home, and dietary pattern likefrequent intake of animal food source and dairy products.As the surveyed children belong to lower socioeconomicclass (4), lower vitamin B12 level of stunted children maybe related with their poor socioeconomic conditions as wellas their vulnerable nutritional status.

As the protein-energy malnutrition is considered to bethe most prevalent nutritional disease in developing coun-tries, assessment of protein status is essential to the preven-tion, diagnosis and treatment of undernutrition. Themeasurement of albumin, the most familiar, abundant andreadily available clinically serum protein, will give an indi-cation about the overall serum protein status of surveyedchildren (9). Clarke et al. (25) examined a significant reduc-tion in serum albumin concentration for undernourishedchildren compared to well-nourished children. Similarly,the present study showed a significant decrease in serumalbumin concentration in stunted children compared withnormal statured children. It has been established that serumalbumin level responds slowly to undernutrition because ofits relatively long half-life (14–20 days) and large body pool(4–5 g ⁄ kg of body weight), making it a poor indicator ofearly protein depletion (26). Indeed, about 60% of totalbody’s protein is found outside the bloodstream. Whenserum concentration is being falling during early undernu-trition, this extravascular albumin moves into the blood-stream, helping to maintain the normal serumconcentration despite protein and energy deficit. The serumalbumin concentration may not decline at earlier stages ofundernutrition, that is, in mild and moderate stunted chil-dren.

In the present study, it has been observed that the overalliron status is associated with haematological and biochemi-cal parameters such as RBC count, serum iron, serum ferri-tin, and TS, but not with haemoglobin concentration.Indeed, regression analysis established a positive significantassociation between nutritional status and serum ferritinand TS. As the both serum ferritin and TS are the marker ofiron status, the association between these parameters withnutritional status indicates that mild iron deficiency of sur-veyed children may be related with their nutritional status.The lower dietary iron intake and parasitic infections arefound to be closely associated with iron deficiency (27). Thelower iron status of stunted children cannot be explainedfrom this study as the nutritional intake for iron was notmeasured and the parasitic infections of surveyed childrenhave not been investigated. The interpretation of the presentstudy also cannot be generalized for the Nepalese childrenas the study has been carried out on small number of sub-jects considering the total number of children in Kath-mandu valley.

The data of the present study indicated that the stuntingmay be due to the deficiency of specific nutrients like iron,vitamin B12, folic acid and protein in surveyed Nepalesechildren. Several studies have explored the link between themicronutrient deficiency and growth failure in preschoolchildren in Nepal (28) and other countries (22,29). The



present survey reveals that, not only in Nepalese preschoolchildren, similar problem persists in Nepalese school chil-dren also. It has already been reported that nutrients likeiron, vitamin B12, folic acid and proteins are essential forphysical growth and brain development and the deficiencyof these nutrients leads to substantial impairment of cogni-tive functions such as low intellectual competence andcapacity to learn in children and neuromuscular functions(30). The results of this study may be utilized to design pre-ventive measure by supplementing the deficient micronutri-ents or by awareness programme in the community to selectthe required food items.

CONCLUSIONStunting is prevalent in Nepalese children. A mild iron defi-ciency was found in stunted Nepalese children. The serumferritin has been identified as a sensitive marker for mea-surement of iron status in surveyed children. A deficiency ofserum protein, serum folate and vitamin B12 was also foundin the undernourished Nepalese children.

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SUPPORTING INFORMATIONAdditional Supporting Information may be found in theonline version of this article:

Table S1 Mean and standard error of mean of height forNepalese boys and girls according to their age groups.

Ghosh et al. Undernutrition of Nepalese children


Table S2 Nutritional status of Nepalese children measuredby height-for-age parameter.Table S3 Values of hematological parameters of nutrition-ally normal and different grades of stunted Nepalese chil-dren.Table S4 Values of biochemical parameters of nutritionalnormal and different grades of stunted Nepalese children.Table S5 Distribution of Nepalese children in differentstages of iron deficiency.

Table S6 Stepwise regression models of the associationbetween nutritional status (Dependent variable) and differ-ent biochemical parameters.

Please note: Wiley-Blackwell is not responsible for the con-tent or functionality of any supporting materials supplied bythe authors. Any queries (other than missing material)should be directed to the corresponding author for thearticle.



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Undernutrition in Nepalese children: a biochemical and haematological study