|Year : 2015 | Volume
| Issue : 2 | Page : 72-78
The impact of anemia and hemoglobin level as a risk factor for asthma and allergic diseases
Abdulbari Bener1, Mohammad S Ehlayel2, Qutayba Hamid3
1 Department of Biostatistics and Medical Informatics, Cerrahpaşa Faculty of Medicine, Istanbul University, Istanbul, Turkey; Department of Evidence for Population Health Unit, School of Epidemiology and Health Sciences, University of Manchester, Manchester, UK
2 Department of Pediatrics, Section of Pediatric Allergy and Immunology, Hamad Medical Corporation, Doha; Department of Pediatrics, Weill Cornell Medical College, Ar Rayyan, Qatar
3 Department of Medicine, Division of Experimental Medicine, Meakins Christie Laboratories, McGill University, Montreal, Canada
|Date of Web Publication||9-Mar-2016|
Department of Biostatistics and Medical Informatics, Cerrahpaşa Faculty of Medicine, Istanbul University, 34098 Cerrahpasa, Istanbul
Source of Support: None, Conflict of Interest: None
Aim: To determine the association between anemia and asthma among children as case-control and also investigate the effect of hemoglobin (Hb) on asthma and atopy markers. Settings: The case-control study was performed during a period between March 2012 and October 2013, on asthmatics and controls (<14 years) at Pediatric Allergy-Immunology Clinics and Primary Health Care Clinics, Qatar. Subjects and Methods: A total of 520 cases and 520 controls matched by age, gender, and ethnicity. Sociodemographic and clinical data were collected through physician diagnosis and questionnaire. Their health status was assessed by past or present clinical manifestations, family history, physical examination, body mass index (BMI), anemia, Hb level, calcium, and phosphorus. Results: About 56.3% of asthmatic and 51.9% of controls were males and 43.7% of asthmatic and 48.1% of controls were females. The mean age (± standard deviation, in years) for asthmatic versus controls was 9.3 ± 3.28 versus 10.2 ± 3.38. Anemia was more prevalent in asthmatics than controls. Lower Hb levels were associated with more allergic disease and elevated serum IgE. The study revealed that Hb level, iron and ferritin deficiencies were considerably higher in asthmatic children compared to healthy children. There was a significant difference found in the mean values of Hb levels between asthmatic (10.58 ± 3.05 g/dL) and control children (11.75 ± 3.10) (P = 0.006). Besides, mean IgE was statistically significantly higher in asthmatic compared to control children (P < 0.001). There was a significant correlation between Hb level and total IgE in asthmatic compared to controls (r = 0.295 vs. r = 0.268, P = 0.001). The analysis revealed that the predictors for development of asthma in children were serum iron deficiency (P < 0.001), phosphorus (P < 0.001), parental consanguinity (P = 0.046), breastfeeding < 6 months (P < 0.001), BMI (P = 0.005), less physical activity (P < 0.001), family history of asthma (P = 0.028), and ferritin (P < 0.001). White blood cell count (P < 0.001), serum IgE level (P < 0.001), and serum calcium level (P < 0.001) were considered as the main risk factors after adjusting for age, gender, and other variables. Conclusion: The study findings showed a high prevalence of iron deficiency among children with asthma and allergic diseases. Serum Hb levels were lower in asthma, allergic rhinitis, and atopic dermatitis children. Hb level and anemia were strong contributors for asthma and allergic diseases.
Keywords: Allergic diseases, anemia, asthma, children, hemoglobin level, predictors, Qatar
|How to cite this article:|
Bener A, Ehlayel MS, Hamid Q. The impact of anemia and hemoglobin level as a risk factor for asthma and allergic diseases. Indian J Allergy Asthma Immunol 2015;29:72-8
|How to cite this URL:|
Bener A, Ehlayel MS, Hamid Q. The impact of anemia and hemoglobin level as a risk factor for asthma and allergic diseases. Indian J Allergy Asthma Immunol [serial online] 2015 [cited 2020 Feb 27];29:72-8. Available from: http://www.ijaai.in/text.asp?2015/29/2/72/178271
| Introduction|| |
Asthma and related allergic diseases are substantial public health problems worldwide (where asthma alone affects nearly 300 million people worldwide).  It is one of the leading causes of morbidity in children and the most common chronic disease among children, where almost 90% of children are diagnosed by the age of 6. It has a tremendous negative impact through increased asthma exacerbations, hospital admissions, absence from school, and high healthcare costs. , The prevalence of asthma and allergic diseases has been increasing rapidly in westernized and industrialized countries. The exact causes of such a rise are poorly understood. However, viral infection with "asthmogenic" viruses in early childhood,  environmental pollution,  changes in lifestyle, and evolving dietary habits have been suspected in genetically susceptible/high-risk patient population. ,,,,,, It was recently proposed that anemia may explain some part of this pattern. 
Asthma and anemia associated with acute infections occur more commonly in children than in adults. ,,,,,, Iron deficiency exerts adverse effects on immune response and alters the metabolism and growth of pathogens. It has already been reported that low hemoglobin impairs tissue oxygenation and acts as an independent risk factor for developing lower respiratory tract infections (LRTIs) in children. ,, There are very few reports available in medical literature regarding the association of anemia and childhood asthma.
Anemia has occurred despite fortification of foods in some westernized countries and in areas of the world that are considered sun-replete. It was documented that the global rise in asthma and allergic diseases may be linked to lower serum of hemoglobin (Hb) and anemia. ,
The growing data suggest that anemia plays an important role in protecting asthma and allergic diseases. The greatest burden of asthma and allergic diseases is during childhood, , when the rapidly rising rates of diseases are more evident in the population.
Considering the high prevalence of Hb insufficiency and allergic diseases in Qatari population, we have conducted a case-control study to better understand its significance and investigate the impact of anemia status on asthma, allergic rhinitis, and wheezing in children.
| Subjects and methods|| |
This is a case-control study which was designed to determine the relationship between anemia and hemoglobin level as a risk factor for and asthma in young Qatari population below 14 years of age. The survey was conducted over a period from March 2012 to October 2013. This current study is based on the 520 asthmatic cases and 520 control subjects matched with age, gender and ethnicity. The study was approved by the Hamad General Hospital, Hamad Medical Corporation (HMC). All human studies have been approved by the Research Ethics Committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 declaration of Helsinki. All the persons who agreed to participate in this study gave their informed consent prior to their inclusion in the study.
Selection of asthmatic subjects
The diagnosis of asthma and other allergic diseases such as allergic rhinitis, atopic dermatitis, urticaria, and food allergy was based on physician diagnosis. Asthmatic subjects aged below 14 years were identified from pediatric clinics as a part of cohort study; a random sample of 703 asthmatic children approached and 520 gave consent and participated in the study with a response rate of 74%.
Selection of controls
Control subjects aged below 14 years were identified from the community as healthy and if not ever been diagnosed as asthmatic or if they never used any inhaler or asthmatic medication. This group involved a random sample of 673 healthy subjects who visited the Primary Health Centre for any reason other than acute or chronic disease, and only 520 subjects were included due to either refusal of the mother or difficulty in drawing blood from very uncooperative subjects; with a response rate of 77%. The healthy subjects were selected in a way matching to the age, gender, and ethnicity of cases to give a good representative sample of the studied population.
Exclusion criteria included children with prematurity, congenital chest wall malformations, severe systemic illness (congenital heart disease, tuberculosis, etc.), chronic diseases (diabetes, hepatitis, liver failure, etc.), intake of iron supplements, and previous history of infection in the control group.
Health professionals and nurses interviewed parents of all children and completed the questionnaires, which covered the information such as age, gender, nationality, educational level, occupation, place of residence (urban and semi-urban), type of house, monthly income, and consanguinity. Furthermore, it included the assessment of nondietary covariates such as height, weight, color of the skin, family history, physical activity, and duration of the exposure to sunlight. Height and weight were measured using standardized methods, and all the participants wore light clothes and no shoes for this part of the examination. The body mass index (BMI) was calculated as the weight in kilograms (with 1 kg subtracted to allow for clothing) divided by height in meters squared. A major part of the designed questionnaire was validated in the previous study of Bener et al. ,, This questionnaire was validated on 50 randomly selected children visiting health centers.
The definition for asthma  is a chronic, inflammatory lung disease characterized by symptoms of cough, wheezing, dyspnea, and chest tightness that occur in paroxysms and are usually related to specific triggering events, airway narrowing that is partially or completely reversible, and increased airway responsiveness to a variety of stimuli. The diagnosis of asthma was performed by a pediatrician and confirmed by the medical record registry. Common symptoms of asthma include wheezing, coughing, and shortness of breath. The International Classification of Diseases and Health-Related Problems 10 th Revision (ICD-10) was used by the Medical Records Section of the HMC for coding the diagnosis using the ICD-10 code for asthma. Wheezing is the high-pitched whistling sound that you may hear as you breathe when air flow is obstructed in your lung. At the beginning of an asthma attack, wheezing usually occurs while breathing out or exhaling, but may occur while breathing in if the attack worsens. ICD-10 code was R06.2 for wheezing. Allergies are an abnormally high sensitivity to certain substances, such as pollens, foods, or microorganisms. Common indications of allergy may include sneezing, itching, and skin rashes.
Blood collection and serum measurements of hemoglobin level
A trained phlebotomist collected blood from the antecubital vein of each child. The blood samples were analyzed at HMC clinical laboratory for complete blood count, iron level, ferritin level, and total iron binding capacity (TIBC). Hb level was estimated in the blood samples using an automatic blood cell counter. The cutoff point for low Hb level was 11 g/dl; meeting the definition of anemia as Hb level being two standard deviations (SDs) below the mean for age, as fixed by the WHO.  Iron level and TIBC were measured using the ferrozine method without deproteinization. Reference ranges were 22-184 μg/dl for iron level and 228-428 μg/dl for TIBC.  As for ferritin, the electrochemiluminescence "ECLIA" was used with a cutoff point of 20 μg/l. The transferrin was measured by immunoturbidimetry assay with 200-360 mg/dl reference ranges.  Mentzer index was calculated through the formula: mean corpuscular volume/red blood cell and the transferrin saturation through the formula: iron level/TIBC × 100 (normal values: 20-45%). C-reactive protein was considered positive if >0.3 mg/dl. The diagnosis of iron deficiency anemia (IDA) was diagnosed in the control group when a low ferritin level was found with high TIBC, as recommended by the Centers of Disease Control Continuous Discharge Certificate/WHO expert groups on May 2004, being the most valuable indicators of IDA.  Total and allergen-specific IgE (to a panel of common food and environmental allergens) levels were measured from serum using RIDA Allergy Screen Panel 2 or 3 test kit (R-Biopharm AG, Darmstadt, Germany). ,
Data are expressed as median, geometric mean, arithmetic mean, and SD unless otherwise stated. Student's t-test was used to ascertain the significance of differences between mean values of two continuous variables, and nonparametric Mann-Whitney test was used. The Fisher's exact test (two-tailed) and Chi-square tests were performed to test for differences in the proportions of categorical variables between two or more groups. Pearson's correlation coefficient was used to evaluate the strength of association between variables. Multiple logistic regression analysis using the forward inclusion and backward deletion method was used to assess the relationship between dependent and independent variables and to adjust for potential confounders and orders the importance of risk factors (determinant) for the asthma and allergic diseases. P <0.05 was considered as the cutoff value for significance.
| Results|| |
Of the total number of children surveyed, 56.3% of asthmatic and 51.9% of healthy children were males and 43.7% of asthmatic and 48.1% of healthy children were females. The mean age (±SD, in years) for asthmatic versus control children was 9.92 ± 3.28 versus 10.20 ± 3.38. [Table 1] shows the sociodemographic characteristics of the studied children according to asthmatic and control subjects. There were statistically significant differences between asthmatic and control subjects with respect to BMI (P = 0.042), consanguinity (P = 0.003), number of peoples living at home (P = 0.023), physical activity (P < 0.001), and number of bedrooms (P = 0.048).
|Table 1: Sociodemographic characteristics of the studied asthmatic and control subjects |
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[Table 2] presents Hb levels among asthmatic Hb level <11.0 g/dL and >11.0 g/dL of the children studied. Most of the variables such as allergic rhinitis, recurrent wheezing, eczema, urticaria, food allergy, and other allergic diseases showed statistically significant differences between asthmatic and control children.
[Table 3] shows allergy biomarker values among asthmatic and control children. The study revealed that Hb level, iron and ferritin deficiencies were considerably higher in asthmatic children compared to healthy children. There was a significant difference found in the mean values of Hb levels between asthmatic (10.58 ± 3.05 g/dL) and control children (11.75 ± 3.10) (P = 0.006). Besides, mean IgE was statistically significantly higher in asthmatic compared to control children (P < 0.001). There was a significant correlation between Hb level and total IgE in asthmatic compared to controls (r = 0.295 vs. r = 0.268, P = 0.001).
|Table 3: Baseline serum hemoglobin, allergy, and biochemical markers of asthmatic and control children |
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[Table 4] identifies the predictors for the development of asthma in children. Serum iron deficiency (OR = 3.19; CI = 166-488 P < 0.001), phosphorus (OR = 3.05; CI = 1.17-4.74, P < 0.001), parental consanguinity (OR = 2.96; CI = 1.45-5.62, P = 0.046), breast feeding < 6 months (OR = 2.84; CI = 1.73-4.96, P < 0.001), BMI (OR = 2.72; CI = 1.76-4.52, P = 0.005), less physical activity (OR = 2.46; CI = 1.29-5.07; P < 0.001), family history of asthma (OR = 2.37; CI = 1.48-3.91; P = 0.028), ferritin (OR = 2.34; CI = 1.71-3.22; P < 0.001), white blood cell count (OR = 2.12; CI = 1.67-3.18; P < 0.001), serum IgE level (OR = 1.94; CI = 1.26-3.05; P < 0.001), and serum calcium level (OR = 1.65; CI = 1.33-2.68; P < 0.001) were considered as strong predictors and the main factors associated with iron deficiency in asthmatic children after adjusting for age, gender, and other variables.
|Table 4: Multivariable logistic regression analysis for the prediction of asthma and associated potential risk factors |
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| Discussion|| |
The epidemic rise in anemia, asthma, and related allergic disease is a common major public health problem worldwide.  Several studies have reported that Hb is associated with an increased incidence of asthma and allergy symptoms. In the current study sample, Qatari children with asthma and allergic diseases experienced a high prevalence of anemia than in healthy children. Few epidemiological studies have reported a similar finding that anemia is associated with an increased incidence of asthma and allergy symptoms. ,,,,
In this study, asthmatic subjects had a lower mean of serum Hb level (10.58 ± 3.05 g/dL) than healthy children with a mean of 11.75 ± 3.08 g/dL which were affected with anemia. This shows that the incidence of anemia is surprisingly high among children such as asthma and allergic diseases. It indicates that low Hb levels may contribute, directly or indirectly, in the risk for the development of asthma and allergies.
Asthma and respiratory diseases account for substantial increasing childhood morbidity, placing a burden on the health care system and on affected individuals and families. In 2007, approximately, 6.7 million children under the age of 18 had asthma,  with rates increasing to nearly 7 million (9.4%) by 2008.  As of 2008, more than 14% of children in the age range of 0-17 had been diagnosed with asthma,  with children in the age range of 0-4 years demonstrating the greatest use of health care services for asthma-related illness.  Increases in childhood respiratory disease over the past decades have highlighted the need to identify specific factors associated with early childhood wheezing and childhood asthma. The rise in prevalence of asthma is quite rapid to be due to genetic mutations, and air pollution has actually declined in many areas where asthma rates have been increasing.
Whatever the etiology of anemia, the relation between low Hb level and LRTI has not been fully investigated, and only few reports are available evaluating this subject. , The prevalence of anemia varies between developed and developing countries, reaching up to 20% of schoolchildren across several Arab Gulf countries ,, and is principally caused by iron deficiency. As many as 20% of children in the United States and 80% of children in developing countries will be anemic at some point by the age of 18-year-old. , In our study, 30.4% of the total number of patients had Hb level below 11 g/dl and 16.7% of healthy controls, which is consistent with the figures in Lebanon children where the mean Hb level was 11.35 ± 1.24 g/dl in hospitalized cases and 11.95 ± 1.03 g/dl in healthy controls. 
One can speculate the possible explanations of the underlying association of IDA and development of allergic diseases including asthma. Further research is necessary to verify the exact mechanism. These explanations could be related to maternal dietary factors. Recent research has suggested that maternal dietary factors during pregnancy may influence the development of childhood asthma. ,, Low maternal iron levels during pregnancy are negatively associated with increased childhood wheeze and atopic sensitization.  The intrauterine environment provides the substrate for many important processes including lung and early immune system development, and support of optimal fetal growth requires adequate maternal nutritional status. Lung development in utero is apparent within 3-4 weeks after fertilization and continues throughout gestation and childhood.  Then, it is possible that inadequate nutritional status during gestation may negatively impact childhood respiratory health, ,, particularly during critical periods of embryonic and fetal growth. 
Another possible explanation is the dietary shift of the population with the discovery of natural gas. It is observed that in many Arab Gulf countries, including Qatar, there are excessive internet use and television viewing, poor lifestyle habits, and fast food consumption restaurants that affect asthma children.  Evidence indicate a role for diet in promoting or protecting against allergic diseases. This deviation from Mediterranean diet in favor of Western diet is associated with obesity, asthma, allergic diseases, and anemia.  Consumption of fast food increased the risk of asthma, rhinoconjunctivitis, and severe eczema. , Furthermore, iron affects the components of immune system including the number and functions of lymphocytes and granulocytes.  It determines the balance between and the intensity of Th1 and Th2 arms of the immune response and leads to a deviation toward Th2 response.  It is known that Th2-skewness of immune response favors the development of allergic diseases.
Asthma and respiratory diseases are the leading causes of death in children, and identification of modifiable risk factors of asthma and respiratory may help in reducing the burden of diseases.  Literature reveals a few studies on anemia in patients with acute asthma. To the best of our knowledge, our study is one of the few studies evaluating Hb level in asthma and allergic diseases, and the first one to be conducted among children in Qatari and other Arabian Gulf Cooperative Council states.
Limitations of study
This study certainly has some limitations. Being a single tertiary care center, many of the cases were referred ones. Another limitation is the lack of data on oral intake of iron supplement and other supplement, and finally, perhaps, the number of different types of allergic diseases was relatively small. Further limitation is the number of controls could be 2-3 times more than the number of cases. Therefore, the patient profile probably does not truly reflect the prevalence of a particular disease in the representative population. Strengths of our study include large sample size, case-control designed, age, gender, and ethnicity-matched, and physician-diagnosed asthma, and allergic diseases.
What is known on this subject?
The data are lacking regarding the association between Hb level anemia and asthma in human beings.
What this study adds?
The association between Hb level anemia and asthma and allergic diseases in children is never been reported. This is the first study to investigate an association between Hb level and asthma. The iron deficiency was higher in studied asthmatic children than in controls.
| Conclusion|| |
The present study investigated the role of iron in childhood asthma and allergies. Hb insufficiency was common in the study sample whereas severe anemia was significantly higher in children with asthma and allergic diseases compared with healthy children. Supplementing infants with iron might prove to be a safe and effective strategy for reducing the risk of asthma and allergic diseases, but further studies to determine the causality need to be done.
The authors would like to thank all parents and children who participated in this study as well as the HMC for their support and ethical approval (HMC-MRC RP# 12034/12-RC/70813/13 and RC# 71612/2012).
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Table 1], [Table 2], [Table 3], [Table 4]