Abstract
The aim of study the correlation of ABO phenotypes in patients of allergic rhinitis and controls and to compare our study with the previous studies to analyse the association of above. 100 patients with symptoms of allergic rhinitis and 100 controls individual were selected from same geographical region and paired by gender and age were enrolled in the study. Detailed history, examination and relevant radiological and hematological investigations were done. ABO phenotypes were identified in red blood cells using hemagglutination technique. This clinic-based observational study was conducted among the patients presenting with signs and symptoms of allergic rhinitis. Maximum no. of cases were seen in ABO phenotype O (52%), followed by A, B and AB (33, 12 and 3% respectively) and it was found to be statistically significant (p = 0.001). Also more number of male patients were found in B and O blood group which was statistically significant (OR 5.33, p = 0.017 and OR 3.63, p = 0.006 respectively). Controls showed marginalized difference in distribution among the basis of different ABO phenotypes. The O blood group phenotype of ABO histo-blood group system is associated with AR. This study contributes to the better understanding of the pathophysiology and clinical variability of this disease and may help to improve strategies towards its prevention and diagnosis. Additionally, ABO histo-blood group phenotyping, an inexpensive and easy to perform assay could be used to identify individuals at risk of developing allergic rhinitis.
Keywords: Allergic rhinitis, ABO phenotype, O blood group
Introduction
Allergic rhinitis (AR) is a common manifestation of allergic diseases affecting approximately 10–25% of the world population [1]. It is a global health problem involving nearly 600 million people all over the world. Allergic rhinitis is one of the most frequent systemic inflammatory disorders. It is one of the most common forms of rhinitis in which immunological response is directed at one or more variety of aeroallergens [2].
The epidemiology of AR has been the subject of numerous studies globally; its prevalence is closely related with age, gender and life style [2]. In the survey conducted in turkey found that the allergic sensitivity was lower in elderly compared to young [3]. The proportion of females was found to be higher than that of males among patients of allergic rhinitis [4]. History of atopy in family is the most predictive factor and the effects of rural and urban factors were not obvious in atopic development [5]. AR may also affect children’s daily activity. It was seen that children’s with AR had 5–20% lower preference to participate in activity than their normal controls [6].
AR is subdivided into Intermittent Allergic Rhinitis (IAR) or Persistent Allergic Rhinitis (PAR) disease. “Intermittent” means that the symptoms are present < 4 days a week or for < 4 consecutive weeks and “Persistent” means that the symptoms are present more than 4 days a week and for more than 4 consecutive weeks [7]. IAR and PAR are not synonymous with “seasonal” and “perennial” [8].
The nasal and bronchial mucosa present similarities and one of the most important concepts regarding nose–lung interactions is the functional complementarity [9]. Most patients with asthma have rhinitis [10] suggesting the concept of one airway one disease. Therefore it is possible that the genetic and environmental factors causing susceptibility to asthma are also involved in the susceptibility for allergic rhinitis.
The ABO histo-blood group system is one of the genetic risk factors linked to the susceptibility to asthma in some populations. Different studies have been conducted and have reported association of asthma with different ABO blood groups [11–14]. One of such study showed significant increase in the percentage of bronchial asthma in group o for both sex in comparison with other groups [14] whereas other study conducted on the patients of atopic diseases showed that the incidence of blood group antigens A and B was somewhat higher in patients than in controls [15]. Despite these contradictory results observed among patients suffering from asthma, studies associating these genetic markers with allergic rhinitis are scarce.
Glycosyltransferases are controlled by the ABO system to build oligosaccharide structures on the cell surface of erythrocytes and vascular endothelium, as well as in the exocrine secretion system including the respiratory tract. Alpha-2-fucosyltransferases FUT1 (H) of red blood cells and vascular endothelium, and FUT2 (Secretor positive) of the exocrine secretion system, are structural genes that collaborate with glycosyltransferases. When a combined analysis of ABO blood groups and secretor phenotypes was performed, a cooperative interaction between the two systems was described. Blood group O/non-secretor subjects had lower lung function values and higher prevalence of atopy [16]. The objective of this study is to test the hypothesis that ABO histo-blood group systems is associated with allergic rhinitis.
Methods
Ethical Considerations
This study was approved by the Ethical Committee, Gajra Raja Medical College, Gwalior, Madhya Pradesh and informed consent was taken from all the participants after explaining the objectives of the study.
Selection of the Patients and Controls
One hundred patients attending outpatient department ENT of both gender age ranging from 11 to 70 years were enrolled. All the patients were matched by age and gender with controls (n = 100) without allergic symptoms.
Diagnosis of Allergic Rhinitis
The diagnosis of allergic rhinitis was done based on the detailed history and clinical examination. The cardinal symptoms considered were sneezing, nasal discharge, nasal obstruction and nasal itching.
Statistical Analysis
To demonstrate any association between results the fisher exact and Chi squared tests were employed to compare proportion and monovariate and bivariate analysis was done by odds ratio. Statistical significance was set for an alpha error of 5% (p value < 0.05).
Results
The results of the analysis of the data of patient and control groups, both with ages ranging from 11 to 70 years, are shown in Table 1. The mean age of the cases was found to be 29.34 years.
Table 1.
Distribution among cases (n = 100) and controls (n = 100) according to age
| Age (years) | Cases | Controls | Odd ratio (95% CI) | p value | ||
|---|---|---|---|---|---|---|
| No. of patients | % | No. of patients | % | |||
| 11–20 | 35 | 35 | 36 | 36 | Reference | 0.09 |
| 21–30 | 23 | 23 | 21 | 21 | 1.12 (0.53, 2.39) | |
| 31–40 | 25 | 25 | 24 | 24 | 1.02 (0.49, 2.12) | 0.005* |
| 41–50 | 9 | 9 | 10 | 10 | 0.92 (0.33, 2.55) | 0.022* |
| 51–60 | 5 | 5 | 5 | 5 | 1.02 (0.27, 3.86) | 0.001* |
| 61–70 | 3 | 3 | 4 | 4 | 0.77 (016, 3.96) | 0.104 |
| Total | 100 | 100 | 100 | 100 | ||
| X2 = 0.32, df = 5, p = 0.99 (NS) | ||||||
* p value significant
34% patients belonged to rural area while 66% patients were from urban area with most common presenting symptom sneezing (40%), followed by nasal obstruction (24%), nasal discharge (21%) and nasal itching (15%). 30% of the patients had positive family history. Most of the patients (66%) complained disturbance in their daily activity and sleep affecting their work productivity and performance. It was also found majority of patients were diagnosed mild intermittent rhinitis (19%), mild persistent rhinitis (15%), moderate–severe intermittent rhinitis (22%), and moderate/severe persistent rhinitis (44%). Moderate–severe persistent rhinitis were most prevailing when compared to mild and moderate intermittent and mild persistent rhinitis. Comorbid conditions associated with allergic rhinitis in our studies were bronchial asthma (17%), sinusitis (73%), atopic dermatitis (9%) and allergic conjunctivitis (4%) (Table 2).
Table 2.
Demographic and clinical profile of patients with allergic rhinitis
| Profile | Number (%) |
|---|---|
| Sex | |
| Male | 48 (48%) |
| Female | 52 (52%) |
| Habitation | |
| Urban | 66 (66%) |
| Rural | 34 (34%) |
| Family history of allergy | 30 (30%) |
| Co-morbid conditions | |
| Bronchial asthma | 17 (17%) |
| Sinusitis | 73 (73%) |
| Atopic dermatitis | 9 (9%) |
| Allergic conjunctivitis | 4 (4%) |
| Predominant symptoms | |
| Sneezing | 40 (40%) |
| Nasal discharge | 21 (21%) |
| Nasal itching | 15 (15%) |
| Nasal obstruction | 24 (24%) |
| Type and severity of disease | |
| Mild intermittent | 19 (19%) |
| Mild persistent | 15 (15%) |
| Moderate–severe intermittent | 22 (22%) |
| Moderate–severe persistent | 44 (44%) |
| Affect on sleep/daily activity | |
| Normal | 34 (34%) |
| Disturbed | 66 (66%) |
In the study, cases found in ABO phenotype A, B, O and AB were 33, 12, 52 and 3 respectively while in control it was 44, 18, 32 and 6 respectively. Cases were found more (52) in blood group O than the control (32) and it was significant (RR 1.59, OR 2.30, p = 0.004). Cases were found less in group A, B and AB than the control (Table 3).
Table 3.
Comparison between cases (n = 100) and controls (n = 100) of allergic rhinitis
| ABO phenotype | Cases | Controls | Risk ratio (95% CI) | OR (95% CI) | p value |
|---|---|---|---|---|---|
| A | 33 | 44 | 0.78 (0.58, 1.06) | 0.62 (0.35, 1.11) | 0.11 |
| B | 12 | 18 | 0.77 (0.48, 1.22) | 0.62 (0.28, 1.36) | 0.23 |
| O | 52 | 32 | 1.49 (1.13, 1.96) | 2.30 (1.29, 4.09) | 0.004* |
| AB | 3 | 6 | 0.65 (0.25, 1.67) | 0.48 (0.11, 1.99) | 0.30 |
Table 3 shows the results of the analysis of the patients and controls by gender. More cases were found in female (52) than the males (48) but more cases were found in males of blood phenotype B and O and it was found significant statistically (OR 5.33, p = 0.017 and OR 3.63, p = 0.006) (Table 4). Distribution of control according to gender was more or less similar percentage in all ABO phenotypes A, B, O and AB (Table 5).
Table 4.
Distribution of cases (n = 100) according to ABO phenotype and gender
| Blood phenotype | Males no. (%) | Females no. (%) | Total | OR (95% CI) | p value |
|---|---|---|---|---|---|
| A | 9 (27.2) | 24 (72.7) | 33 | Reference | 0.017* |
| B | 8 (66.6) | 4 (33.3) | 12 | 5.33 (1.28, 22.15) | |
| O | 30 (57.6) | 22 (42.3) | 52 | 3.63 (1.41, 9.33) | 0.006* |
| AB | 1 (33.3) | 2 (66.6) | 3 | 1.33 (0.10, 16.56) | 0.824 |
| Total | 48 | 52 | 100 |
Table 5.
Distribution of controls (n = 100) according to ABO phenotype and gender
| Blood phenotype | Males no. (%) | Females no.(%) | OR (95% CI) | p value |
|---|---|---|---|---|
| A | 20 (45.4) | 24 (54.5) | Reference | 0.005 |
| B | 8 (44.4) | 10 (55.6) | 0.96 (0.31, 2.89) | |
| O | 15 (46.8) | 17 (53.1) | 1.05 (0.42, 2.64) | 0.014 |
| AB | 4 (66.7) | 2 (33.3) | 2.40 (0.39, 14.49) | 0.93 |
| Total | 47 | 53 |
Discussion
The patients and controls enrolled in this study came from the same geographical region of the state of Madhya Pradesh. 11–20 years age group was the commonest having 35% patients followed by 31–40 years age group with 25% patients. Deb et al. [4] majority of the AR patients (33.3%) belonged to 30–39 years of age group followed by 30.5% in 20–29 years age group. Also in study of Osman et al. [17] that presentation of allergic rhinitis increased progressively during childhood reaching a peak at 16 years. The result of our study can be explained as patients of age 11–20 years are the most active and self caring group of populations. Also consultation rates for children up to the age of 16 may be affected simply by the fact that consultations occur when the children’s parents decide that they have a problem.
Majority of patients in our study belonged to urban region which was in concordance with Cingi et al. [18] whereas in discordance with Zheng et al. [19] and Deb et al. [4] where population affected more belong to the rural region. The reason for higher incidence of AR in urban population may be the higher level of air pollution in urban areas.
Lee et al. [20] concluded that a positive family history increases the risk of developing allergic rhinitis. Similarly Dold et al. [21] showed that the influence of the mother was little stronger than that of the father which is in concordance with our study.
Similar to our study, Yeger et al. [6] concluded that children with allergic rhinitis showed significant 5–20% lower preference to participate in activity than their typical peers. Also Canonica et al. [22] study reported large percentage of patients had difficulty in falling asleep ranging from 47% in Spain to 26% in Germany and the United kingdom. AR shows most pronounced symptoms in the night and the early morning. Nasal airway resistance is also increased in the recumbent position further increasing nocturnal congestion [26]. These causes insomnia at night, thus causing daytime sleepiness and fatigue.
In the study most patients presented, fell within the moderate–severe persistent group. In Lee et al. [23], Navarro et al. [24] and Bousquet et al. [7] study the most prevalent group was moderate–severe persistent group (51, 34.7 and 35% respectively). This may be because the patients reported late to the doctor.
Our study showed majority of the patients had blood group O showing association between ABO phenotype and allergic rhinitis. This was in consistent with the study of Falsarella et al. [25]. Similar association were seen in the patients of bronchial asthma with the blood group O in the study of Saini et al. [12], Al-Shamma et al. [14], Chen et al. [11] and Ronchetti et al. [13].
However many of the studies showed different results. El-Mehairy et al. [26] and Filsoufi [27] observed much higher A and AB and lower O frequencies in the patients of allergic diseases than in controls. Bijanzadeh et al. [28] and Brachtel et al. [15] showed no significant differences in the distribution of ABO phenotypes between patients and controls. de la Vega et al. [29], Anand [30], Khalil [31] and Moniwa [32] have analyzed the ABO distribution in the patients with bronchial asthma and found a clear and statistically significant surplus of B phenotypes and an O deficit. This discordances in result may be because our study evaluated only patients with diagnosis of allergic rhinitis whereas the majority of the patients enrolled in previous studies were carriers of atopic diseases other than allergic rhinitis.
Also in our study, more cases were found in female 52% than the males 48% but more cases were found in males of ABO phenotype B and O and it was found significant statistically. Our result was consistent to the study of Falsarella et al. [25] which showed more susceptibility to allergic rhinitis of ABO phenotype O in males.
Al-Shamma et al. [14] showed variation from our result. His result indicated a significant increase in the percentage of group A in asthmatic males than that of female and significant increase in percentage of B and AB blood groups in asthmatic female than male where as no significant differences in percentages of blood group O and rhesus factor between asthmatic male and female.
Conclusion
Our study concludes that O blood group phenotype is associated with allergic rhinitis. This study contributes to the better understanding of the pathophysiology and clinical variability of this disease and may help to improve strategies towards its prevention and diagnosis.
Compliance with Ethical Standards
Conflict of interest
The authors declare that they have no competing interests.
Ethical Standard
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed Consent
Informed consent was obtained from all individual participants included in the study.
References
- 1.Bousquet J, Van Cauwenberge P, Khaltaev N, Aria Workshop Group. World Health Organisation Allergic rhinitis and its impact on asthma. J Allergy Clin Immunol. 2001;108(5 suppl):S147–S334. doi: 10.1067/mai.2001.118891. [DOI] [PubMed] [Google Scholar]
- 2.Kilpelainen M, Terho EO, Helenius H, Koskenvuo M. Body mass index and physical activity in relation to asthma and atopic diseases in young adults. Respir Med. 2006;100:1518–1525. doi: 10.1016/j.rmed.2006.01.011. [DOI] [PubMed] [Google Scholar]
- 3.Karabulut K, Baysal S, Acar B, Babademez MA, Karasen MR. Allergic rhinitis in geriatric patients. Arch Gerontol Geriatr. 2011;5:2414–2444. doi: 10.1016/j.archger.2010.12.007. [DOI] [PubMed] [Google Scholar]
- 4.Deb A, Mukherjee S, Saha BK, Sharma BB, Pal J, Pandey N, Nandi TK, Nandi S. Profile of patients with allergic rhinitis (AR): a clinic based cross-sectional study from Kolkata. India J Clin Diagn Res. 2014;8(1):67–70. doi: 10.7860/JCDR/2014/6812.3958. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Guner SN, Gokturk B, Kilic M, Ozkiraz S. The prevelences of allergic disease in urban and rural areas are similar. Allergol Immunopathol. 2010;39(3):140–144. doi: 10.1016/j.aller.2010.05.004. [DOI] [PubMed] [Google Scholar]
- 6.Yeger BE, Engel A, Kessel A. Differences in leisure activities between children with allergic rhinitis and health peers. Int J Pediatr Otorhinolaryngol. 2010;74:1415–1418. doi: 10.1016/j.ijporl.2010.09.021. [DOI] [PubMed] [Google Scholar]
- 7.Bousquet J, Neukirch F, Bousquet PJ, Gehano P, Klossek JM, Gal ML, Allaf B. Severity and impairment of allergic rhinitis in patients consulting in primary care. J Allergy Clin Immunol. 2006;117:158–162. doi: 10.1016/j.jaci.2005.09.047. [DOI] [PubMed] [Google Scholar]
- 8.Van Hoecke H, Vastesaeger N, Dewulf L, Sys L, van Cauwenberge P. Classification and management of allergic rhinitis patients in general practice during pollen season. Allergy. 2006;61:705–711. doi: 10.1111/j.1398-9995.2006.01057.x. [DOI] [PubMed] [Google Scholar]
- 9.Togias A. Rhinitis and asthma: evidence for respiratory system integration. J Allergy Clin Immunol. 2003;111(6):1171–1183. doi: 10.1067/mai.2003.1592. [DOI] [PubMed] [Google Scholar]
- 10.Bousquet J, Vignola AM, Demoly P. Links between rhinitis and asthma. Allergy. 2003;58:691–706. doi: 10.1034/j.1398-9995.2003.00105.x. [DOI] [PubMed] [Google Scholar]
- 11.Chen YL, Chen JC, Lin TM, Huang TJ, Wang ST, Lee MF, Wang JY. ABO/secretor genetic complex is associated with the susceptibility of childhood asthma in Taiwan. Clin Exp Allergy. 2005;35:926–932. doi: 10.1111/j.1365-2222.2005.02278.x. [DOI] [PubMed] [Google Scholar]
- 12.Saini M, Yadav AS. Distribution of ABO & Rh (D) allele frequency among asthmatic patients. IMPACT Int J Res Appl Nat Soc Sci (IMPACT: IJRANSS) 2014;2(5):217–222. [Google Scholar]
- 13.Ronchetti F, Villa MP, Ronchetti R, Bonci E, Latini L, Pascone R, Bottini N, Gloria-Bottiniz F. ABO/Secretor genetic complex and susceptibility to asthma in childhood. Eur Respir J. 2001;17:1236–1238. doi: 10.1183/09031936.01.99109101. [DOI] [PubMed] [Google Scholar]
- 14.Al-Shamma YMH, Al-Zubaidy AM, Al-Turjoman AA. The Association of Bronchial Asthma to (ABO) Blood Groups in Najaf Governorate. Kufa Med J. 2008;11(1):234–245. [Google Scholar]
- 15.Brachtel R, Walter H, Beck W, Hilling M. Associations between atopic diseases and the polymorphic systems ABO, kidd, inv and red cell acid phosphatase. Hum Genet. 1979;49(3):337–348. doi: 10.1007/BF00569354. [DOI] [PubMed] [Google Scholar]
- 16.Carpeggiani C. Allergic rhinitis and association with the O blood group. Rev Bras Hematol Hemoter. 2011;33(6):400–409. doi: 10.5581/1516-8484.20110113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Osman M, Hansell AL, Simpson CR, Hollowell J, Helms PJ. Gender- specific presentations for asthma, allergic rhinitis and eczema in primary care. Prim Care Respir J. 2007;16(1):28–35. doi: 10.3132/pcrj.2007.00006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Cingi C, Cakli H, Us T, Akgun Y, Kezban M, Ozudogru E, Cingi E, Ozdamar K. The prevalence of allergic rhinitis in urban and rural areas of Eskişehir-Turkey. Allerol Immunopathol. 2005;33(3):151–156. doi: 10.1157/13075698. [DOI] [PubMed] [Google Scholar]
- 19.Zheng M, Wang X, Bo M, Wang K, Zhao Y, He F, Cao F, Zhang L, Bachert C. Prevalence of allergic rhinitis among adults in urban and rural areas of china: a population- based cross-sectional survey. Allergy Asthma Immunol Res. 2015;7(2):148–157. doi: 10.4168/aair.2015.7.2.148. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Lee JT, Lam ZCM, Lee WT, Kuo LCT, Jayant V, Singh G, Lee J. Familial risk of allergic rhinitis and atopic dermatitis among Chinese families in Singapore. Ann Acad Med Singapore. 2004;33:71–74. [PubMed] [Google Scholar]
- 21.Dold S, Wjst M, Mutius EV, Reitmeir P, Stiepel E. Genetic risk of asthma, allergic rhinitis and atopic dermatitis. Arch Dis Child. 1992;67:1018–1022. doi: 10.1136/adc.67.8.1018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Canonica GW, Mullol J, Pradalier A, Didier A. Patient perceptions of allergic rhinitis and quality of life findings from a survey conducted in Europe and the United States. WAO J. 2008;1:138–144. doi: 10.1097/WOX.0b013e3181865faf. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Lee CH, Jang JH, Lee HJ, Kim IT, Chu MJ, Kim CD, Won YS, Kim JW. Clinical characteristics of allergic rhinitis according to allergic rhinitis and its impact on asthma guidelines. Clin Exp Otorhinolaryngol. 2008;1(4):196–200. doi: 10.3342/ceo.2008.1.4.196. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Navarro A, Valero A, Juliá B, Quirce S. Coexistence of asthma and allergic rhinitis in adult patients attending allergy clinics: ONEAIR study. J Investig Allergol Clin Immunol. 2008;18(4):233–238. [PubMed] [Google Scholar]
- 25.Falsarella N, Ferreira AIC, Nakashima F, Mattos CCB, Mattos LC. Allergic rhinitis and association with the O blood group. Rev Bras Hematol Hemoter. 2011;33(6):444–448. doi: 10.5581/1516-8484.20110120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.El-mehairy MM, El-Tarabishi N. The correlation between ABO blood groups and allergic orders. Ann Allergy. 1966;24:366–368. [PubMed] [Google Scholar]
- 27.Filsoufi J. Statistical study of the relationship between allergic diseases and the blood group. Fr J Allerg Clin Immunol. 1975;15(2):115–117. [Google Scholar]
- 28.Bijanzadeh M, Ramachandra NB, Mahesh PA, Savitha MR, Manjunath BS, Jayaraj BS. Lack of association between asthma and ABO blood group. Lung. 2009;187(6):389–392. doi: 10.1007/s00408-009-9175-1. [DOI] [PubMed] [Google Scholar]
- 29.de la Vega AR, Cortes JG, Gallestey JB. Genetics polymorphisms of ABO and Rh system in relation to bronchial asthma: preliminary report. Allergol Immunopathol (Madr) 1976;4:305–310. [PubMed] [Google Scholar]
- 30.Anand S. The relationship of ABO, MN, and Rhesus blood groups to asthma. Indian J Chest Dis Allied Sci. 1964;6:74. [Google Scholar]
- 31.Khalil L. The ABO blood groups and diseases in infant and children. Acta Paediatr Scand. 1960;49:76–80. doi: 10.1111/j.1651-2227.1960.tb07706.x. [DOI] [PubMed] [Google Scholar]
- 32.Moniwa H. Statistical studies on the correlation between the ABO blood group and some diseases. Tohoku J Exp Med. 1960;72:275–280. doi: 10.1620/tjem.72.275. [DOI] [PubMed] [Google Scholar]
