Frequency of non-asthma-like symptoms of allergic diseases based on ISAAC results in adolescents of the Khabarovsk region, Russia

Background. In the course of the ISAAC standardized survey, not only asthma-like symptoms are revealed, but also other atopy symptoms, the prevalence of which in their relationship with asthma-like symptoms is of great interest for determining the likelihood of developing BA. This work presents the first study of the frequency of symptoms occurrence in school students of the Khabarovsk Territory (Russia).

Materials and methods. The survey involved 696 teenagers living in the city of Khabarovsk and Khabarovsk rural district who meet the requirements of the ISAAC program method by age (13–14 years).

Results. The prevalence of symptoms of allergic rhinitis in all interviewed adolescents of the Khabarovsk Territory was 69.3 %. In the group with asthma-like symptoms it is significantly higher (77.2 % versus 56.6 %). Complications in the form of conjunctivitis with non-infectious rhinitis occurred in 12.6 % of cases, and also much more often in children with asthma-like symptoms (30.1 % versus 8.9 %). Symptoms of atopic dermatitis occur in 11.8 % of adolescents, 4.6 times more often when combined with asthma-like symptoms (22 % versus 4.8 %), and localize in typical places of atopic dermatitis in 5.3 % of cases, which happens more often in case of asthma-like symptoms (11.4 % versus 3.9 %).

Conclusion. Studies using the ISAAC standard continuous survey showed that prevalence of non-asthma-like symptoms of atopy among adolescents in Khabarovsk and Khabarovsk Krai is higher than in most countries where this study was conducted. The frequency and structure of non-asthma-like symptoms revealed in the course of the survey is characteristic of industrially developed countries. It should be noted that the prevalence and severity of non-asthma-like symptoms in Khabarovsk is significantly higher than in the Khabarovsk rural area, however, the symptoms of non-infectious rhinitis in the countryside are more severe. 

1. GINA 2018 https://ginasthma.org/wp-content/uploads/2018/04/wms-GINA-2018-report-tracked_v1.3.pdf.

2. Evseeva KP, Kholodok MR, Morozova NV, Suprun EN, Kozlov FC, Lazar KG. Epidemiology of bronchopulmonary diseases of children and adolescents of the Khabarovsk Territory. Bulletin of physiology and pathology of respiration. 2016; 61: 31–35. (In Russ.)] https://doi.org/10.12737/21436.

3. The national program “Bronchial asthma in children. Treatment strategy and prevention”. 5th ed., reprint. and additional. M.: Original layout, 2017. 160 p. (In Russ.)]

4. Chung KF, Bel EH, Wensell SE. Difficult-to-Treat Severe Asthma (out of print) Wenzel Book. Published in 2011. https://doi.org/10.1183/1025448x.erm5110.

5. NHWS-National Health and Wellness Survey https://www.kantarhealth.com/docs/datasheets/kh-national-health-and-wellness-survey.pdf.

6. Clinical recommendations “Bronchial asthma”. Ministry of health of the Russian Federation, 2019. http://spulmo.ru/upload/kr_bronhastma_2019.pdf. (In Russ.)]

7. Arkhipov VV, Grigoryeva EV, Gavrishina EV. Control of bronchial asthma in Russia: results of NIKA multi-center observational study. Pulmonologiya. 2011; 6: 87–93. (In Russ.) https://doi.org/10.18093/0869-0189-2011-0-6-87-93.

8. Wong GW, Brunekreef B, Ellwood P, Anderson HR, Asher MI, Crane J, Lai CK; ISAAC Phase Three Study Group. Cooking fuels and prevalence of asthma: a global analysis of phase three of the International Study of Asthma and Allergies in Childhood (ISAAC). Lancet Respir Med. 2013 Jul; 1 (5): 386–394. https://doi.org/10.1016/S2213-2600(13)70073-0.

9. Weinmayr G, Gehring U, Genuneit J, Büchele G, Kleiner A, Siebers R, Wickens K, Crane J, Brunekreef B, Strachan DP; ISAAC Phase Two Study Group. Dampness and moulds in relation to respiratory and allergic symptoms in children: results from Phase Two of the International Study of Asthma and Allergies in Childhood (ISAAC Phase Two). Clin Exp Allergy. 2013 Jul; 43 (7): 762–774. https://doi.org/10.1111/cea.12107.

10. Asher MI, Keil U, Anderson HR, Beasley R, Crane J, Martinez F, Mitchell EA, Pearce N, Sibbald B, Stewart AW, et al. International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods. Eur Respir J. 1995 Mar; 8 (3): 483–491. https://doi.org/10.1183/09031936.95.08030483.

11. Rosa AM, Ignotti E, Hacon Sde S, Castro HA. Prevalence of asthma in children and adolescents in a city in the Brazilian Amazon region. J Bras Pneumol. 2009 Jan; 35 (1): 7–13. English, Portuguese. https://doi.org/10.1590/s1806-37132009000100002.

12. Nasiri Kalmarzi R, Shekari A, Tajik M, Ataee P, Homagostar Gh, Roshani D, et al. The Prevalence of Asthma Symptoms in Elementary and Middle School Students in Kurdistan Province, the West of Iran. International Journal of Pediatrics 2016; 4 (2): 1323–1330. https://doi.org/10.22038/ijp.2016.6428.

13. Suprun E, Suprun S, Shkunova M, Yakovlev EI, Evseeva GP, Lebedko OA. Incidence of asthma-like symptoms in adolescents of Khabarovsk and the Khabarovsk rural area, Russian Federation. Int J Pediatr 2020; 8 (12): 12697–12704. https://doi.org/10.22038/ijp.2020.53259.4230.

14. Glushkova AV, Grjibovski AM. Prevalence and correlates of asthma among children in central St. Petersburg, Russia: cross-sectional study. Croat Med J. 2008 Dec; 49 (6): 741–750. https://doi.org/10.3325/cmj.2008.49.741.

15. Kamaltynova YeM, Deyev IA, Belonogova YeG. Comparative epidemiological characteristics of bronchial asthma according to data of International Study of Asthma and Allergy in Childhood (ISAAC). Bulletin of Siberian medicine. 2009; 8 (4): 92–98. (In Russ.)] https://doi.org/10.20538/1682-0363-2009-4-92-97.

16. Batozhargalova BTs, Mizernitsky YuL, Podolnaya MA. Meta-analysis of the prevalence of asthma-like symptoms and bronchial asthma in Russia (based on the results of the ISAAC program). Russian Bulletin of Perinatology and Pediatrics. 2016; 61 (4): 59–69. (In Russ.)] https://doi.org/10.21508/1027-4065-2016-614-59-69.

17. Bragina EYu, Freidin MB, Puzyrev VP. Genetics of «atopic march» syntropy. Siberian Scientific Medical Journal. 2020; 40 (5): 4–17. [In Russ.] https://doi.org/10.15372/SSMJ20200501.

18. Martín Fernández-Mayoralas D, Martín Caballero JM, García-Marcos Alvarez L. Asociación entre dermatitis atópica, rinitisalérgica y asmaenescolares de 13 y 14 años [Association between atopic dermatitis, allergic rhinitis and asthma in schoolchildren aged 13–14 years old]. An Pediatr (Barc). 2004 Mar; 60 (3): 236–242. Spanish. https://doi.org/10.1016/s16954033(04)78257-0.

19. Eder W, Gamper A, Oberfeld G, Riedler J. Prävalenz und Schweregrad von Asthma bronchiale, allergischer Rhinitis und atopischer Dermatitis bei Salzburger Schulkindern [Prevalence and severity of bronchial asthma, allergic rhinitis and atopic dermatitis in Salzburg school children]. Wien Klin Wochenschr. 1998 Oct 16; 110 (19): 669–677. German. PMID: 9823620.

20. Montefort S, Lenicker HM, Caruna S, Agius Muscat H. Asthma, rhinitis and eczema in Maltese 13–15 year-old schoolchildren — prevalence, severity and associated factors [ISAAC]. International Study of Asthma and Allergies in Childhood. Clin Exp Allergy. 1998 Sep; 28 (9): 1089–1099. https://doi.org/10.1046/j.1365-2222.1998.00350.x. PMID: 9761012.

21. Falade AG, Olawuyi F, Osinusi K, Onadeko BO. Prevalence and severity of symptoms of asthma, allergic rhino-conjunctivitis and atopic eczema in secondary school children in Ibadan, Nigeria. East Afr Med J. 1998 Dec; 75 (12): 695–698. PMID: 10065208.

22. Phathammavong O, Ali M, Phengsavanh A, Xaysomphou D, Odajima H, Nishima S, Kuroiwa C. Prevalence and potential risk factors of rhinitis and atopic eczema among schoolchildren in Vientiane capital, Lao PDR: ISAAC questionnaire. Biosci Trends. 2008 Oct; 2 (5): 193–199. PMID: 20103927.

23. Ece A, Ceylan A, Saraçlar Y, Saka G, Gürkan F, Haspolat K. Prevalence of asthma and other allergic disorders among schoolchildren in Diyarbakir, Turkey. Turk J Pediatr. 2001 Oct-Dec; 43 (4): 286–292. PMID: 11765156.

24. Solis Soto MT, Patiño A, Nowak D, Radon K. Prevalence of asthma, rhinitis and eczema symptoms in rural and urban schoolaged children from Oropeza Province — Bolivia: a cross-sectional study. BMC Pulm Med. 2014 Mar 10; 14: 40. https://doi.org/10.1186/1471-2466-14-40.

25. Hasnain SM, Khan M, Saleem A, Waqar MA. Prevalence of asthma and allergic rhinitis among school children of Karachi, Pakistan, 2007. J Asthma. 2009 Feb; 46 (1): 86–90. https://doi.org/10.1080/02770900802513023.

26. Zhao T, Wang HJ, Chen Y, Xiao M, Duo L, Liu G, Lau Y, Karlberg J. Prevalence of childhood asthma, allergic rhinitis and eczema in Urumqi and Beijing. J Paediatr Child Health. 2000 Apr; 36 (2): 128–133. https://doi.org/10.1046/j.1440-1754.2000.00457.

27. Farrokhi S, Gheybi MK, Movahhed A, Dehdari R, Gooya M, Keshvari S, Gholampour H, Mansourian Z, Khosravi Y, Ghahramani F, Zandi S, Etemadan R, Tahmasebi R, Reaisi A, Keshmiri S, Fadaizadeh L, Masjedi MR. Prevalence and risk factors of asthma and allergic diseases in primary schoolchildren living in Bushehr, Iran: phase I, III ISAAC protocol. Iran J Allergy Asthma Immunol. 2014 Oct; 13 (5): 348–355. PMID: 25150076.

28. Zivković Z, Vukašinović Z, Cerović S, Radulović S, Zivanović S, Panić E, Hadnadjev M, Adžović O. Prevalence of childhood asthma and allergies in Serbia and Montenegro. World J Pediatr. 2010 Nov; 6 (4): 331–336. https://doi.org/10.1007/s12519010-0207-y.

29. Teeratakulpisarn J, Wiangnon S, Kosalaraksa P, Heng S. Surveying the prevalence of asthma, allergic rhinitis and eczema in school-children in Khon Kaen, Northeastern Thailand using the ISAAC questionnaire: phase III. Asian Pac J Allergy Immunol. 2004 Dec; 22 (4): 175–181. PMID: 15783129.

30. Amarasekera ND, Gunawardena NK, de Silva NR, Weerasinghe A. Prevalence of childhood atopic diseases in the Western Province of Sri Lanka. Ceylon Med J. 2010 Mar; 55 (1): 5–8. https://doi.org/10.4038/cmj.v55i1.1700.

31. Kabir ML, Rahman F, Hassan MQ, Ahamed F, Mridha MA. Asthma, atopic eczema and allergic rhino-conjunctivitis in school children. Mymensingh Med J. 2005 Jan; 14 (1): 41–45. PMID: 15695953.

32. Quah BS, Razak AR, Hassan MH. Prevalence of asthma, rhinitis and eczema among schoolchildren in Kelantan, Malaysia. Acta Paediatr Jpn. 1997 Jun; 39 (3): 329–335. https://doi.org/10.1111/j.1442-200x.1997.tb03746.x.

33. Rahimi Rad MH, Hejazi ME, Behrouzian R. Asthma and other allergic diseases in 13–14-year-old schoolchildren in Urmia, Iran. [corrected]. East Mediterr Health J. 2007 Sep-Oct; 13 (5): 1005–1016. https://doi.org/10.26719/2007.13.5.1005. Erratum in: East Mediterr Health J. 2009 Nov-Dec; 15 (6): 1364. PMID: 18290392.

34. Solé D, Cassol VE, Silva AR, Teche SP, Rizzato TM, Bandim LC, Sarinho ES, Camelo-Nunes IC. Prevalence of symptoms of asthma, rhinitis, and atopic eczema among adolescents living in urban and rural areas in different regions of Brazil. Allergol Immunopathol (Madr). 2007 Nov-Dec; 35 (6): 248–253. https://doi.org/10.1157/13112991.

35. Standardized epidemiology researches of allergic diseases for children. Adaptation of the program «International research of asthma and allergy for children («ISAAC») in Russia. Moscow, 1998. 30 s. (In Russ.)]

36. Brożek JL, Bousquet J, Agache I, Agarwal A, Bachert C, Bosnic-Anticevich S, Brignardello-Petersen R, Canonica GW, Casale T, Chavannes NH, Correia de Sousa J, Cruz AA, Cuello-Garcia CA, Demoly P, Dykewicz M, Etxeandia-Ikobaltzeta I, Florez ID, Fokkens W, Fonseca J, Hellings PW, Klimek L, Kowalski S, Kuna P, Laisaar K-T, Larenas-Linnemann DE, Lødrup Carlsen KC, Manning PJ, Meltzer E, Mullol J, Muraro A, O’Hehir R, Ohta K, Panzner P, Papadopoulos N, Park H-S, Passalacqua G, Pawankar R, Price D, Riva JJ, Roldán Y, Ryan D, Sadeghirad B, Samolinski B, Schmid-Grendelmeier P, Sheikh A, Togias A, Valero A, Valiulis A, Valovirta E, Ventresca M, Wallace D, Waserman S, Wickman M, Wiercioch W, Yepes-Nuñez JJ, Zhang L, Zhang Y, Zidarn M, Zuberbier T, Schünemann HJ, Allergic Rhinitis and its Impact on Asthma (ARIA) Guidelines. 2016 Revision, Journal of Allergy and Clinical Immunology (2017). https://doi.org/10.1016/j.jaci.2017.03.050.

37. Shamssain MH, Shamsian N. Prevalence and severity of asthma, rhinitis, and atopic eczema in 13- to 14-year-old schoolchildren from the northeast of England. Ann Allergy Asthma Immunol. 2001 Apr; 86 (4): 428–432. https://doi.org/10.1016/S10811206(10)62490-8.

38. John Asekhaen Ohiolei, Clement Isaac, Oriri Asemota Omorodion. A review of soil transmitted helminthiasis in Nigeria. Asian Pacific Journal of Tropical Disease. 2017; 7 (12): 841–848. https://doi.org/10.12980/apjtd.7.2017D7-235.