Skin prick reactivity among asthmatics in East Africa

Richard Kwizera, Vincent Wadda, Levicatus Mugenyi, Hellen Aanyu-Tukamuhebwa, George Nyale, Getnet Yimer, Jeremiah Chakaya, Corina De Jong, Thys Van der Molen, David W Denning, Robin Gore, Bruce J Kirenga, Richard Kwizera, Vincent Wadda, Levicatus Mugenyi, Hellen Aanyu-Tukamuhebwa, George Nyale, Getnet Yimer, Jeremiah Chakaya, Corina De Jong, Thys Van der Molen, David W Denning, Robin Gore, Bruce J Kirenga

Abstract

Background: The burden of asthma in Africa is high, and yet the disease is not universally prioritised. Data on allergic asthma and its impact on asthma morbidity are limited in Africa. Our aim was to describe the distribution of skin prick positivity among asthmatics in Eastern Africa.

Methods: From August 2016 to May 2018, 1671 asthmatic patients were enrolled from Uganda, Kenya, and Ethiopia as part of the African Severe Asthma Program clinical study. Skin prick testing was performed at baseline using a panel of 12 allergens, and factors associated with skin prick reactivity determined.

Results: Of the 1, 671 patients recruited, 71% were female with a median age of 40 years, 93.6% were aged >15 years and the patterns of asthma symptom frequency was intermittent in 2.9%, mild persistent in 19.9%, moderate persistent in 42.6% and severe persistent in 34.6% at baseline. Self-reported triggers, were dust (92%), cold weather (89%), upper respiratory infections (84%), strong smells (79%) and exposure to tobacco (78%). The majority (90%) of the participants had at least 1 positive allergen reaction, with 0.9% participants reacting to all the 12 allergens. Participants commonly reacted to house dust mites (66%), Blomia tropicalis (62%), and the German cockroach (52%). Patients sensitized to more allergens (>2) had significantly reduced lung function (FEV ≤ 80%; p = 0.001) and were more likely to visit the emergency department due to asthma (p = 0.012). There was no significant relationship between number of allergens and measures of asthma control, quality of life, and other clinical outcomes. Only the country of origin was independently associated with atopy among African asthmatics.

Conclusion: There is a high prevalence of skin prick positivity among East African patients with asthma, with the commonest allergen being house dust mite. Skin reactivity did not correlate well with asthma severity and poor asthma control. The relation between atopy, measured through skin prick testing, and measures of asthma control among asthma patients in Eastern Africa is unclear and needs further study.

Trial registration: The ASAP study was registered prospectively. ClinicalTrials.gov Identifier: NCT03065920; Registration date: February 28, 2017; Last verified: February 28, 2017.

Keywords: A. fumigatus, Aspergillus fumigatus; ACT, Asthma control test; AQLQ, Asthma Quality of Life Questionnaire; ASAP, African Severe Asthma Project; Africa; Allergy; Asthma; Atopy; COPD, Chronic obstructive pulmonary disease; East Africa; FEV, Forced Expiratory Volume; HIV, Human immunodeficiency virus; IQR, Interquartile range; Ig, Immunoglobulin; SPT; SPT, Skin prick testing; TB, Tuberculosis.

© 2020 Published by Elsevier Inc. on behalf of World Allergy Organization.

Figures

Fig. 1
Fig. 1
Distribution of allergens in adults. Figure shows the percentage positivity for each allergen per country among adults (16+ years). Participants mostly reacted to house dust mites, Blomia tropicalis and the German cockroach
Fig. 2
Fig. 2
Distribution of allergens in children. Figure shows the percentage positivity for each allergen per country among adults (12–15 years). Participants mostly reacted to house dust mites, Blomia tropicalis and the German cockroach
Fig. 3
Fig. 3
Percentage positivity of allergens per patient. The number of positive allergens per patient varied widely across the 3 countries. Ten percent of the participants did not react to any of the allergens, while 1% reacted to all the 12 allergens. Ugandans had a noticeably higher degree of atopy

References

    1. Asher M.I., Ellwood P. Global Asthma Network; Auckland: 2014. The Global Asthma Report 2014; pp. 16–17. 0473291266 0473291266.
    1. Bateman E.D., Hurd S.S., Barnes P.J. Global strategy for asthma management and prevention: GINA executive summary. Eur Respir J. 2008;31(1):143–178. doi: 10.1183/09031936.00138707.
    1. Wechsler M.E. Elsevier; 2009. Managing Asthma in Primary Care: Putting New Guideline Recommendations into Context; pp. 707–717.
    1. Adeloye D., Chan K.Y., Rudan I., Campbell H. An estimate of asthma prevalence in Africa: a systematic analysis. Croat Med J. 2013;54(6):519–531. doi: 10.3325/cmj.2013.54.519.
    1. Asher M.I., Montefort S., Bjorksten B. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet. 2006;368(9537):733–743. doi: 10.1016/S0140-6736(06)69283-0.
    1. Kwizera R., Musaazi J., Meya D.B. Burden of fungal asthma in Africa: a systematic review and meta-analysis. PLoS One. 2019;14(5) doi: 10.1371/journal.pone.0216568. e0216568.
    1. Zhong N.S. New insights into risk factors of asthma. Respirology. 1996;1(3):159–166.
    1. Johansson S., Bieber T., Dahl R. Revised nomenclature for allergy for global use: report of the nomenclature review committee of the world allergy organization, october 2003. Journal of allergy and clinical immunology. 2004;113(5):832–836.
    1. Rasool R., Shera I.A., Nissar S. Role of skin prick test in allergic disorders: a prospective study in Kashmiri population in light of review. Indian J Dermatol. 2013;58(1):12–17. doi: 10.4103/0019-5154.105276.
    1. van Kampen V., de Blay F., Folletti I. EAACI position paper: skin prick testing in the diagnosis of occupational type I allergies. Allergy. 2013;68(5):580–584. doi: 10.1111/all.12120.
    1. Heinzerling L., Mari A., Bergmann K.-C. The skin prick test–European standards. Clinical and translational allergy. 2013;3(1):3.
    1. Ansotegui I.J., Melioli G., Canonica G.W. IgE allergy diagnostics and other relevant tests in allergy, a World Allergy Organization position paper. World Allergy Organ J. 2020;13(2):100080. doi: 10.1016/j.waojou.2019.100080.
    1. Bryant D., Burns M., Lazarus L. The correlation between skin tests, bronchial provocation tests and the serum level of IgE specific for common allergens in patients with asthma. Clinical & Experimental Allergy. 1975;5(2):145–157.
    1. O'Brien R.M. Skin prick testing and in vitro assays for allergic sensitivity. Australian Prescriber. 2002;25(4):91–93.
    1. Haahtela T., Burbach G.J., Bachert C. Clinical relevance is associated with allergen-specific wheal size in skin prick testing. Clin Exp Allergy. 2014;44(3):407–416. doi: 10.1111/cea.12240.
    1. Addo-Yobo E.O., Custovic A., Taggart S.C., Craven M., Bonnie B., Woodcock A. Risk factors for asthma in urban Ghana. J Allergy Clin Immunol. 2001;108(3):363–368. doi: 10.1067/mai.2001.117464.
    1. Motala C., Hawarden D. Diagnostic testing in allergy. SAMJ: South African Medical Journal. 2009;99(7):531–535.
    1. Kirenga B. 2017. African severe asthma Program (ASAP) February 28, 2017. Retrieved 14/08/2018, 2018, from.
    1. Kirenga B., Muttamba W., Mugenyi L. AMER THORACIC SOC; 25 BROADWAY, 18 FL, NEW YORK, NY 10004 USA: 2018. A Prospective Cohort Study of Severe Asthma and its Determinants in an African Population: The African Severe Asthma Program.
    1. Schatz M., Sorkness C.A., Li J.T. Asthma Control Test: reliability, validity, and responsiveness in patients not previously followed by asthma specialists. Journal of Allergy and Clinical Immunology. 2006;117(3):549–556.
    1. Bousquet J., Mantzouranis E., Cruz A.A. Uniform definition of asthma severity, control, and exacerbations: document presented for the World Health Organization Consultation on Severe Asthma. J Allergy Clin Immunol. 2010;126(5):926–938. doi: 10.1016/j.jaci.2010.07.019.
    1. Juniper E.F., Svensson K., Mork A.C., Stahl E. Modification of the asthma quality of life questionnaire (standardised) for patients 12 years and older. Health Qual Life Outcomes. 2005;3(1):58. doi: 10.1186/1477-7525-3-58.
    1. Dreborg S. The skin prick test in the diagnosis of atopic allergy. J Am Acad Dermatol. 1989;21(4 Pt 2):820–821. doi: 10.1016/s0190-9622(89)70256-5.
    1. ASCIA . 2016. Skin prick testing for the diagnosis of allergic disease: a manual for practitioners. March 2016. Retrieved 15 January 2020, from.
    1. Heinzerling L., Mari A., Bergmann K.C. The skin prick test - European standards. Clin Transl Allergy. 2013;3(1):3. doi: 10.1186/2045-7022-3-3.
    1. Jensen-Jarolim E., Jensen A.N., Canonica G.W. Debates in allergy medicine: molecular allergy diagnosis with ISAC will replace screenings by skin prick test in the future. World Allergy Organ J. 2017;10(1):33. doi: 10.1186/s40413-017-0162-3.
    1. Malling H.J., Allesen-Holm P., Karved L.S., Poulsen L.K. Proficiency testing of skin prick testers as part of a quality assurance system. Clin Transl Allergy. 2016;6:36. doi: 10.1186/s13601-016-0126-7.
    1. Mpairwe H., Muhangi L., Ndibazza J. Skin prick test reactivity to common allergens among women in Entebbe, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2008;102(4):367–373.
    1. Liam C.K., Loo K.L., Wong C.M., Lim K.H., Lee T.C. Skin prick test reactivity to common aeroallergens in asthmatic patients with and without rhinitis. Respirology. 2002;7(4):345–350.
    1. Montealegre F., Quinones C., Michelen V. Prevalence of skin reactions to aeroallergens in asthmatics of Puerto Rico. P R Health Sci J. 1997;16(4):359–367.
    1. Koshak E.A. Skin test reactivity to indoor allergens correlates with asthma severity in jeddah, Saudi Arabia. Allergy Asthma Clin Immunol. 2006;2(1):11–19. doi: 10.1186/1710-1492-2-1-11.
    1. Peat J.K., Tovey E., Toelle B.G. House dust mite allergens. A major risk factor for childhood asthma in Australia. Am J Respir Crit Care Med. 1996;153(1):141–146. doi: 10.1164/ajrccm.153.1.8542107.
    1. Sporik R., Holgate S.T., Platts-Mills T.A., Cogswell J.J. Exposure to house-dust mite allergen (Der p I) and the development of asthma in childhood. A prospective study. N Engl J Med. 1990;323(8):502–507. doi: 10.1056/NEJM199008233230802.
    1. Arshad S.H., Tariq S.M., Matthews S., Hakim E. Sensitization to common allergens and its association with allergic disorders at age 4 years: a whole population birth cohort study. Pediatrics. 2001;108(2):E33.
    1. Boulet L.P., Turcotte H., Laprise C. Comparative degree and type of sensitization to common indoor and outdoor allergens in subjects with allergic rhinitis and/or asthma. Clinical & Experimental Allergy. 1997;27(1):52–59.
    1. Arruda L.K., Rizzo M., Chapman M.D. Exposure and sensitization to dust mite allergens among asthmatic children in Sao Paulo, Brazil. Clinical & Experimental Allergy. 1991;21(4):433–439.
    1. Murray A.B., Ferguson A.C. Dust-free bedrooms in the treatment of asthmatic children with house dust or house dust mite allergy: a controlled trial. Pediatrics. 1983;71(3):418–422.
    1. Woodcock A., Forster L., Matthews E. Control of exposure to mite allergen and allergen-impermeable bed covers for adults with asthma. N Engl J Med. 2003;349(3):225–236. doi: 10.1056/NEJMoa023175.
    1. Peat J., Woolcock A. Sensitivity to common allergens: relation to respiratory symptoms and bronchial hyper-responsiveness in children from three different climatic areas of Australia. Clinical & Experimental Allergy. 1991;21(5):573–581.
    1. Lau S., Illi S., Sommerfeld C. Early exposure to house-dust mite and cat allergens and development of childhood asthma: a cohort study. Multicentre Allergy Study Group. Lancet. 2000;356(9239):1392–1397. doi: 10.1016/s0140-6736(00)02842-7.
    1. Gøtzsche P.C., Johansen H.K. House dust mite control measures for asthma. Cochrane Database of Systematic Reviews. 2008;(2)
    1. Andiappan A.K., Puan K.J., Lee B. Allergic airway diseases in a tropical urban environment are driven by dominant mono-specific sensitization against house dust mites. Allergy. 2014;69(4):501–509. doi: 10.1111/all.12364.
    1. Santos A.B.R., Chapman M.D., Aalberse R.C. Cockroach allergens and asthma in Brazil: identification of tropomyosin as a major allergen with potential cross-reactivity with mite and shrimp allergens. Journal of Allergy and Clinical Immunology. 1999;104(2):329–337.
    1. Jeong K.Y., Kim C.R., Park J., Han I.S., Park J.W., Yong T.S. Identification of novel allergenic components from German cockroach fecal extract by a proteomic approach. Int Arch Allergy Immunol. 2013;161(4):315–324. doi: 10.1159/000347034.
    1. Arruda L.K., Vailes L.D., Ferriani V.P., Santos A.B.R., Pomés A., Chapman M.D. Cockroach allergens and asthma. Journal of allergy and clinical immunology. 2001;107(3):419–428.
    1. Bush R.K., Prochnau J.J. Alternaria-induced asthma. J Allergy Clin Immunol. 2004;113(2):227–234. doi: 10.1016/j.jaci.2003.11.023.
    1. O'Driscoll B.R., Hopkinson L.C., Denning D.W. Mold sensitization is common amongst patients with severe asthma requiring multiple hospital admissions. BMC pulmonary medicine. 2005;5(1):4.
    1. Denning D., O'driscoll B., Hogaboam C., Bowyer P., Niven R. The link between fungi and severe asthma: a summary of the evidence. European Respiratory Journal. 2006;27(3):615–626.
    1. Menzies D., Holmes L., McCumesky G., Prys-Picard C., Niven R. Aspergillus sensitization is associated with airflow limitation and bronchiectasis in severe asthma. Allergy. 2011;66(5):679–685.
    1. Fairs A., Agbetile J., Hargadon B. IgE sensitization to Aspergillus fumigatus is associated with reduced lung function in asthma. American journal of respiratory and critical care medicine. 2010;182(11):1362–1368.
    1. Agarwal R., Noel V., Aggarwal A.N., Gupta D., Chakrabarti A. Clinical significance of Aspergillus sensitisation in bronchial asthma. Mycoses. 2011;54(5):e531–e538. doi: 10.1111/j.1439-0507.2010.01971.x.
    1. Kwizera R., Bongomin F., Meya D.B., Denning D.W., Fahal A.H., Lukande R. Mycetoma in Uganda: a neglected tropical disease. PLOS Neglected Tropical Diseases. 2020;14(4) doi: 10.1371/journal.pntd.0008240. e0008240.
    1. Kwizera R., Bongomin F., Lukande R. Deep fungal infections diagnosed by histology in Uganda: a 70-year retrospective study. Med Mycol. 2020:1–9. doi: 10.1093/mmy/myaa018.
    1. WHO . World Health Organization; Geneva: 2003. Prevention and Control of Chronic Respiratory Diseases in Low and Middle-Income African Countries: A Preliminary Report. WHO/MNC/CRA/02.2 WHO/MNC/CRA/02.2 22.
    1. Olanrewaju F.O., Ajayi L.A., Loromeke E. Masculinity and men's health-seeking behaviour in Nigerian academia. Cogent Social Sciences. 2019;5(1):1682111. doi: 10.1080/23311886.2019.1682111.
    1. Yawn B.P., Wollan P., Kurland M., Scanlon P. A longitudinal study of the prevalence of asthma in a community population of school-age children. J Pediatr. 2002;140(5):576–581. doi: 10.1067/mpd.2002.123764.
    1. Wright A.L., Stern D.A., Kauffmann F., Martinez F.D. Factors influencing gender differences in the diagnosis and treatment of asthma in childhood: the Tucson Children's Respiratory Study. Pediatr Pulmonol. 2006;41(4):318–325. doi: 10.1002/ppul.20373.
    1. Radhakrishnan D.K., Dell S.D., Guttmann A., Shariff S.Z., Liu K., To T. Trends in the age of diagnosis of childhood asthma. J Allergy Clin Immunol. 2014;134(5):1057–1062. doi: 10.1016/j.jaci.2014.05.012. e1055.
    1. Guilbert T.W., Morgan W.J., Zeiger R.S. Atopic characteristics of children with recurrent wheezing at high risk for the development of childhood asthma. Journal of Allergy and Clinical Immunology. 2004;114(6):1282–1287.
    1. Haldar P., Pavord I.D., Shaw D.E. Cluster analysis and clinical asthma phenotypes. Am J Respir Crit Care Med. 2008;178(3):218–224. doi: 10.1164/rccm.200711-1754OC.
    1. Wenzel S.E. Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med. 2012;18(5):716–725. doi: 10.1038/nm.2678.
    1. Romanet-Manent S., Charpin D., Magnan A., Lanteaume A., Vervloet D., Group E.C. Allergic vs nonallergic asthma: what makes the difference? Allergy. 2002;57(7):607–613.
    1. Gilliland F.D. Outdoor air pollution, genetic susceptibility, and asthma management: opportunities for intervention to reduce the burden of asthma. Pediatrics. 2009;123(Suppl 3):S168–S173. doi: 10.1542/peds.2008-2233G.
    1. Kemp S., deShazo R.D. UpToDate: UpToDate; Waltham, MA: 2012. Relationships between Rhinosinusitis and Asthma.

Source: PubMed

3
Iratkozz fel