December 2008 no white pages.indd ABSTRACT Objective: Identification of relevant allergens that are prevalent in each environment which may have diagnostic and therapeutic implications in allergic diseases. This study aimed to identify the pattern of sensitisation to inhalant allergens in Omani patients with asthma, allergic rhinitis and rhinoconjunctivitis. Methods: The study was carried out during three consecutive years (2004-2006) at the allergy skin test laboratory of Sultan Qaboos University Hospital, Oman. Records of patients who had undergone an allergy skin prick test with a referring diagnosis of asthma, allergic rhinitis or rhinoconjunctivitis were reviewed. Two panels were used during the 3 years period. The frequencies of positive skin tests were analysed. Results: 689 patients were tested, 384 for the first panel and 305 for the second panel. In the first panel, the commonest positive allergens were: house dust mites (37.8%), hay dust (35.4%), feathers (33.3%), sheep wool (26.6%), mixed threshing dust (25.8%), cat fur (24.2%), cockroach (22.7%), straw dust (22.7%), horse hair (7.4%), maize (6.%), grasses (.5%), cotton flock (0.7%), trees (0.4%), cow hair (7.8%), Alternaria alternata (3.6%), Aspergillus Niger (3.4%), and Aspergillus fumigatus (.3%). In the second panel, the commonest positive allergens were also house dust mites: Dermat- ophagoides pteronyssinus (50.8%), Dermatophagoides farinae (47.9%); Mesquite (Prosopis glandulosa) (35.7%), Russian thistle (Salsola kali) (34.4%), cockroach (32.%), Bermuda grass (Cynodon dactylon) (9.7%), grass mix-five standard (8.0%), wheat cultivate (4.%), cats (3.8%), Penicillium notatum (4.3%), Alternaria tenius (3.9%), Aspergillus Niger (3.3%), feather mix (3.0%), dog (2.6%), horse hair and dander (2.6%), and Aspergillus fumigatus (.6%). Conclusion: The pattern of sensitisation to environmental allergens in Oman seems to be similar to other reports from the Arabian Peninsula. Methods to identify and characterise environment specific allergens The Pattern of Sensitisation to Inhalant Allergens in Omani Patients with Asthma, Allergic Rhinitis and Rhinoconjunctivitis *Salem H Al-Tamemi,1 Azza N Al-Shidhani,1 Rashid K Al-Abri,2 Balaji Jothi,3 Omar A Al-Rawas,4 Bazdawi M Al-Riyami4 Departments of 1Child Health, 2Surgery, 3Clinical Physiology, Sultan Qaboos University Hospital, Muscat, Sultanate of Oman; 4Department of Medicine, College of Medicine & Health Sciences, Sultan Qaboos University, Muscat, Sultanate of Oman. *To whom correspondence should be addressed. Email: tamemi@squ.edu.om املصابني العمانيني عند املستنشقة أرِجات تَ سْ للمُ التحسيس منط والعينني األنف وحساسية الربو، مبرض الريامي بازدوي الرواس، عمر باالجي جوثي، ، العبري راشد الشيذاني، التميمي، عزا سالم احلساسية. أمراض وعالج تشخيص عملية مهما في يكون أن ميكن كل بيئة في املنتشرة املهمة النشوقة تَأرِجات ُسْ امل على امللخص: الهدف: التعرف والعينني. األنف ــية وحساس الربو مبرض املصابني العمانيني عند ــوقة النش ــتَأرِجات سْ للمُ ــيس التحس نوعية على التعرف تهدف إلى ــة هذه الدراس اجللد فحص حساسية مختبر في (2006-2004) متتالية ــنوات س ثالث خالل ــية أجروا فحص احلساس الذين املرضى ــجالت مراجعة س مت الطريقة: احلساسية من مستخلصات استخدام مت كما والعينني. األنف وحساسية الربو يعانون من أنهم والذي تبني قابوس السلطان جامعة مستشفى في عدد النتائج: كان ــتخدم. مس بيئي ــتأرج مس لكل اجللدي ــية احلساس لفحص املوجبة البيانات ــاب مت حس مختلفتني. فترتني في مختلفني مصنعني في ــنة، 30 س هو تكرر عمر أكثر وكان 5-81 عاما، بني العمر تراوح . الثانية الفترة و305 في في الفترة األولى 384 منهم مت فحص ، 689 املرضى (26.6%) اخلرفان وصوف الطيور(33.3%) ريش ثم ،(35.4%) القش غبار يليها ، (37.8%) غبار البيت ــوس س كانت أرِجات ــتَ ُسْ أكثر امل األولى الفترة ــاب ، واألعش (16.1%) الذرة %17.4 و اخليول ــعر %22.7 وغبار القصب%22.7 و ش الصراصير %24.2 و القطط ــعر وش (25.8%) الوط والغبار ناء خْ الدَّ يَّةُ اشِ الرَّشَّ و (3.4%) وداء السَّ يَّةُ اشِ الرَّشَّ و (3.6%) ُتَناوِبَة امل والنَّوباءُ (7.8%) البقر وشعر (10.4%) (10.7 %) واألشجار والقطن (11.5%) ــجر ،ش (47.9%) الدقيق ة مَ تَضِ قْ مُ ،(50.8%) ــة ُنْتَسَّ امل ةُ مَ تَضِ ُقْ امل أيضا: البيت غبار ــوس ــتَأرِجات س ُسْ امل أكثر كانت الفترة الثانية في أما .(1.3%) نبات احلنطة ، (18%) خليط أعشاب ، (19.7%) برمودا عشب ، (32.1%) الصراصير كالي) (34.4%) (سالسوال روسي ثيستل ، (35.7%) الغاف الطيور ريش خليط ، (3.3%) ــوداء السَّ يَّةُ اشِ الرَّشَّ ، (3.9%) ــريطية الش ، النوباء (4.3%) يَّنَة ُعَ امل ــيَّةُ نَسِ ِكْ امل ، (13.8%) ــعرالقطط ، ش (14.1%) تَأرِجات ُسْ عن امل الناجتة ــية احلساس اخلالصة: طبيعة .(1.6%) الدخناء ــية والرشاش (2.6%) وقشرته اخليول ــعر ش (2.6%) الكالب ــعر ، ش (3%) وتصنيفها البيئة في اخلاصة النشوقة تَأرِجات ُسْ على امل التعرف .طرق العربية في اجلزيرة نشرت لدراسات مشابهة تبدوا عمان النشوقة البيئية في والعينني. األنف وعالج مرضى الربو وحساسية تشخيص على يساعد رمبا عمان. فحص اجللد، سلطنة تَأرِجات, ُسْ امل العينني ، ، األنف حساسية ، ، الكلمات: الربو مفتاح SULTAN QABOOS UNIVERSITY MEDICAL JOURNAL NOVEMBER 2008, VOLUME 8, ISSUE 3, P. 319-324 SULTAN QABOOS UNIVERSITY© SUBMITTED - 26RD FEBRUARY 2008 ACCEPTED - 8TH MAY 2008 C L I N I C A L A N D B A S I C R E S E A R C H S A L E M H A L -TA M E M I , A Z Z A N A L -S H I D H A N I , R A S H I D K A L - A B R I , B A L A J I J O T H I , O M A R A A L - R AWA S A N D B A Z D AW I M A L - R I YA M I 320 ENVIRONMENTAL ALLERGENS ARE IMPORTANT immunopathogens that contribute to the pathophysiology of allergic diseases repre- sented mainly by bronchial asthma, allergic rhinitis and rhinoconjuctivitis. It is very important to iden- tify the most relevant allergens in each environment as they differ from one to another. This has diagnos- tic and therapeutic implications. These patients may benefit from environmental allergen control measures and, where medical therapy is not sufficient to control their symptoms, immunotherapy might be beneficial; hence, the identification of allergens is vital. Atopy is the tendency of an individual to develop specific IgE against common allergens in the environ- ment. IgE mediates the early phase response of an al- lergic reaction by involving mast cells as an effecter cell that release chemical mediators which are responsible for the clinical features of an allergic reaction.1, 2 Asth- ma is a worldwide problem that affects around 10-15% of all populations. In Omani children, as assessed by ISAAC study, the prevalence rates of reported diag- noses of asthma and allergic rhinitis were higher in older children, 20.7% and 10.5%, compared with 10.5% and 7.4% respectively, in younger children.3 Asthma is a chronic inflammatory airway disease characterised by the presence of inflammatory cells and cytokines in the airway mucosa that lead to inflammation re- sponsible for the symptoms of asthma. The etiology of asthma is multifactorial, the role of allergy in asthma is well established; for example, there is a strong link be- tween house dust mites (HDM) sensitisation and the development of asthma.4, 5 Allergic rhinitis is a com- mon medical condition characterised by nasal, throat, and ocular itching; rhinorrhea; sneezing; nasal con- gestion and, less frequently, coughing. Patients could be sensitised to perennial or seasonal allergens that are present in the environment. Patients with allergic rhinitis may benefit from specific immunotherapy in case medical treatment is insufficient to control their symptoms.6, 7, 8 There is now evidence supporting a link between asthma and allergic rhinitis which may have therapeutic implications.9 Most of the experi- ence of environmental allergies comes from the West- ern hemisphere. There are several studies conducted in neighbouring countries which have shown a dif- ferent pattern of allergies from the West.10-15 Little is known about the pattern of environmental allergies in Oman.16 The aim of this study was to identify the pat- Advances in Knowledge • Environmental allergens are well identified and characterised in Western countries, but only a few reports have been published on environmental allergies from the Arabian Peninsula, mainly from Kuwait and Saudi Arabia. • Each environment may have unique allergens that may contribute to the pathogenesis of allergic diseases. • This paper highlights the pattern of sensitisation in Omani patients with asthma, allergic rhinitis and rhino- conjunctivitis, • The common and uncommon allergens are identified for skin testing in Omani patients. This opens up the potential for other allergens to be included in the panel of skin testing. Application to Patient Care • Patients should be tested with a panel of allergen extracts that would identify the highest number of sen- sitising agents that may contribute to their allergic disease; hence measures could be instituted to avoid exposure to the responsible allergens. • Immunotherapy for allergic diseases is dependent on identifying the sensitising agents. • This can make postoperative management more specific and result oriented. like a pollen survey may help in the management of patients with allergic asthma, allergic rhinitis and rhinoconjunctivitis. Key words: Asthma; Allergic; Rhinitis; Conjunctivitis; Allergens; Skin tests; Oman. TH E PAT T E R N O F S E N S I T I S AT I O N T O I N H A L A N T A L L E R G E N S I N O M A N I PAT I E N T S W I T H A S T H M A , A L L E R G I C R H I N I T I S & R H I N O C O N J U N C T I V I T I S 321 tern of sensitisation to inhalant allergens in Omani patients with asthma, allergic rhinitis and rhinocon- junctivitis. M E T H O D S Medical records of allergy skin tests of patients with a referring diagnosis of asthma, or allergic rhinitis or rhinoconjunctivitis for three consecutive years 2004- 2006 were reviewed. The patients had been referred to the allergy skin test laboratory from the pulmo- nary, ENT, child health, and other clinics at Sultan Qaboos University Hospital (SQUH) and Ministry of Health hospitals in Oman. SQUH is the referral centre for allergy skin testing for the whole country. The al- lergy laboratory is supervised by pulmonologists and recently by an allergist. Patients consents verbally for the skin prick tests. There were two panels of extracts used during the three year period, bought from two different compa- nies, and represented by two different graphs in the re- sults. The panel of allergens used consisted of common inhalant allergens believed to be of significance. In the first period, the extracts used were bought from Ben- card Company. In the second period, the extracts used were bought from Allergy Laboratories, Inc., USA. Skin prick tests were performed by qualified techni- cians according to standard method.17 Disposable Greenlan needles, lancet 23G, were used to prick the skin. Histamine positive control and diluent negative control were used. A skin test was considered positive when a wheal was 3 mm greater than the negative con- trol. Eight patients (7 from the first period and 1 from Figure 1: Number of patients with positive tests and cumulative percentage of positive tests during the first period Number = 689 Percentage % Age Category < 12 years ≥ 12 years Sex Male Female Nationality Omani Non-Omani Referring Clinic Chest ENT Child Health Ophthalmology Other Diagnosis Asthma Allergic rhinitis Rhinoconjuctivitis 28 661 314 375 635 54 264 327 9 1 88 271 420 13 4.1 95.9 45.6 54.4 92.2 7.8 38.3 47.5 1.3 0.1 12.8 39.3 61.0 1.9 Table 1: Patient data S A L E M H A L -TA M E M I , A Z Z A N A L -S H I D H A N I , R A S H I D K A L - A B R I , B A L A J I J O T H I , O M A R A A L - R AWA S A N D B A Z D AW I M A L - R I YA M I 322 the second period) were not included in the analysis as they had negative histamine control; none tested posi- tive for negative control. Using the Statistical Package for the Social Sciences (SPSS), data were entered into two different sheets. For the analysis of baseline characteristics, the data were combined and frequencies were calculated. The two panels of allergens were analysed separately, as they are different and the frequencies were calculated. R E S U L T S There were a total of 689 patients with asthma, allergic rhinitis and rhinoconjuctivitis tested during the study period. A total of 384 were tested for the first panel and 305 for the second panel. The youngest patient was 5 years old and the oldest 81 years old; the median age was 30 years. The majority of patients were re- ferred from the chest and ENT clinics. Of the patients tested, 39.2% had a diagnosis of asthma, 61.3% allergic rhinitis and 1.9% rhinoconjuctivitis. Baseline data are summarised in Table 1. During the first period [Figure 1], the commonest positive allergen was house dust mites with 37.8% of patients being sensitis ed, hay dust (35.4%), straw dust (22.7%), mixed threshing dust (25.8%), grasses (11.5%) (in 11 cases the extract was not available), trees (10.4%), maize (16.1%), cotton flock (10.7%), animal allergens, sheep wool (26.6%), horse hair (17.4%), cat fur (24.2%), cow hair (7.8%), feathers (33.3%), cockroaches (22.7%) (in 19 cases the extract was not available); mould al- lergens: Alternaria alternata (3.6%), Aspergillus Niger (3.4%), and Aspergillus fumigatus (1.3%). During the second period [Figure 2], the com- monest positive allergens were also house dust mites: Dermatophagoides pteronyssinus (50.8%), Dermat- ophagoides farinae (47.9%); pollen allergens: mesquite (Prosopis glandulosa) (35.7%), Russian thistle (Sal- sola kali) (34.4%), Bermuda grass (Cynodon dactylon) (19.7%), grass mix-five standard (18.0%) and wheat cultivate (14.1%) [in 2 cases the extracts were not avail- able]; animal allergens: cat (13.8%), dog (2.6%), horse hair and dander (2.6%), feather mix 3.0%; moulds: As- pergillus Niger (3.3%), Aspergillus fumigatus (1.6%), Penicillium notatum (4.3%) [in 11 cases the extract was not available] and Alternaria tenius (3.9%) and cockroach (32.1%). Figure 2: Number of patients with positive tests and cumulative percentage of positive tests during the second period TH E PAT T E R N O F S E N S I T I S AT I O N T O I N H A L A N T A L L E R G E N S I N O M A N I PAT I E N T S W I T H A S T H M A , A L L E R G I C R H I N I T I S & R H I N O C O N J U N C T I V I T I S 323 D I S C U S S I O N In this study, we are able to demonstrate that house dust mites are the commonest sensitisation in Omani patients; half of all patients were sensitised to them which is in agreement with other studies conducted on asthmatic patients elsewhere.18 About one third of patients were sensitised to mesquite tree and Rus- sian thistle, both common plants in Oman. Grasses contributed to 10% of cases. However, there are oth- er plants in Oman that are potentially allergenic like date palm (phoenix dactylifera), a widely planted tree in Oman, for which it may be necessary to test. The families of Chenopodiaceous and Compositae plants both exist in Oman and may contribute to sensitis- ing agents. Hay dust, straw dust and mixed thresh- ing contributed to about one third in the first period, but these were not individual allergens. One third of patients were sensitised to cockroaches implicating a significant contribution. In Oman, animals are not often allowed into hous- es, but sometimes there are domestic cats and dogs that stay around houses and people might get ex- posed to their allergens. Horses are mainly raised in stables and exposure might be limited to people that work with them. The difference in rate of sensitisation between the two panels could be because of lack of standardised allergen extracts from different manu- facturers. Some people raise cattle, goat and sheep in small farms attached to the backyard of their houses. Pigeons are found in Oman; it is not a common prac- tice to keep them inside houses, however exposure to their feathers is still possible as they nest on buildings. There were more patients sensitised to animals and birds in the first period than in the second period. This might be due to variation in allergen extracts because of lack of standardised allergens made by different manufacturers. Goats are raised in Omani farms and sometimes close to houses therefore it might be an important allergen that should be tested in conjunc- tion with sheep. In general, not all patients necessarily need to be tested unless there is a history of exposure or ownership of a certain animal or bird. Oman is a warm country with a dry weather, ex- cept in the coastal area where it may be humid in the summer. Houses are usually exposed to sun all year around and well ventilated, and usually there are no basements. Moulds grow in humid places and are well known to cause allergies; their environmental control might be more amenable than other allergens and im- munotherapy is readily available, hence all patients should be tested. In both study periods, they did not contribute significantly in patients tested; however, it might be useful to use mixtures of moulds rather than individual ones to minimise skin pricks and, if immu- notherapy is contemplated, individual moulds could then be tested. C O N C L U S I O N The pattern of sensitisation to environmental allergens in Oman seems to be more or less similar to other re- ports published from Arabian Peninsula. Methods to identify and characterise unique allergens through a pollen survey may still be necessary. This will help in the management of patients with asthma and rhino- conjuctivitis who are sensitised to environmental al- lergens and may benefit from environmental control measures and immunotherapy. A C K N OW L E D G ME N TS This study was approved by the Institutional Review Board (Scientific & Ethics Committee) of College of Medicine at Sultan Qaboos University R E F E R E N C E S 1. Arshad SH, Karmaus W, Matthews S, Mealy B, Dean T, Frischer T, et al. SPACE study group (Study of Preven- tion of Allergy in Children of Europe). Association of allergy-related symptoms with sensitisation to common allergens in an adult European population. J Investig Al- lergol Clin Immunol 2001; 11:94-102. 2. Arshad SH, Tariq SM, Matthews S, Hakim E. Sensitiza- tion to common allergens and its association with al- lergic disorders at age 4 years: a whole population birth cohort study. Pediatrics 2001; 108:E33. 3. Al-Riyami BM, Al-Rawas OA, Al-Riyami AA, Jasim LG, Mohammed AJ. A relatively high prevalence and se- verity of asthma, allergic rhinitis and atopic eczema in schoolchildren in the Sultanate of Oman. Respirol 2003; 8:69-76. 4. Johnson JR, Wiley RE, Fattouh R, Swirski FK, Gajewska BU, Coyle AJ, et al. Continuous exposure to house dust mite elicits chronic airway inflammation and structural remodeling. Am J Respir Crit Care Med 2004; 169:378- 385. Epub Nov 2003. 5. Arshad SH, Hamilton RG, Adkinson NF Jr. Repeated aerosol exposure to small doses of allergen. A model for chronic allergic asthma. Am J Respir Crit Care Med 1998; 157:1900-1906. 6. Hellings PW, Fokkens WJ. Allergic rhinitis and its im- pact on otorhinolaryngology. Allergy 2006; 61:656-664. 7. Frew AJ, Powell RJ, Corrigan CJ, Durham SR. Efficacy S A L E M H A L -TA M E M I , A Z Z A N A L -S H I D H A N I , R A S H I D K A L - A B R I , B A L A J I J O T H I , O M A R A A L - R AWA S A N D B A Z D AW I M A L - R I YA M I 324 and safety of specific immunotherapy with SQ allergen extract in treatment-resistant seasonal allergic rhinoc- onjunctivitis. Allergy Clinic Immunol, 2006; 117:319- 325. 8. Varney VA, Tabbah K, Mavroleon G, Frew AJ. Useful- ness of specific immunotherapy in patients with severe perennial allergic rhinitis induced by house dust mite: a double-blind, randomized, placebo-controlled trial. Clin Exp Allergy 2003; 33:1076-1082. 9. Sale R, Silvestri M, Battistini E, Defilippi AC, Sabatini F, Pecora S, et al. Nasal inflammation and bronchial reac- tivity to methacholine in atopic children with respira- tory symptoms. Allergy 2003; 58:1171-1175. 10. Al-Dowaisan A, Fakim N, Khan MR, Arifhodzic N, Panicker R, Hanoon A, et al. Salsola pollen as a pre- dominant cause of respiratory allergies in Kuwait. Ann Allergy Asthma Immunol 2004; 92:262-267. 11. Behbehani N, Arifhodzic N, Al-Mousawi M, Marafie S, Ashkanani L, Moussa M, et al. The seasonal varia- tion in allergic rhinitis and its correlation with outdoor allergens in Kuwait. Int Arch Allergy Immunol 2004; 133:164-167. Epub Feb 2004. 12. Al Mousawi M, Behbehani N, Arifhodzic N, Lovel H, Woodcock A, Custovic A. Environmental allergens in Kuwait. Allergy 2001; 56:1237-1238. 13. Ezeamuzie CI, Thomson MS, Al-Ali S, Dowaisan A, Khan M, Hijazi Z. Asthma in the desert: spectrum of the sensitising aeroallergens. Allergy 2000; 55:157-162. 14. Kwaasi AA, Parhar RS, Harfi H, Tipirneni P, Al-Sedairy ST. Major allergens of date palm (Phoenix dactylifera L.) pollen. Identification of IgE-binding components by ELISA and immunoblot analysis. Allergy 1993; 48:511- 518. 15. Al-Nahdi M, Al-Quorain AA. Sex distribution and com- mon allergens of bronchial asthma in a Saudi Arabian (eastern province) population. Allergol Immunopathol (Madr) 1987; 15:389-391. 16. Al-Amri M, Al-Rawas OA, Al-Riyami BMS, Richens ER. Atopy in Omani patients with asthma. SQUJ Sci Res Med Sci 2002; 4:15-23. 17. Skin tests used in type I allergy testing position paper. EAACI. Sub-committee on skin tests of the European Academy of Allergology and Clinical Immunology. Al- lergy 1989; 44:1– 59. 18. Dibek, ME, Reha, CM. Skin prick test results of child patients diagnosed with bronchial asthma. Allergol Im- munopathol (Madr) 2007; 35:21-24.