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Imbalanced serum levels of resolvin E1 (RvE1) and leukotriene B4 (LTB4) in patients with allergic rhinitis

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Abstract

Timely and successful resolution of acute inflammation plays a crucial role in preventing the development of chronic airway inflammation in allergic rhinitis (AR). This study intends to assess the serum levels of pro-inflammatory leukotriene B4 (LTB4), anti-inflammatory mediators, including resolvin E1 (RvE1), RvD1, IL-10, and TGF-β, besides mRNA expression level of G-protein coupled receptor 120 (GPR120) and peroxisome proliferator-activated receptor-γ (PPAR-γ) receptors in peripheral blood leukocytes of AR patients. Thirty-seven AR patients and thirty age- and gender-matched healthy subjects were enrolled in this study. The serum levels of LTB4, RvE1, RvD1, IL-10, and TGF-β were measured using enzyme-linked immunosorbent assay (ELISA) technique, and the mRNA expression level of GPR120 and PPAR-γ was assessed by the real-time PCR method. The serum levels of RvE1 and LTB4 were significantly higher in patients with AR than in healthy subjects (P < 0.01 and P < 0.0001, respectively). However, a significantly lower ratio of RvE1 and RvD1 to LTB4 was found in patients with AR relative to healthy subjects (P < 0.05 and P < 0.0001, respectively). Likewise, the serum levels of both IL-10 and TGF-β cytokines were significantly reduced in patients with AR compared to healthy subjects (P < 0.01 and P < 0.0001, respectively). Furthermore, the mRNA expression of PPAR-γ was significantly lower in patients with AR than in healthy subjects (P < 0.05). Our findings indicate that imbalanced pro-resolving lipid mediator RvE1 and pro-inflammatory LTB4 might contribute to the defective airway inflammation-resolution and subsequent progression toward chronic inflammation in AR patients.

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Abbreviations

AR:

Allergic rhinitis

AHR:

Airway hyperresponsiveness

RvE1:

Resolvin E1

IgE:

Immunoglobulin E

LTB4:

Leukotriene B4

AA:

Arachidonic acid

PPAR-γ:

Peroxisome proliferator-activated receptor-γ

GPR120:

G-protein coupled receptor 120

SPMs:

Specialized pro-resolving lipid mediators

EPA:

Eicosapentaenoic acid

DHA:

Docosahexaenoic acid

IL-10:

Interleukin-10

TGF-β:

Transforming growth factor-β

EDTA:

Ethylenediamine tetraacetic acid

PBMCs:

Peripheral blood mononuclear cells

ELISA:

Enzyme-linked immunosorbent assay

qRT-PCR:

Quantitative real-time polymerase chain reaction

References

  1. Kakli HA, Riley TD (2016) Allergic rhinitis. Prim Care 43(3):465–475. https://doi.org/10.1016/j.pop.2016.04.009

    Article  PubMed  Google Scholar 

  2. Tran NP, Vickery J, Blaiss MS (2011) Management of rhinitis: allergic and non-allergic. Allergy Asthma Immunol Res 3(3):148–156. https://doi.org/10.4168/aair.2011.3.3.148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Serhan CN, Levy BD (2018) Resolvins in inflammation: emergence of the pro-resolving superfamily of mediators. J Clin Invest 128(7):2657–2669. https://doi.org/10.1172/jci97943

    Article  PubMed  PubMed Central  Google Scholar 

  4. Barnig C, Frossard N, Levy BD (2018) Towards targeting resolution pathways of airway inflammation in asthma. Pharmacol Ther 186:98–113. https://doi.org/10.1016/j.pharmthera.2018.01.004

    Article  CAS  PubMed  Google Scholar 

  5. Alessandri AL, Sousa LP, Lucas CD, Rossi AG, Pinho V, Teixeira MM (2013) Resolution of inflammation: mechanisms and opportunity for drug development. Pharmacol Ther 139(2):189–212. https://doi.org/10.1016/j.pharmthera.2013.04.006

    Article  CAS  PubMed  Google Scholar 

  6. Lee HN, Surh YJ (2012) Therapeutic potential of resolvins in the prevention and treatment of inflammatory disorders. Biochem Pharmacol 84(10):1340–1350. https://doi.org/10.1016/j.bcp.2012.08.004

    Article  CAS  PubMed  Google Scholar 

  7. Liu M, Yokomizo T (2015) The role of leukotrienes in allergic diseases. Allergol Int 64(1):17–26. https://doi.org/10.1016/j.alit.2014.09.001

    Article  CAS  PubMed  Google Scholar 

  8. Profita M, Montuschi P, Bonanno A, Riccobono L, Montalbano AM, Ciabattoni G, Albano GD, Liotta G, Bousquet J, Gjomarkaj M, La Grutta S (2010) Novel perspectives in the detection of oral and nasal oxidative stress and inflammation in pediatric united airway diseases. Int J Immunopathol Pharmacol 23(4):1211–1219. https://doi.org/10.1177/039463201002300425

    Article  CAS  PubMed  Google Scholar 

  9. Tanou K, Koutsokera A, Kiropoulos TS, Maniati M, Papaioannou AI, Georga K, Zarogiannis S, Gourgoulianis KI, Kostikas K (2009) Inflammatory and oxidative stress biomarkers in allergic rhinitis: the effect of smoking. Clin Exp Allergy 39(3):345–353. https://doi.org/10.1111/j.1365-2222.2008.03149.x

    Article  CAS  PubMed  Google Scholar 

  10. Csoma Z, Kharitonov SA, Balint B, Bush A, Wilson NM, Barnes PJ (2002) Increased leukotrienes in exhaled breath condensate in childhood asthma. Am J Respir Crit Care Med 166(10):1345–1349. https://doi.org/10.1164/rccm.200203-233OC

    Article  PubMed  Google Scholar 

  11. O’Driscoll BR, Cromwell O, Kay AB (1984) Sputum leukotrienes in obstructive airways diseases. Clin Exp Immunol 55(2):397–404

    PubMed  PubMed Central  Google Scholar 

  12. Sampson AP, Castling DP, Green CP, Price JF (1995) Persistent increase in plasma and urinary leukotrienes after acute asthma. Arch Dis Child 73(3):221–225. https://doi.org/10.1136/adc.73.3.221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Shindo K, Matsumoto Y, Hirai Y, Sumitomo M, Amano T, Miyakawa K, Matsumura M, Mizuno T (1990) Measurement of leukotriene B4 in arterial blood of asthmatic patients during wheezing attacks. J Intern Med 228(2):91–96. https://doi.org/10.1111/j.1365-2796.1990.tb00200.x

    Article  CAS  PubMed  Google Scholar 

  14. Wardlaw AJ, Hay H, Cromwell O, Collins JV, Kay AB (1989) Leukotrienes, LTC4 and LTB4, in bronchoalveolar lavage in bronchial asthma and other respiratory diseases. J Allergy Clin Immunol 84(1):19–26. https://doi.org/10.1016/0091-6749(89)90173-5

    Article  CAS  PubMed  Google Scholar 

  15. Wenzel SE, Trudeau JB, Kaminsky DA, Cohn J, Martin RJ, Westcott JY (1995) Effect of 5-lipoxygenase inhibition on bronchoconstriction and airway inflammation in nocturnal asthma. Am J Respir Crit Care Med 152(3):897–905. https://doi.org/10.1164/ajrccm.152.3.7663802

    Article  CAS  PubMed  Google Scholar 

  16. Cap P, Maly M, Pehal F, Pelikan Z (2009) Exhaled leukotrienes and bronchial responsiveness to methacholine in patients with seasonal allergic rhinitis. Ann Allergy Asthma Immunol 102(2):103–109. https://doi.org/10.1016/s1081-1206(10)60238-4

    Article  CAS  PubMed  Google Scholar 

  17. Lotfi R, Rezaiemanesh A, Mortazavi SH, Karaji AG, Salari F (2019) Immunoresolvents in asthma and allergic diseases: review and update. J Cell Physiol 234(6):8579–8596. https://doi.org/10.1002/jcp.27836

    Article  CAS  PubMed  Google Scholar 

  18. Fredman G, Hellmann J, Proto JD, Kuriakose G, Colas RA, Dorweiler B, Connolly ES, Solomon R, Jones DM, Heyer EJ, Spite M, Tabas I (2016) An imbalance between specialized pro-resolving lipid mediators and pro-inflammatory leukotrienes promotes instability of atherosclerotic plaques. Nat Commun 7:12859. https://doi.org/10.1038/ncomms12859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Karp CL, Flick LM, Park KW, Softic S, Greer TM, Keledjian R, Yang R, Uddin J, Guggino WB, Atabani SF, Belkaid Y, Xu Y, Whitsett JA, Accurso FJ, Wills-Karp M, Petasis NA (2004) Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway. Nat Immunol 5(4):388–392. https://doi.org/10.1038/ni1056

    Article  CAS  PubMed  Google Scholar 

  20. Levy BD, Bonnans C, Silverman ES, Palmer LJ, Marigowda G, Israel E (2005) Diminished lipoxin biosynthesis in severe asthma. Am J Respir Crit Care Med 172(7):824–830. https://doi.org/10.1164/rccm.200410-1413OC

    Article  PubMed  PubMed Central  Google Scholar 

  21. Fredman G, Oh SF, Ayilavarapu S, Hasturk H, Serhan CN, Van Dyke TE (2011) Impaired phagocytosis in localized aggressive periodontitis: rescue by Resolvin E1. PLoS ONE 6(9):e24422. https://doi.org/10.1371/journal.pone.0024422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Krishnamoorthy N, Abdulnour RE, Walker KH, Engstrom BD, Levy BD (2018) Specialized proresolving mediators in innate and adaptive immune responses in airway diseases. Physiol Rev 98(3):1335–1370. https://doi.org/10.1152/physrev.00026.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Basil MC, Levy BD (2016) Specialized pro-resolving mediators: endogenous regulators of infection and inflammation. Nat Rev Immunol 16(1):51–67. https://doi.org/10.1038/nri.2015.4

    Article  CAS  PubMed  Google Scholar 

  24. Weylandt KH, Chiu CY, Gomolka B, Waechter SF, Wiedenmann B (2012) Omega-3 fatty acids and their lipid mediators: towards an understanding of resolvin and protectin formation. Prostaglandins Other Lipid Mediat 97(3–4):73–82. https://doi.org/10.1016/j.prostaglandins.2012.01.005

    Article  CAS  PubMed  Google Scholar 

  25. Aoki H, Hisada T, Ishizuka T, Utsugi M, Kawata T, Shimizu Y, Okajima F, Dobashi K, Mori M (2008) Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem Biophys Res Commun 367(2):509–515. https://doi.org/10.1016/j.bbrc.2008.01.012

    Article  CAS  PubMed  Google Scholar 

  26. Sawada Y, Honda T, Hanakawa S, Nakamizo S, Murata T, Ueharaguchi-Tanada Y, Ono S, Amano W, Nakajima S, Egawa G, Tanizaki H, Otsuka A, Kitoh A, Dainichi T, Ogawa N, Kobayashi Y, Yokomizo T, Arita M, Nakamura M, Miyachi Y, Kabashima K (2015) Resolvin E1 inhibits dendritic cell migration in the skin and attenuates contact hypersensitivity responses. J Exp Med 212(11):1921–1930. https://doi.org/10.1084/jem.20150381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Haworth O, Cernadas M, Yang R, Serhan CN, Levy BD (2008) Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat Immunol 9(8):873–879. https://doi.org/10.1038/ni.1627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kim TH, Kim GD, Jin YH, Park YS, Park CS (2012) Omega-3 fatty acid-derived mediator, Resolvin E1, ameliorates 2,4-dinitrofluorobenzene-induced atopic dermatitis in NC/Nga mice. Int Immunopharmacol 14(4):384–391. https://doi.org/10.1016/j.intimp.2012.08.005

    Article  CAS  PubMed  Google Scholar 

  29. Norling LV, Dalli J, Flower RJ, Serhan CN, Perretti M (2012) Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: receptor-dependent actions. Arterioscler Thromb Vasc Biol 32(8):1970–1978. https://doi.org/10.1161/atvbaha.112.249508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Liao Z, Dong J, Wu W, Yang T, Wang T, Guo L, Chen L, Xu D, Wen F (2012) Resolvin D1 attenuates inflammation in lipopolysaccharide-induced acute lung injury through a process involving the PPARgamma/NF-kappaB pathway. Respir Res 13:110. https://doi.org/10.1186/1465-9921-13-110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Flesher RP, Herbert C, Kumar RK (2014) Resolvin E1 promotes resolution of inflammation in a mouse model of an acute exacerbation of allergic asthma. Clin Sci (Lond) 126(11):805–814. https://doi.org/10.1042/cs20130623

    Article  CAS  Google Scholar 

  32. Seki H, Tani Y, Arita M (2009) Omega-3 PUFA derived anti-inflammatory lipid mediator resolvin E1. Prostaglandins Other Lipid Mediat 89(3–4):126–130. https://doi.org/10.1016/j.prostaglandins.2009.03.002

    Article  CAS  PubMed  Google Scholar 

  33. Im DS (2012) Omega-3 fatty acids in anti-inflammation (pro-resolution) and GPCRs. Prog Lipid Res 51(3):232–237. https://doi.org/10.1016/j.plipres.2012.02.003

    Article  CAS  PubMed  Google Scholar 

  34. Croasdell A, Duffney PF, Kim N, Lacy SH, Sime PJ, Phipps RP (2015) PPAR gamma and the innate immune system mediate the resolution of inflammation. PPAR Res. https://doi.org/10.1155/2015/549691

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kim SR, Lee KS, Park HS, Park SJ, Min KH, Jin SM, Lee YC (2005) Involvement of IL-10 in peroxisome proliferator-activated receptor gamma-mediated anti-inflammatory response in asthma. Mol Pharmacol 68(6):1568–1575. https://doi.org/10.1124/mol.105.017160

    Article  CAS  PubMed  Google Scholar 

  36. Lee KS, Park SJ, Hwang PH, Yi HK, Song CH, Chai OH, Kim JS, Lee MK, Lee YC (2005) PPAR-gamma modulates allergic inflammation through up-regulation of PTEN. FASEB J 19(8):1033–1035. https://doi.org/10.1096/fj.04-3309fje

    Article  CAS  PubMed  Google Scholar 

  37. Wang W, Zhu Z, Zhu B, Ma Z (2011) Peroxisome proliferator-activated receptor-gamma agonist induces regulatory T cells in a murine model of allergic rhinitis. Otolaryngol Head Neck Surg 144(4):506–513. https://doi.org/10.1177/0194599810396133

    Article  PubMed  Google Scholar 

  38. Xu J, Zhu YT, Wang GZ, Han D, Wu YY, Zhang DX, Liu Y, Zhang YH, Xie XM, Li SJ, Lu JM, Liu L, Feng W, Sun XZ, Li MX (2015) The PPAR gamma agonist, rosiglitazone, attenuates airway inflammation and remodeling via heme oxygenase-1 in murine model of asthma. Acta Pharmacol Sin 36(2):171–178. https://doi.org/10.1038/aps.2014.128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Woerly G, Honda K, Loyens M, Papin JP, Auwerx J, Staels B, Capron M, Dombrowicz D (2003) Peroxisome proliferator-activated receptors alpha and gamma down-regulate allergic inflammation and eosinophil activation. J Exp Med 198(3):411–421. https://doi.org/10.1084/jem.20021384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Honda K, Marquillies P, Capron M, Dombrowicz D (2004) Peroxisome proliferator-activated receptor gamma is expressed in airways and inhibits features of airway remodeling in a mouse asthma model. J Allergy Clin Immunol 113(5):882–888. https://doi.org/10.1016/j.jaci.2004.02.036

    Article  CAS  PubMed  Google Scholar 

  41. Trifilieff A, Bench A, Hanley M, Bayley D, Campbell E, Whittaker P (2003) PPAR-alpha and -gamma but not -delta agonists inhibit airway inflammation in a murine model of asthma: in vitro evidence for an NF-kappaB-independent effect. Br J Pharmacol 139(1):163–171. https://doi.org/10.1038/sj.bjp.0705232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Benayoun L, Letuve S, Druilhe A, Boczkowski J, Dombret MC, Mechighel P, Megret J, Leseche G, Aubier M, Pretolani M (2001) Regulation of peroxisome proliferator-activated receptor gamma expression in human asthmatic airways: relationship with proliferation, apoptosis, and airway remodeling. Am J Respir Crit Care Med 164(8 Pt 1):1487–1494. https://doi.org/10.1164/ajrccm.164.8.2101070

    Article  CAS  PubMed  Google Scholar 

  43. Pawankar R, Bunnag C, Khaltaev N, Bousquet J (2012) Allergic rhinitis and its impact on asthma in Asia Pacific and the ARIA update 2008. World Allergy Organ J 5(Suppl 3):S212–S217. https://doi.org/10.1097/WOX.0b013e318201d831

    Article  PubMed  PubMed Central  Google Scholar 

  44. Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, Willett WC (2007) Dietary patterns, insulin resistance, and prevalence of the metabolic syndrome in women. Am J Clin Nutr 85(3):910–918. https://doi.org/10.1093/ajcn/85.3.910

    Article  CAS  PubMed  Google Scholar 

  45. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29(9):e45. https://doi.org/10.1093/nar/29.9.e45

    Article  CAS  PubMed  Google Scholar 

  46. Small P, Kim H (2011) Allergic rhinitis. Allergy Asthma Clin Immunol 7(Suppl 1):S3. https://doi.org/10.1186/1710-1492-7-s1-s3

    Article  PubMed  PubMed Central  Google Scholar 

  47. Licona-Limon P, Kim LK, Palm NW, Flavell RA (2013) TH2, allergy and group 2 innate lymphoid cells. Nat Immunol 14(6):536–542. https://doi.org/10.1038/ni.2617

    Article  CAS  PubMed  Google Scholar 

  48. Headland SE, Norling LV (2015) The resolution of inflammation: principles and challenges. Semin Immunol 27(3):149–160. https://doi.org/10.1016/j.smim.2015.03.014

    Article  CAS  PubMed  Google Scholar 

  49. Aoki H, Hisada T, Ishizuka T, Utsugi M, Ono A, Koga Y, Sunaga N, Nakakura T, Okajima F, Dobashi K, Mori M (2010) Protective effect of resolvin E1 on the development of asthmatic airway inflammation. Biochem Biophys Res Commun 400(1):128–133. https://doi.org/10.1016/j.bbrc.2010.08.025

    Article  CAS  PubMed  Google Scholar 

  50. Siddiquee A, Patel M, Rajalingam S, Narke D, Kurade M, Ponnoth DS (2019) Effect of omega-3 fatty acid supplementation on resolvin (RvE1)-mediated suppression of inflammation in a mouse model of asthma. Immunopharmacol Immunotoxicol 41(2):250–257. https://doi.org/10.1080/08923973.2019.1584903

    Article  CAS  PubMed  Google Scholar 

  51. Xia H, Wang J, Sun S, Wang F, Yang Y, Chen L, Sun Z, Yao S (2019) Resolvin D1 alleviates ventilator-induced lung injury in mice by activating ppargamma/nf-kappab signaling pathway. Biomed Res Int 2019:6254587. https://doi.org/10.1155/2019/6254587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Miyahara N, Takeda K, Miyahara S, Matsubara S, Koya T, Joetham A, Krishnan E, Dakhama A, Haribabu B, Gelfand EW (2005) Requirement for leukotriene B4 receptor 1 in allergen-induced airway hyperresponsiveness. Am J Respir Crit Care Med 172(2):161–167. https://doi.org/10.1164/rccm.200502-205OC

    Article  PubMed  PubMed Central  Google Scholar 

  53. Miyahara N, Takeda K, Miyahara S, Taube C, Joetham A, Koya T, Matsubara S, Dakhama A, Tager AM, Luster AD, Gelfand EW (2005) Leukotriene B4 receptor-1 is essential for allergen-mediated recruitment of CD8 + T cells and airway hyperresponsiveness. J Immunol 174(8):4979–4984. https://doi.org/10.4049/jimmunol.174.8.4979

    Article  CAS  PubMed  Google Scholar 

  54. Barden A, Mas E, Croft KD, Phillips M, Mori TA (2014) Short-term n-3 fatty acid supplementation but not aspirin increases plasma proresolving mediators of inflammation. J Lipid Res 55(11):2401–2407. https://doi.org/10.1194/jlr.M045583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Konno Y, Ueki S, Takeda M, Kobayashi Y, Tamaki M, Moritoki Y, Oyamada H, Itoga M, Kayaba H, Omokawa A, Hirokawa M (2015) Functional analysis of free fatty acid receptor GPR120 in human eosinophils: implications in metabolic homeostasis. PLoS ONE 10(3):e0120386. https://doi.org/10.1371/journal.pone.0120386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Prihandoko R, Kaur D, Wiegman CH, Alvarez-Curto E, Donovan C, Chachi L, Ulven T, Tyas MR, Euston E, Dong Z, Alharbi AGM, Kim RY, Lowe JG, Hansbro PM, Chung KF, Brightling CE, Milligan G, Tobin AB (2020) Pathophysiological regulation of lung function by the free fatty acid receptor FFA4. Sci Transl Med 12(557):eaaw9009. https://doi.org/10.1126/scitranslmed.aaw9009

    Article  CAS  PubMed  Google Scholar 

  57. Kang HJ, Cinn YG, Hwang SJ, Won Chae S, Woo JS, Lee SH, Lee HM (2006) Up-regulation of peroxisome proliferator-activated receptor gamma in perennial allergic rhinitis. Arch Otolaryngol Head Neck Surg 132(11):1196–1200. https://doi.org/10.1001/archotol.132.11.1196

    Article  PubMed  Google Scholar 

  58. Cardell LO, Hagge M, Uddman R, Adner M (2005) Downregulation of peroxisome proliferator-activated receptors (PPARs) in nasal polyposis. Respir Res 6:132. https://doi.org/10.1186/1465-9921-6-132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kobayashi M, Thomassen MJ, Rambasek T, Bonfield TL, Raychaudhuri B, Malur A, Winkler AR, Barna BP, Goldman SJ, Kavuru MS (2005) An inverse relationship between peroxisome proliferator-activated receptor gamma and allergic airway inflammation in an allergen challenge model. Ann Allergy Asthma Immunol 95(5):468–473. https://doi.org/10.1016/s1081-1206(10)61173-8

    Article  CAS  PubMed  Google Scholar 

  60. Chowdary V, Vinaykumar E, Rao J, Rao R, Babu KR, Rangamani V (2003) A study on serum IgE and eosinophils in respiratory allergy patients. Indian J Allergy Asthma Immunol 17(1):21–24

    Google Scholar 

  61. Novak N, Bieber T (2003) Allergic and nonallergic forms of atopic diseases. J Allergy Clin Immunol 112(2):252–262. https://doi.org/10.1067/mai.2003.1595

    Article  PubMed  Google Scholar 

  62. Ciprandi G, Vizzaccaro A, Cirillo I, Tosca M, Massolo A, Passalacqua G (2005) Nasal eosinophils display the best correlation with symptoms, pulmonary function and inflammation in allergic rhinitis. Int Arch Allergy Immunol 136(3):266–272. https://doi.org/10.1159/000083953

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors appreciate all participating patients and subjects. This study was performed in partial fulfillment of the requirements for the M.Sc. dissertation of Ramin Lotfi, in the school of medicine, Kermanshah University of Medical Sciences (KUMS), Kermanshah, Iran. Financial support from the KUMS is highly appreciated.

Funding

This study was supported by the Research Administration Department of Kermanshah University of Medical Sciences, Kermanshah, Iran [F.S., Grant Number: KUMS 96043].

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Authors and Affiliations

  1. Lung Diseases and Allergy Research Center, Research Institute for Health Development, Kurdistan University of Medical Sciences, Sanandaj, Iran

    Ramin Lotfi

  2. Student Research Committee, School of Medicine, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Ramin Lotfi & Akram Davoodi

  3. Department of Pediatrics, School of Medicine, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Seyed Hamidreza Mortazavi

  4. Department of Immunology, School of Medicine, Kermanshah University of Medical Sciences, PO-Box: 6714869914, Kermanshah, Iran

    Ali Gorgin Karaji, Hanieh Tarokhian, Alireza Rezaiemanesh & Farhad Salari

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Contributions

FS planned and supervised the study. RL performed experiments, calculations, and manuscript writing. AD participated in sample preparation. SHM as a specialist physician referred the patients for sampling. HT and AR critically revised the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Farhad Salari.

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Lotfi, R., Davoodi, A., Mortazavi, S.H. et al. Imbalanced serum levels of resolvin E1 (RvE1) and leukotriene B4 (LTB4) in patients with allergic rhinitis. Mol Biol Rep 47, 7745–7754 (2020). https://doi.org/10.1007/s11033-020-05849-x

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