Histamine: Bridging Food and Atopic Dermatitis

Main Article Content

Arya Bharti Santosh K. Mishra

Abstract

Atopic dermatitis is a most common chronic inflammatory skin diseases, and it is often characterized by itch, inflammation, and disruption of skin barriers. Itch associated with atopic dermatitis severely impacts the quality of life of individuals, families, and caregivers, and the incidence of itch is increasing. Here, we focused on the interplay between histamine, food, and itch mechanisms in atopic dermatitis. Histamine, a biogenic amine, plays a significant role in the pathogenesis of atopic dermatitis and related itch, and histamine levels are found elevated in atopic dermatitis individuals. A histamine-rich diet, such as ingesting foods rich in histamine and foods that trigger the cellular release of histamine, exacerbates atopic dermatitis symptoms, and the elimination of a histamine-rich diet attenuates the pathology. Further, we discussed the role of histamine receptors, specifically H1 and H4, in itch and inflammation associated with atopic dermatitis. Drugs such as antihistamines are effective in some cases, but fail to alleviate itch in atopic dermatitis, suggesting non-histaminergic itch pathways. In addition, we discussed enzymes such as diamine oxidase and histamine N-Methyltransferase, which are involved in the metabolism of histamine and, by inhibiting the activity of these enzymes leading to the accumulation of histamine, which, in turn, is responsible for atopic dermatitis and associated itch. This review provides intricate interactions between itch, diet, and histamine in atopic dermatitis and provide essential mechanistic insights and further in the development of future therapeutics.

Keywords: Atopic dermatitis, Itch, Food, Histamine, G Protein-coupled receptors, histamine receptors, Diamine oxidase

Article Details

How to Cite
BHARTI, Arya; MISHRA, Santosh K.. Histamine: Bridging Food and Atopic Dermatitis. Medical Research Archives, [S.l.], v. 12, n. 11, dec. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/6144>. Date accessed: 12 dec. 2024. doi: https://doi.org/10.18103/mra.v12i11.6144.
Section
Research Articles

References

1. Avena-Woods C. Overview of atopic dermatitis. Am J Manag Care. Jun 2017;23(8 Suppl): S115-S123.

2. Odhiambo JA, Williams HC, Clayton TO, Robertson CF, Asher MI, Group IPTS. Global variations in prevalence of eczema symptoms in children from ISAAC Phase Three. J Allergy Clin Immunol. Dec 2009;124(6):1251-8 e23.
doi:10.1016/j.jaci.2009.10.009

3. Eckert L, Gupta S, Amand C, Gadkari A, Mahajan P, Gelfand JM. The burden of atopic dermatitis in US adults: Health care resource utilization data from the 2013 National Health and Wellness Survey. J Am Acad Dermatol. Jan 2018; 78(1):54-61 e1. doi:10.1016/j.jaad.2017.08.002

4. Lerner EA. Is the Nervous System More Important Than the Immune System in Itch and Atopic Dermatitis? J Investig Dermatol Symp Proc. Dec 2018;19(2):S94. doi:10.1016/j.jisp.2018.10.002

5. Chung BY, Cho SI, Ahn IS, et al. Treatment of Atopic Dermatitis with a Low-histamine Diet. Ann Dermatol. Sep 2011;23 Suppl 1:S91-5. doi:10.5021/ad.2011.23.S1.S91

6. Worm M, Fiedler EM, Dolle S, et al. Exogenous histamine aggravates eczema in a subgroup of patients with atopic dermatitis. Acta Derm Venereol. 2009;89(1):52-6. doi:10.2340/00015555-0565

7. Uenishi T, Sugiura H, Tanaka T, Uehara M. Aggravation of atopic dermatitis in breast-fed infants by tree nut-related foods and fermented foods in breast milk. J Dermatol. Feb 2011;38 (2):140-5. doi:10.1111/j.1346-8138.2010.00968.x

8. Wang Z, Zhang LJ, Guha G, et al. Selective ablation of Ctip2/Bcl11b in epidermal keratinocytes triggers atopic dermatitis-like skin inflammatory responses in adult mice. PLoS One. 2012;7(12) :e51262. doi:10.1371/journal.pone.0051262

9. Mishra SK, Hoon MA. The cells and circuitry for itch responses in mice. Science. May 24 2013; 340(6135):968-71. doi:10.1126/science.1233765

10. Bath-Hextall F, Delamere FM, Williams HC. Dietary exclusions for established atopic eczema. Cochrane Database Syst Rev. Jan 23 2008;2008(1): CD005203. doi:10.1002/14651858.CD005203.pub2

11. Amon U, Menz U, Wolff HH. Investigations on plasma levels of mast cell mediators in acute atopic dermatitis. J Dermatol Sci. Feb 1994;7(1):63-7. doi:10.1016/0923-1811(94)90023-x

12. Nemeth K, Wilson T, Rada B, et al. Characterization and function of histamine receptors in human bone marrow stromal cells. Stem Cells. Feb 2012;30(2):222-31. doi:10.1002/stem.771

13. Parsons ME, Ganellin CR. Histamine and its receptors. Br J Pharmacol. Jan 2006;147 Suppl 1:S127-35. doi:10.1038/sj.bjp.0706440

14. Xie H, He SH. Roles of histamine and its receptors in allergic and inflammatory bowel diseases. World J Gastroenterol. May 21 2005;11 (19):2851-7. doi:10.3748/wjg.v11.i19.2851

15. Wantke F, Gotz M, Jarisch R. [The histamine-free diet]. Hautarzt. Aug 1993;44(8):512-6. Die histaminfreie Diat.

16. Kajihara Y, Murakami M, Imagawa T, Otsuguro K, Ito S, Ohta T. Histamine potentiates acid-induced responses mediating transient receptor potential V1 in mouse primary sensory neurons. Neuroscience. Mar 10 2010;166(1):292-304. doi:10.1016/j.neuroscience.2009.12.001

17. Kim BM, Lee SH, Shim WS, Oh U. Histamine-induced Ca(2+) influx via the PLA(2)/lipoxygenase/ TRPV1 pathway in rat sensory neurons. Neurosci Lett. May 6 2004;361(1-3):159-62. doi:10.1016/j.neulet.2004.01.019

18. Behrendt H, Ring J. Histamine, antihistamines and atopic eczema. Clin Exp Allergy. Nov 1990;20 Suppl 4:25-30. doi:10.1111/j.1365-2222.1990.tb0 2473.x

19. Mohajeri S, Newman SA. Review of evidence for dietary influences on atopic dermatitis. Skin Therapy Lett. Jul-Aug 2014;19(4):5-7.

20. Rossbach K, Schaper K, Kloth C, et al. Histamine H4 receptor knockout mice display reduced inflammation in a chronic model of atopic dermatitis. Allergy. Feb 2016;71(2):189-97.
doi:10.1111/all.12779

21. Sampson HA, Jolie PL. Increased plasma histamine concentrations after food challenges in children with atopic dermatitis. N Engl J Med. Aug 9 1984;311(6):372-6. doi:10.1056/NEJM198408093110605

22. De Benedetto A, Yoshida T, Fridy S, Park JE, Kuo IH, Beck LA. Histamine and Skin Barrier: Are Histamine Antagonists Useful for the Prevention or Treatment of Atopic Dermatitis? J Clin Med. Apr 21 2015;4(4):741-55. doi:10.3390/jcm4040741

23. Son JH, Chung BY, Kim HO, Park CW. A Histamine-Free Diet Is Helpful for Treatment of Adult Patients with Chronic Spontaneous Urticaria. Ann Dermatol. Apr 2018;30(2):164-172. doi:10.5021/ad.2018.30.2.164

24. Guida B, De Martino CD, De Martino SD, et al. Histamine plasma levels and elimination diet in chronic idiopathic urticaria. Eur J Clin Nutr. Feb 2000;54(2):155-8. doi:10.1038/sj.ejcn.1600911

25. Matterne U, Bohmer MM, Weisshaar E, Jupiter A, Carter B, Apfelbacher CJ. Oral H1 antihistamines as 'add-on' therapy to topical treatment for eczema. Cochrane Database Syst Rev. Jan 22 2019;1(1):CD012167.
doi:10.1002/14651858.CD012167.pub2

26. Chung BY, Cho SI, Ahn IS, et al. Treatment of Atopic Dermatitis with a Low-histamine Diet. Ann Dermatol. Sep 2011;23 Suppl 1(Suppl 1):S91-5. doi:10.5021/ad.2011.23.S1.S91

27. Rosell-Camps A, Zibetti S, Perez-Esteban G, Vila-Vidal M, Ferres-Ramis L, Garcia-Teresa-Garcia E. Histamine intolerance as a cause of chronic digestive complaints in pediatric patients. Rev Esp Enferm Dig. Apr 2013;105(4):201-6. doi:10.4321/s1130-01082013000400004

28. Schwelberger HG. Histamine intolerance: a metabolic disease? Inflamm Res. Mar 2010;59 Suppl 2:S219-21. doi:10.1007/s00011-009-0134-3

29. Lucas PM, Claisse O, Lonvaud-Funel A. High frequency of histamine-producing bacteria in the enological environment and instability of the histidine decarboxylase production phenotype. Appl Environ Microbiol. Feb 2008;74(3):811-7. doi:10.1128/AEM.01496-07

30. Toro-Funes N, Bosch-Fuste J, Latorre-Moratalla ML, Veciana-Nogues MT, Vidal-Carou MC. Biologically active amines in fermented and non-fermented commercial soybean products from the Spanish market. Food Chem. Apr 15 2015;173: 1119-24. doi:10.1016/j.foodchem.2014.10.118

31. Jantschitsch C, Kinaciyan T, Manafi M, Safer M, Tanew A. Severe scombroid fish poisoning: an underrecognized dermatologic emergency. J Am Acad Dermatol. Jul 2011;65(1):246-7.
doi:10.1016/j.jaad.2009.12.058

32. Morrow JD, Margolies GR, Rowland J, Roberts LJ, 2nd. Evidence that histamine is the causative toxin of scombroid-fish poisoning. N Engl J Med. Mar 14 1991;324(11):716-20. doi:10.1056/NEJM199103143241102

33. Hoffmann KM, Gruber E, Deutschmann A, Jahnel J, Hauer AC. Histamine intolerance in children with chronic abdominal pain. Arch Dis Child. Oct 2013;98(10):832-3. doi:10.1136/archdischild-2013-305024

34. Kofler L, Ulmer H, Kofler H. Histamine 50-skin-prick test: a tool to diagnose histamine intolerance. ISRN Allergy. 2011;2011:353045. doi:10.5402/2011/353045

35. Kovacova-Hanuskova E, Buday T, Gavliakova S, Plevkova J. Histamine, histamine intoxication and intolerance. Allergol Immunopathol (Madr). Sep-Oct 2015;43(5):498-506. doi:10.1016/j.aller.2015.05.001

36. Maintz L, Novak N. Histamine and histamine intolerance. Am J Clin Nutr. May 2007;85(5):1185-96. doi:10.1093/ajcn/85.5.1185

37. Zopf Y, Baenkler HW, Silbermann A, Hahn EG, Raithel M. The differential diagnosis of food intolerance. Dtsch Arztebl Int. May 2009;106(21): 359-69; quiz 369-70; 4 p following 370. doi:10.3238/arztebl.2009.0359

38. Chin KW, Garriga MM, Metcalfe DD. The histamine content of oriental foods. Food Chem Toxicol. May 1989;27(5):283-7. doi:10.1016/0278-6915(89)90129-4

39. Tan SP, Brown SB, Griffiths CE, Weller RB, Gibbs NK. Feeding filaggrin: effects of l-histidine supplementation in atopic dermatitis. Clin Cosmet Investig Dermatol. 2017;10:403-411. doi:10.2147/CCID.S146760

40. Holecek M. Histidine in Health and Disease: Metabolism, Physiological Importance, and Use as a Supplement. Nutrients. Mar 22 2020;12(3) doi:10.3390/nu12030848

41. Manzotti G, Breda D, Di Gioacchino M, Burastero SE. Serum diamine oxidase activity in patients with histamine intolerance. Int J Immunopathol Pharmacol. Mar 2016;29(1):105-11. doi:10.1177/0394632015617170

42. Lugovic-Mihic L, Seserko A, Duvancic T, Situm M, Mihic J. [Histamine intolerance--possible dermatologic sequences]. Acta Med Croatica. Dec 2012;66(5):375-81. Intolerancija na histamin--koje su moguce posljedice na kozi?

43. Petersen J, Drasche A, Raithel M, Schwelberger HG. Analysis of genetic polymorphisms of enzymes involved in histamine metabolism. Inflamm Res. Apr 2003;52 Suppl 1:S69-70. doi:10.1007/s000110300059

44. Petersen J, Raithel M, Schwelberger HG. Histamine N-methyltransferase and diamine oxidase gene polymorphisms in patients with inflammatory and neoplastic intestinal diseases. Inflamm Res. Apr 2002;51 Suppl 1:S91-2. doi:10.1007/pl00022464

45. Petersen J, Raithel M, Schwelberger HG. Characterisation of functional polymorphisms of the human diamine oxidase gene. Inflamm Res. Apr 2005;54 Suppl 1:S58-9. doi:10.1007/s00011-004-0426-6

46. Lee HS, Kim SH, Kim KW, et al. Involvement of human histamine N-methyltransferase gene polymorphisms in susceptibility to atopic dermatitis in korean children. Allergy Asthma Immunol Res. Jan 2012;4(1):31-6. doi:10.4168/aair.2012.4.1.31

47. Oroszi G, Enoch MA, Chun J, Virkkunen M, Goldman D. Thr105Ile, a functional polymorphism of histamine N-methyltransferase, is associated with alcoholism in two independent populations. Alcohol Clin Exp Res. Mar 2005;29(3):303-9. doi:10.1097/01.alc.0000156128.28257.2e

48. Stevenson J, Sonuga-Barke E, McCann D, et al. The role of histamine degradation gene polymorphisms in moderating the effects of food additives on children's ADHD symptoms. Am J Psychiatry. Sep 2010;167(9):1108-15. doi:10.1176/appi.ajp.2010.09101529

49. McGrath AP, Hilmer KM, Collyer CA, et al. Structure and inhibition of human diamine oxidase. Biochemistry. Oct 20 2009;48(41):9810-22. doi:10.1021/bi9014192

50. Mizuguchi H, Imamura I, Takemura M, Fukui H. Purification and characterization of diamine oxidase (histaminase) from rat small intestine. J Biochem. Sep 1994;116(3):631-5.
doi:10.1093/oxfordjournals.jbchem.a124572

51. Razali NN, Hashim NH, Leow ATC, Salleh AB. Conformational Design and Characterisation of a Truncated Diamine Oxidase from Arthrobacter globiformis. High Throughput. Aug 25 2018;7(3) doi:10.3390/ht7030021

52. Kiehl R, Ionescu G. [Histamine degrading enzymes in atopic eczema]. Z Hautkr. Dec 15 1989;64(12):1121-3. Histamin-Abbauende Enzyme bei Atopischem Ekzem.

53. Maintz L, Benfadal S, Allam JP, Hagemann T, Fimmers R, Novak N. Evidence for a reduced histamine degradation capacity in a subgroup of patients with atopic eczema. J Allergy Clin Immunol. May 2006;117(5):1106-12. doi:10.1016/j.jaci.2005.11.041

54. Leitner R, Zoernpfenning E, Missbichler A. Evaluation of the inhibitory effect of various drugs / active ingredients on the activity of human diamine oxidase in vitro. Clinical and Translational Allergy. 2014;4(S3)doi:10.1186/2045-7022-4-s3-p23

55. Wagner A, Buczylko K, Zielinska-Blizniewska H, Wagner W. Impaired resolution of wheals in the skin prick test and low diamine oxidase blood level in allergic patients. Postepy Dermatol Alergol. Oct 2019;36(5):538-543. doi:10.5114/ada.2019.89504

56. Lagerstrom MC, Schioth HB. Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat Rev Drug Discov. Apr 2008;7(4):339-57. doi:10.1038/nrd2518

57. Hirasawa N, Ohsawa Y, Katoh G, et al. Modification of the picryl chloride-induced allergic dermatitis model in mouse ear lobes by 12-O-tetradecanoylphorbol 13-acetate, and analysis of the role of histamine in the modified model. Int Arch Allergy Immunol. 2009;148(4):279-88. doi:10.1159/000170381

58. Cowden JM, Riley JP, Ma JY, Thurmond RL, Dunford PJ. Histamine H4 receptor antagonism diminishes existing airway inflammation and dysfunction via modulation of Th2 cytokines. Respir Res. Jun 24 2010;11:86. doi:10.1186/1465-9921-11-86

59. Takahashi Y, Kagawa Y, Izawa K, Ono R, Akagi M, Kamei C. Effect of histamine H4 receptor antagonist on allergic rhinitis in mice. Int Immunopharmacol. Jun 2009;9(6):734-8. doi:10.1016/j.intimp.2009.02.011

60. Cowden JM, Yu F, Banie H, et al. The histamine H4 receptor mediates inflammation and Th17 responses in preclinical models of arthritis. Ann Rheum Dis. Mar 2014;73(3):600-8. doi:10.1136/annrheumdis-2013-203832

61. Jutel M, Watanabe T, Akdis M, Blaser K, Akdis CA. Immune regulation by histamine. Curr Opin Immunol. Dec 2002;14(6):735-40. doi:10.1016/s0952-7915(02)00395-3

62. Seifert R, Strasser A, Schneider EH, Neumann D, Dove S, Buschauer A. Molecular and cellular analysis of human histamine receptor subtypes. Trends Pharmacol Sci. Jan 2013;34(1):33-58. doi:10.1016/j.tips.2012.11.001

63. Ohtsu H, Seike M. Histamine and Histamine Receptors in Allergic Dermatitis. Handb Exp Pharmacol. 2017;241:333-345. doi:10.1007/164_2016_9

64. Kochling H, Schaper K, Wilzopolski J, et al. Combined treatment with H1 and H4 receptor antagonists reduces inflammation in a mouse model of atopic dermatitis. J Dermatol Sci. Aug 2017;87 (2):130-137. doi:10.1016/j.jdermsci.2017.04.004

65. Ohsawa Y, Hirasawa N. The antagonism of histamine H1 and H4 receptors ameliorates chronic allergic dermatitis via anti-pruritic and anti-inflammatory effects in NC/Nga mice. Allergy. Aug 2012;67(8):1014-22.
doi:10.1111/j.1398-9995.2012.02854.x

66. Mollanazar NK, Smith PK, Yosipovitch G. Mediators of Chronic Pruritus in Atopic Dermatitis: Getting the Itch Out? Clin Rev Allergy Immunol. Dec 2016;51(3):263-292. doi:10.1007/s12016-015-8488-5

67. Garibyan L, Rheingold CG, Lerner EA. Understanding the pathophysiology of itch. Dermatol Ther. Mar-Apr 2013;26(2):84-91. doi:10.1111/dth.12025

68. Nicolson TA, Bevan S, Richards CD. Characterisation of the calcium responses to histamine in capsaicin-sensitive and capsaicin-insensitive sensory neurones. Neuroscience. 2002;110(2):329-38.
doi:10.1016/s0306-4522(01)00561-9

69. Shim WS, Tak MH, Lee MH, et al. TRPV1 mediates histamine-induced itching via the activation of phospholipase A2 and 12-lipoxygenase. J Neurosci. Feb 28 2007;27(9):2331-7.
doi:10.1523/JNEUROSCI.4643-06.2007

70. Morita T, McClain SP, Batia LM, et al. HTR7 Mediates Serotonergic Acute and Chronic Itch. Neuron. Jul 1 2015;87(1):124-38. doi:10.1016/j.neuron.2015.05.044

71. Akiyama T, Merrill AW, Zanotto K, Carstens MI, Carstens E. Scratching behavior and Fos expression in superficial dorsal horn elicited by protease-activated receptor agonists and other itch mediators in mice. J Pharmacol Exp Ther. Jun 2009;329(3):945-51. doi:10.1124/jpet.109.152256

72. Steinhoff M, Neisius U, Ikoma A, et al. Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J Neurosci. Jul 16 2003;23(15):6176-80.

73. Weisshaar E, Ziethen B, Gollnick H. Can a serotonin type 3 (5-HT3) receptor antagonist reduce experimentally-induced itch? Inflamm Res. Oct 1997;46(10):412-6. doi:10.1007/s000110050213

74. Sun YG, Chen ZF. A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature. Aug 9 2007;448(7154):700-U10. doi:10.1038/nature06029

75. Leknes SG, Bantick S, Willis CM, Wilkinson JD, Wise RG, Tracey I. Itch and motivation to scratch: an investigation of the central and peripheral correlates of allergen- and histamine-induced itch in humans. J Neurophysiol. Jan 2007;97(1):415-22. doi:10.1152/jn.00070.2006

76. Liu Q, Tang Z, Surdenikova L, et al. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. Dec 24 2009;139(7):1353-65. doi:10.1016/j.cell.2009.11.034

77. Imamachi N, Park GH, Lee H, et al. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc Natl Acad Sci U S A. Jul 7 2009;106(27): 11330-5. doi:10.1073/pnas.0905605106

78. Han SK, Mancino V, Simon MI. Phospholipase Cbeta 3 mediates the scratching response activated by the histamine H1 receptor on C-fiber nociceptive neurons. Neuron. Nov 22 2006;52(4):691-703. doi:10.1016/j.neuron.2006.09.036

79. Cui TT, Wang GX, Wei NN, Wang K. A pivotal role for the activation of TRPV3 channel in itch sensations induced by the natural skin sensitizer carvacrol. Acta Pharmacol Sin. Mar 2018;39(3):331-335. doi:10.1038/aps.2017.152

80. Han L, Dong X. Itch mechanisms and circuits. Annu Rev Biophys. 2014;43:331-55.
doi:10.1146/annurev-biophys-051013-022826

81. Kennedy MJ, Loehle JA, Griffin AR, et al. Association of the histamine N-methyltransferase C314T (Thr105Ile) polymorphism with atopic dermatitis in Caucasian children. Pharmacotherapy. Dec 2008;28(12):1495-501.
doi:10.1592/phco.28.12.1495