Abstract
Purpose of Review
The prevalence and incidence of allergic disease have been rising in Westernized countries since the twentieth century. Increasingly, evidence suggests that damage to the epithelium initiates and shapes innate and adaptive immune responses to external antigens. The objective of this review is to examine the role of detergents as a potential risk factor for developing allergic disease.
Recent Findings
Herein, we identify key sources of human detergent exposure. We summarize the evidence suggesting a possible role for detergents and related chemicals in initiating epithelial barrier dysfunction and allergic inflammation. We primarily focus on experimental models of atopic dermatitis, asthma, and eosinophilic esophagitis, which show compelling associations between allergic disease and detergent exposure. Mechanistic studies suggest that detergents disrupt epithelial barrier integrity through their effects on tight junction or adhesion molecules and promote inflammation through epithelial alarmin release.
Summary
Environmental exposures that disrupt or damage the epithelium may account for the increasing rates of allergic disease in genetically susceptible individuals. Detergents and related chemical compounds represent possible modifiable risk factors for the development or exacerbation of atopy.
Similar content being viewed by others
Abbreviations
- ALI:
-
Air-liquid interface
- ACD:
-
Allergic contact dermatitis
- CMC:
-
Critical micelle concentration
- DMSO:
-
Dimethylsulfoxide
- EoE:
-
Eosinophilic esophagitis
- FITC:
-
Fluorescein isothiocyanate
- ICD:
-
Irritant contact dermatitis
- IgE:
-
Immunoglobulin E
- OVA:
-
Ovalbumin
- PGE3:
-
Prostaglandin E3
- ROS:
-
Reactive oxygen species
- SDBS:
-
Sodium dodecyl benzene sulfonate
- SDS:
-
Sodium dodecyl sulfate
- SLS:
-
Sodium lauryl sulfate
- TEER:
-
Transepithelilal electrical resistance
- US:
-
United States
References
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
Centers for Disease Control and Prevention, National Center for Health Statistics. FastStats: Allergies. 2021 April 21, 2023]; Available from: https://www.cdc.gov/nchs/fastats/allergies.htm.
Centers for Disease Control and Prevention; Asthma, National Health Interview (NHIS) Data. 2020 April 21, 2023]; Available from: https://www.cdc.gov/asthma/nhis/2020/table2-1.htm.
Gupta RS, et al. The prevalence, severity, and distribution of childhood food allergy in the United States. Pediatrics. 2011;128(1):e9-17.
Jackson KD, Howie LD, Akinbami LJ. Trends in allergic conditions among children: United States, 1997–2011. NCHS Data Brief. 2013;121:1–8.
Attwood SE, et al. Esophageal eosinophilia with dysphagia. A distinct clinicopathologic syndrome. Dig Dis Sci. 1993;38(1):109–16.
Straumann A, et al. Idiopathic eosinophilic esophagitis: a frequently overlooked disease with typical clinical aspects and discrete endoscopic findings. Schweiz Med Wochenschr. 1994;124(33):1419–29.
Dellon ES, Hirano I. Epidemiology and Natural History of Eosinophilic Esophagitis. Gastroenterology. 2018;154(2):319–332 e3.
Attwood SE, Furuta GT. Eosinophilic esophagitis: historical perspective on an evolving disease. Gastroenterol Clin North Am. 2014;43(2):185–99.
Spechler SJ, Konda V, Souza R. Can eosinophilic esophagitis cause achalasia and other esophageal motility disorders? Am J Gastroenterol. 2018;113(11):1594–9.
Strachan DP. Hay fever, hygiene, and household size. BMJ. 1989;299(6710):1259–60.
Rook GA, et al. Mycobacteria and other environmental organisms as immunomodulators for immunoregulatory disorders. Springer Semin Immunopathol. 2004;25(3–4):237–55.
Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13(4):260–70.
Pascal M, et al. Microbiome and allergic diseases Front Immunol. 2018;9:1584.
Myles IA. Allergy as a disease of dysbiosis: is it time to shift the treatment paradigm? Front Cell Infect Microbiol. 2019;9:50.
Hellings PW, Steelant B. Epithelial barriers in allergy and asthma. J Allergy Clin Immunol. 2020;145(6):1499–509.
Akdis CA. Does the epithelial barrier hypothesis explain the increase in allergy, autoimmunity and other chronic conditions? Nat Rev Immunol. 2021;21(11):739–51.
Singer MM, Tjeerdema RS. Fate and effects of the surfactant sodium dodecyl sulfate. Rev Environ Contam Toxicol. 1993;133:95–149.
Pothoven KL, Schleimer RP. The barrier hypothesis and Oncostatin M: restoration of epithelial barrier function as a novel therapeutic strategy for the treatment of type 2 inflammatory disease. Tissue Barriers. 2017;5(3): e1341367.
Levinson, M.I., Surfactant production : present realities and future perspectives, in Handbook of detergents: part F: production (1st ed.), U. Zoller and P. Sosis, Editors. 2008, CRC Press. https://doi.org/10.1201/9781420014655.
National Archives, Code of Federal Regulations, Title 21, Chapter I, Subchapter B, Part 172, Subpart I, § 172.822, Sodium lauryl sulfate April 21, 2023]; Available from: https://www.ecfr.gov/current/title-21/chapter-I/subchapter-B/part-172/subpart-I/section-172.822.
HERA Substance Team. Human & Environmental Risk Assessment (HERA) on ingredients of European household cleaning products: Alcohol Sulphates Human Health Risk Assessment. 2002 March 17, 2022]; p. 122]. Available from: https://www.heraproject.com/files/3-HH-04-%20HERA%20AS%20HH%20web%20wd.pdf.
SkinSAFE. April 24, 2023]; Available from: https://www.skinsafeproducts.com/.
Narkar Y, et al. Evaluation of mucosal damage and recovery in the gastrointestinal tract of rats by a penetration enhancer. Pharm Res. 2008;25(1):25–38.
de Freitas Araujo Reis MY, et al. A general approach on surfactants use and properties in drug delivery systems. Curr Pharm Des. 2021;27(42):4300–4314.
Keller S, et al. Thermodynamics of lipid membrane solubilization by sodium dodecyl sulfate. Biophys J. 2006;90(12):4509–21.
le Maire M, Champeil P, Moller JV. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim Biophys Acta. 2000;1508(1–2):86–111.
Juan-Colas J, et al. The mechanism of vesicle solubilization by the detergent sodium dodecyl sulfate. Langmuir. 2020;36(39):11499–507.
Winogradoff D, John S, Aksimentiev A. Protein unfolding by SDS: the microscopic mechanisms and the properties of the SDS-protein assembly. Nanoscale. 2020;12(9):5422–34.
Otzen DE, et al. How do surfactants unfold and refold proteins? Adv Colloid Interface Sci. 2022;308: 102754.
Nilzen A, Wikstrom K. The influence of lauryl sulphate on the sensitization of guineapigs to chrome and nickle. Acta Derm Venereol. 1955;35(4–5):292–9.
Kligman AM. The identification of contact allergens by human assay. II. Factors influencing the induction and measurement of allergic contact dermatitis. J Invest Dermatol. 1966;47(5):375–92.
De Rentiis AMA, et al. Assessment of the different skin sensitization potentials of irritants and allergens as single substances and in combination using the KeratinoSens assay. Contact Dermatitis. 2021;84(5):317–25.
De Jong WH, et al. Determination of the sensitising activity of the rubber contact sensitisers TMTD, ZDMC, MBT and DEA in a modified local lymph node assay and the effect of sodium dodecyl sulfate pretreatment on local lymph node responses. Toxicology. 2002;176(1–2):123–34.
Cumberbatch M, et al. Influence of sodium lauryl sulphate on 2,4-dinitrochlorobenzene-induced lymph node activation. Toxicology. 1993;77(1–2):181–91.
Clausen SK, et al. Study of adjuvant effect of model surfactants from the groups of alkyl sulfates, alkylbenzene sulfonates, alcohol ethoxylates and soaps. Food Chem Toxicol. 2000;38(11):1065–74.
Prottey C, Ferguson TF. The effect of surfactants upon rat peritoneal mast cells in vitro. Food Cosmet Toxicol. 1976;14(5):425–30.
Alexander BR. An assessment of the comparative sensitization potential of some common isothiazolinones. Contact Dermatitis. 2002;46(4):191–6.
Castanedo-Tardana MP, Zug KA. Methylisothiazolinone. Dermatitis. 2013;24(1):2–6.
Bonnekoh H, et al. Topical inflammasome inhibition with disulfiram prevents irritant contact dermatitis. Clin Transl Allergy. 2021;11(5): e12045.
Lee SW, et al. Effects of anionic surfactants on the water permeability of a model stratum corneum lipid membrane. Langmuir. 2014;30(1):220–6.
Ananthapadmanabhan KP, et al. Cleansing without compromise: the impact of cleansers on the skin barrier and the technology of mild cleansing. Dermatol Ther. 2004;17(Suppl 1):16–25.
Chiang A, Tudela E, Maibach HI. Percutaneous absorption in diseased skin: an overview. J Appl Toxicol. 2012;32(8):537–63.
Mao G, et al. Imaging the distribution of sodium dodecyl sulfate in skin by confocal Raman and infrared microspectroscopy. Pharm Res. 2012;29(8):2189–201.
Fullerton A, Broby-Johansen U, Agner T. Sodium lauryl sulphate penetration in an in vitro model using human skin. Contact Dermatitis. 1994;30(4):222–5.
Morris SAV, et al. The effect of prolonged exposure on sodium dodecyl sulfate penetration into human skin. Toxicol In Vitro. 2021;77: 105246.
Watanabe H, et al. Activation of the IL-1beta-processing inflammasome is involved in contact hypersensitivity. J Invest Dermatol. 2007;127(8):1956–63.
Mizutani T, et al. Sodium lauryl sulfate stimulates the generation of reactive oxygen species through interactions with cell membranes. J Oleo Sci. 2016;65(12):993–1001.
Cohen C, et al. Measurement of inflammatory mediators produced by human keratinocytes in vitro: a predictive assessment of cutaneous irritation. Toxicol In Vitro. 1991;5(5–6):407–10.
Torma H, Lindberg M, Berne B. Skin barrier disruption by sodium lauryl sulfate-exposure alters the expressions of involucrin, transglutaminase 1, profilaggrin, and kallikreins during the repair phase in human skin in vivo. J Invest Dermatol. 2008;128(5):1212–9.
Agner T. Susceptibility of atopic dermatitis patients to irritant dermatitis caused by sodium lauryl sulphate. Acta Derm Venereol. 1991;71(4):296–300.
Cork MJ, et al. Epidermal barrier dysfunction in atopic dermatitis. J Invest Dermatol. 2009;129(8):1892–908.
Xian M, et al. Anionic surfactants and commercial detergents decrease tight junction barrier integrity in human keratinocytes. J Allergy Clin Immunol. 2016;138(3):890–893 e9.
Bormann JL, Maibach HI. Draize human repeat insult patch test (HRIPT): seven decades of pitfalls and progress. Regul Toxicol Pharmacol. 2021;121: 104867.
Agner T, et al. Combined effects of irritants and allergens. Synergistic effects of nickel and sodium lauryl sulfate in nickel- sensitized individuals. Contact Dermatitis. 2002;47(1):21–6.
Jacob SE, Amini S. Cocamidopropyl betaine. Dermatitis. 2008;19(3):157–60.
Fowler JF Jr. Cocamidopropyl betaine. Dermatitis. 2004;15(1):3–4.
Loxham M, Davies DE. Phenotypic and genetic aspects of epithelial barrier function in asthmatic patients. J Allergy Clin Immunol. 2017;139(6):1736–51.
Boonpiyathad T, et al. Immunologic mechanisms in asthma. Semin Immunol. 2019;46: 101333.
Heijink IH, et al. Epithelial cell dysfunction, a major driver of asthma development. Allergy. 2020;75(8):1902–17.
Cullinan P, et al. An outbreak of asthma in a modern detergent factory. Lancet. 2000;356(9245):1899–900.
Medina-Ramon M, et al. Asthma, chronic bronchitis, and exposure to irritant agents in occupational domestic cleaning: a nested case-control study. Occup Environ Med. 2005;62(9):598–606.
Zock JP, et al. The use of household cleaning sprays and adult asthma: an international longitudinal study. Am J Respir Crit Care Med. 2007;176(8):735–41.
van Rooy FG, et al. A cross-sectional study among detergent workers exposed to liquid detergent enzymes. Occup Environ Med. 2009;66(11):759–65.
Adisesh A, et al. Occupational asthma and rhinitis due to detergent enzymes in healthcare. Occup Med (Lond). 2011;61(5):364–9.
Laborde-Casterot H, et al. Occupational rhinitis and asthma due to EDTA-containing detergents or disinfectants. Am J Ind Med. 2012;55(8):677–82.
Le Moual N, et al. Domestic use of cleaning sprays and asthma activity in females. Eur Respir J. 2012;40(6):1381–9.
• Wang M, et al. Laundry detergents and detergent residue after rinsing directly disrupt tight junction barrier integrity in human bronchial epithelial cells. J Allergy Clin Immunol. 2019;143(5):1892–903. This study demonstrated laundry detergent rinse residue (concentration less than 1:20,000 dilution of laundry detergent) has cytotoxic and barrier disruptive effects on human bronchial epithelial cells.
Siegel IA, Gordon HP. Surfactant-induced alterations of permeability of rabbit oral mucosa in vitro. Exp Mol Pathol. 1986;44(2):132–7.
Herlofson BB, Barkvoll P. Sodium lauryl sulfate and recurrent aphthous ulcers. A preliminary study Acta Odontol Scand. 1994;52(5):257–9.
Stec IP. A possible relationship between desquamation and dentifrices. A clinical study. J Am Dent Hyg Assoc. 1972;46(1):42–5.
Herlofson BB, Barkvoll P. Oral mucosal desquamation caused by two toothpaste detergents in an experimental model. Eur J Oral Sci. 1996;104(1):21–6.
Perez-Lopez D, et al. Oral mucosal peeling related to dentifrices and mouthwashes: a systematic review. Med Oral Patol Oral Cir Bucal. 2019;24(4):e452–60.
Jenkins SM, Addy R. Newcombe, Triclosan and sodium lauryl sulphate mouthwashes (I). Effects on salivary bacterial counts. J Clin Periodontol. 1991;18(2):140–4.
Kabara JJ. Structure-function relationships of surfactants as antimicrobial agents. J Soc Cosmet Chem. 1978;29(11):733–41.
Howett MK, et al. A broad-spectrum microbicide with virucidal activity against sexually transmitted viruses. Antimicrob Agents Chemother. 1999;43(2):314–21.
Birkeland, JM, Steinhaus EA. selective bacteriostatic action of sodium lauryl sulfate and of “Dreft.”. Proc Soc Exp Biol Med. 1939;40(1):86–88.
Diaz De Rienzo MA, et al. Antibacterial properties of biosurfactants against selected Gram-positive and -negative bacteria. FEMS Microbiol Lett. 2016:363(2):fnv224.
Travers J, et al. IL-33 is induced in undifferentiated, non-dividing esophageal epithelial cells in eosinophilic esophagitis. Sci Rep. 2017;7(1):17563.
•• Doyle AD, et al. Detergent exposure induces epithelial barrier dysfunction and eosinophilic inflammation in the esophagus. Allergy. 2023;78(1):192–201. This study demonstrated SDS at 1:600 dilution found in toothpaste elicits barrier disruption and inflammatory signals in human esophageal epithelium. In addition, 0.5% SDS (1:6 dilution of toothpaste) in drinking water elicited eosinophilic inflammation in the mouse esophagus.
Epstein S, et al. Possible deleterious effects of using soap substitutes in dentrifices. J Am Dent Assoc. 1939;26:1461–71.
Tanzer J, et al. Laundry detergent promotes allergic skin inflammation and esophageal eosinophilia in mice. PLoS ONE. 2022;17(6): e0268651.
• Ogulur I, et al. Gut epithelial barrier damage caused by dishwasher detergents and rinse aids. J Allergy Clin Immunol. 2023;151(2):469–84. This study demonstrated dish detergent rinse aid at levels similar to those on cleaned dishes has cytotoxic and barrier disruptive effects on human gut epithelial cells.
Acknowledgements
We would like to thank Huijun Luo, PhD, Arina Putikova, and Jessica Gibson for their scientific contributions to EoE studies referenced in this article. Figure 1 created with BioRender.com.
Funding
This work was supported by the Donald R. Levin Family Foundation. M. Y. M. is a member of the Immunology Graduate Program and is supported by the Mayo Clinic Graduate School of Biomedical Sciences. B.L.W. also reports funding from NIH (K23AI158813-01). H. K. was supported by funding from NIH (R37AI71106, R01AI128729).
Author information
Authors and Affiliations
Contributions
B. L. W. and A. D. D. co-wrote the first draft of the manuscript. All authors have reviewed and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
Mayo Clinic and Dr. Yiannias have a financial relationship with SkinSAFE.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wright, B.L., Masuda, M.Y., Ortiz, D.R. et al. Allergies Come Clean: The Role of Detergents in Epithelial Barrier Dysfunction. Curr Allergy Asthma Rep 23, 443–451 (2023). https://doi.org/10.1007/s11882-023-01094-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11882-023-01094-x