Atopic Dermatitis and the Risk of Infection in End-Stage Renal Disease
Abstract
:1. Introduction
2. Materials and Methods
2.1. Population
2.2. Database
2.3. Outcome Variables
2.4. Main Independent Variable—Atopic Dermatitis Diagnosis
2.5. Demographic and Other Clinical Risk Factors
2.6. Statistical Analysis
3. Results
3.1. Descriptive Statistics
3.2. Risk Factors Associated with Atopic Dermatitis
3.3. Associations with Infectious Outcomes of Interest
4. Discussion
4.1. Associations with Infectious Outcomes of Interest
4.2. Demographic and Other Clinical Risk Factors
4.3. Treatments
4.4. Strengths and Limitations
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Disclaimer
References
- Mohn, C.H.; Blix, H.S.; Halvorsen, J.A.; Nafstad, P.; Valberg, M.; Lagerløv, P. Incidence Trends of Atopic Dermatitis in Infancy and Early Childhood in a Nationwide Prescription Registry Study in Norway. JAMA Netw. Open 2018, 1, e184145. [Google Scholar] [CrossRef]
- Chiesa Fuxench, Z.C.; Block, J.K.; Boguniewicz, M.; Boyle, J.; Fonacier, L.; Gelfand, J.M.; Grayson, M.H.; Margolis, D.J.; Mitchell, L.; Silverberg, J.I.; et al. Atopic Dermatitis in America Study: A Cross-Sectional Study Examining the Prevalence and Disease Burden of Atopic Dermatitis in the US Adult Population. J. Investig. Dermatol. 2019, 139, 583–590. [Google Scholar] [CrossRef] [PubMed]
- Bylund, S.; Kobyletzki, L.B.; Svalstedt, M.; Svensson, Å. Prevalence and Incidence of Atopic Dermatitis: A Systematic Review. Acta Derm. Venereol. 2020, 100, adv00160. [Google Scholar] [CrossRef] [PubMed]
- Arkwright, P.D.; Koplin, J.J. Impact of a Decade of Research Into Atopic Dermatitis. J. Allergy Clin. Immunol. Pract. 2023, 11, 63–71. [Google Scholar] [CrossRef] [PubMed]
- Leung, D.Y.M.; Boguniewicz, M.; Howell, M.D.; Nomura, I.; Hamid, Q.A. New Insights into Atopic Dermatitis. J. Clin. Investig. 2004, 113, 651–657. [Google Scholar] [CrossRef]
- Silverberg, J.I.; Vakharia, P.P.; Chopra, R.; Sacotte, R.; Patel, N.; Immaneni, S.; White, T.; Kantor, R.; Hsu, D.Y. Phenotypical Differences of Child- and Adult-Onset Atopic Dermatitis. J. Allergy Clin. Immunol. Pract. 2018, 6, 1306–1312. [Google Scholar] [CrossRef] [PubMed]
- Abuabara, K.; Margolis, D.J. Do Children Really Outgrow Their Eczema, or Is There More than One Eczema? J. Allergy Clin. Immunol. 2013, 132, 1139–1140. [Google Scholar] [CrossRef]
- Furue, M.; Kadono, T. “Inflammatory Skin March” in Atopic Dermatitis and Psoriasis. Inflamm. Res. 2017, 66, 833–842. [Google Scholar] [CrossRef]
- Lugović-Mihić, L.; Meštrović-Štefekov, J.; Potočnjak, I.; Cindrić, T.; Ilić, I.; Lovrić, I.; Skalicki, L.; Bešlić, I.; Pondeljak, N. Atopic Dermatitis: Disease Features, Therapeutic Options, and a Multidisciplinary Approach. Life 2023, 13, 1419. [Google Scholar] [CrossRef]
- Guttman-Yassky, E.; Waldman, A.; Ahluwalia, J.; Ong, P.; Eichenfield, L. Atopic Dermatitis: Pathogenesis. Semin. Cutan. Med. Surg. 2017, 36, 100–103. [Google Scholar] [CrossRef]
- Horiuchi, Y. Th1 Regulatory Events by Infectious Pathogens, Herpes Zoster and Herpes Simplex Viruses: Prospects for Therapeutic Options for Atopic Eczema. Adv. Derm. Allergol. 2022, 39, 662–667. [Google Scholar] [CrossRef]
- Wang, V.; Boguniewicz, J.; Boguniewicz, M.; Ong, P.Y. The Infectious Complications of Atopic Dermatitis. Ann. Allergy Asthma Immunol. 2021, 126, 3–12. [Google Scholar] [CrossRef] [PubMed]
- Hashmi, M.F.; Benjamin, O.; Lappin, S.L. End-Stage Renal Disease. In StatPearls; StatPearls Publishing: Treasure Island, FL, USA, 2023. [Google Scholar]
- Kato, S.; Chmielewski, M.; Honda, H.; Pecoits-Filho, R.; Matsuo, S.; Yuzawa, Y.; Tranaeus, A.; Stenvinkel, P.; Lindholm, B. Aspects of Immune Dysfunction in End-Stage Renal Disease. Clin. J. Am. Soc. Nephrol. 2008, 3, 1526–1533. [Google Scholar] [CrossRef] [PubMed]
- Santoro, D.; Benedetto, F.; Mondello, P.; Pipitò, N.; Barillà, D.; Spinelli, F.; Ricciardi, C.A.; Cernaro, V.; Buemi, M. Vascular Access for Hemodialysis: Current Perspectives. Int. J. Nephrol. Renov. Dis. 2014, 7, 281–294. [Google Scholar] [CrossRef] [PubMed]
- Lamarche, C.; Iliuta, I.-A.; Kitzler, T. Infectious Disease Risk in Dialysis Patients: A Transdisciplinary Approach. Can. J. Kidney Health Dis. 2019, 6, 2054358119839080. [Google Scholar] [CrossRef]
- Zhang, H.; Yuan, S.; Li, Y.; Li, D.; Yu, Z.; Hu, L.; Li, X.; Wang, Y.; Larsson, S.C. Atopic Dermatitis and Chronic Kidney Disease: A Bidirectional Mendelian Randomization Study. Front. Med. 2023, 10, 1180596. [Google Scholar] [CrossRef]
- Schonmann, Y.; Mansfield, K.E.; Mulick, A.; Roberts, A.; Smeeth, L.; Langan, S.M.; Nitsch, D. Inflammatory Skin Diseases and the Risk of Chronic Kidney Disease: Population-Based Case–Control and Cohort Analyses. Br. J. Dermatol. 2021, 185, 772–780. [Google Scholar] [CrossRef]
- Galperin, T.A.; Cronin, A.J.; Leslie, K.S. Cutaneous Manifestations of ESRD. Clin. J. Am. Soc. Nephrol. 2014, 9, 201. [Google Scholar] [CrossRef]
- Hay, R.J.; Johns, N.E.; Williams, H.C.; Bolliger, I.W.; Dellavalle, R.P.; Margolis, D.J.; Marks, R.; Naldi, L.; Weinstock, M.A.; Wulf, S.K.; et al. The Global Burden of Skin Disease in 2010: An Analysis of the Prevalence and Impact of Skin Conditions. J. Investig. Derm. 2014, 134, 1527–1534. [Google Scholar] [CrossRef]
- Lamb, E.J. United Kingdom Guidelines for Chronic Kidney Disease. Scand. J. Clin. Lab. Investig. Suppl. 2008, 241, 16–22. [Google Scholar] [CrossRef]
- Annual Data Report. USRDS. Available online: https://adr.usrds.org/ (accessed on 5 September 2023).
- Langan, S.M.; Abuabara, K.; Henrickson, S.E.; Hoffstad, O.; Margolis, D.J. Increased Risk of Cutaneous and Systemic Infections in Atopic Dermatitis—A Cohort Study. J. Investig. Derm. 2017, 137, 1375–1377. [Google Scholar] [CrossRef]
- Patel, D.; Jahnke, M.N. Serious Complications from Staphylococcal Aureus in Atopic Dermatitis. Pediatr. Dermatol. 2015, 32, 792–796. [Google Scholar] [CrossRef] [PubMed]
- Hoeger, P.H.; Ganschow, R.; Finger, G. Staphylococcal Septicemia in Children with Atopic Dermatitis. Pediatr. Dermatol. 2000, 17, 111–114. [Google Scholar] [CrossRef]
- Narla, S.; Silverberg, J.I. Association between Atopic Dermatitis and Serious Cutaneous, Multiorgan and Systemic Infections in US Adults. Ann. Allergy Asthma Immunol. 2018, 120, 66–72.e11. [Google Scholar] [CrossRef] [PubMed]
- Benenson, S.; Zimhony, O.; Dahan, D.; Solomon, M.; Raveh, D.; Schlesinger, Y.; Yinnon, A.M. Atopic Dermatitis—A Risk Factor for Invasive Staphylococcus Aureus Infections: Two Cases and Review. Am. J. Med. 2005, 118, 1048–1051. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, D.B.; Arduino, M.J.; Patel, P.R. Hemodialysis-Associated Infections. In Chronic Kidney Disease, Dialysis, and Transplantation; Elsevier: Amsterdam, The Netherlands, 2019; pp. 389–410.e8. [Google Scholar] [CrossRef]
- Ravn, N.H.; Ahmadzay, Z.F.; Christensen, T.A.; Larsen, H.H.P.; Loft, N.; Rævdal, P.; Heegaard, S.; Kolko, M.; Egeberg, A.; Silverberg, J.I.; et al. Bidirectional Association between Atopic Dermatitis, Conjunctivitis, and Other Ocular Surface Diseases: A Systematic Review and Meta-Analysis. J. Am. Acad. Dermatol. 2021, 85, 453–461. [Google Scholar] [CrossRef] [PubMed]
- Mullaem, G.; Rosner, M.H. Ocular Problems in the Patient with End-Stage Renal Disease. Semin. Dial. 2012, 25, 403–407. [Google Scholar] [CrossRef]
- Tokuyama, T.; Ikeda, T.; Sato, K.; Mimura, O.; Morita, A.; Tabata, T. Conjunctival and Corneal Calcification and Bone Metabolism in Hemodialysis Patients. Am. J. Kidney Dis. 2002, 39, 291–296. [Google Scholar] [CrossRef]
- Alfrey, A.C. The Role of Abnormal Phosphorus Metabolism in the Progression of Chronic Kidney Disease and Metastatic Calcification. Kidney Int. 2004, 66, S13–S17. [Google Scholar] [CrossRef]
- Blauvelt, A.; de Bruin-Weller, M.; Gooderham, M.; Cather, J.C.; Weisman, J.; Pariser, D.; Simpson, E.L.; Papp, K.A.; Hong, H.C.-H.; Rubel, D.; et al. Long-Term Management of Moderate-to-Severe Atopic Dermatitis with Dupilumab and Concomitant Topical Corticosteroids (LIBERTY AD CHRONOS): A 1-Year, Randomised, Double-Blinded, Placebo-Controlled, Phase 3 Trial. Lancet 2017, 389, 2287–2303. [Google Scholar] [CrossRef]
- Schwade, M.J.; Tien, L.; Waller, J.L.; Davis, L.S.; Baer, S.L.; Mohammed, A.; Young, L.; Kheda, M.F.; Bollag, W.B. Treatment of Psoriasis in End-Stage Renal Disease Patients Is Associated with Decreased Mortality: A Retrospective Cohort Study. Am. J. Med. Sci. 2021, 362, 24–33. [Google Scholar] [CrossRef]
- Rystedt, I.; Strannegard, I.L.; Strannegard, O. Recurrent Viral Infections in Patients with Past or Present Atopic Dermatitis. Br. J. Dermatol. 1986, 114, 575–582. [Google Scholar] [CrossRef]
- Chiu, H.-Y.; Hung, Y.-T.; Huang, S.-W.; Huang, Y.-H. Comparative Risk of Herpes Zoster in Patients with Psoriatic Disease on Systemic Treatments: A Systematic Review and Network Meta-Analysis. Ther. Adv. Chronic Dis. 2022, 13, 20406223221091188. [Google Scholar] [CrossRef]
- Chiu, H.-Y.; Hung, Y.-T.; Huang, Y.-H. Comparative Short-Term Risks of Infection and Serious Infection in Patients Receiving Biologic and Small-Molecule Therapies for Psoriasis and Psoriatic Arthritis: A Systemic Review and Network Meta-Analysis of Randomized Controlled Trials. Ther. Adv. Chronic Dis. 2023, 14, 20406223231206225. [Google Scholar] [CrossRef] [PubMed]
- Ahn, J.H.; Waller, J.L.; Baer, S.L.; Colombo, R.E.; Kheda, M.F.; Nahman, N.S., Jr.; Turrentine, J.E. Mortality Risk after Herpes Zoster Infection in End-Stage Renal Disease Patients. Clin. Kidney J. 2019, 12, 101–105. [Google Scholar] [CrossRef] [PubMed]
- Rendon, A.; Schäkel, K. Psoriasis Pathogenesis and Treatment. Int. J. Mol. Sci. 2019, 20, 1475. [Google Scholar] [CrossRef] [PubMed]
- Croce, E.A.; Levy, M.L.; Adamson, A.S.; Matsui, E.C. Reframing Racial and Ethnic Disparities in Atopic Dermatitis in Black and Latinx Populations. J. Allergy Clin. Immunol. 2021, 148, 1104–1111. [Google Scholar] [CrossRef]
- Johansson, E.K.; Bergström, A.; Kull, I.; Melén, E.; Jonsson, M.; Lundin, S.; Wahlgren, C.-F.; Ballardini, N. Prevalence and Characteristics of Atopic Dermatitis among Young Adult Females and Males—Report from the Swedish Population-Based Study BAMSE. J. Eur. Acad. Dermatol. Venereol. 2022, 36, 698–704. [Google Scholar] [CrossRef]
- Bannister, M.J.; Freeman, S. Adult-Onset Atopic Dermatitis. Australas. J. Dermatol. 2000, 41, 225–228. [Google Scholar] [CrossRef] [PubMed]
- Sinnakirouchenan, R.; Holley, J.L. Peritoneal Dialysis Versus Hemodialysis: Risks, Benefits, and Access Issues. Adv. Chronic Kidney Dis. 2011, 18, 428–432. [Google Scholar] [CrossRef]
- Miller, L.M.; Clark, E.; Dipchand, C.; Hiremath, S.; Kappel, J.; Kiaii, M.; Lok, C.; Luscombe, R.; Moist, L.; Oliver, M.; et al. Hemodialysis Tunneled Catheter-Related Infections. Can. J. Kidney Health Dis. 2016, 3, 2054358116669129. [Google Scholar] [CrossRef]
- Yi, O.; Kwon, H.-J.; Kim, H.; Ha, M.; Hong, S.-J.; Hong, Y.-C.; Leem, J.-H.; Sakong, J.; Lee, C.G.; Kim, S.-Y.; et al. Effect of Environmental Tobacco Smoke on Atopic Dermatitis among Children in Korea. Environ. Res. 2012, 113, 40–45. [Google Scholar] [CrossRef]
- Lee, C.H.; Chuang, H.Y.; Hong, C.H.; Huang, S.K.; Chang, Y.C.; Ko, Y.C.; Yu, H.S. Lifetime Exposure to Cigarette Smoking and the Development of Adult-onset Atopic Dermatitis. Br. J. Dermatol. 2011, 164, 483–489. [Google Scholar] [CrossRef]
- Abdualrasool, M.; Al-Shanfari, S.; Booalayan, H.; Boujarwa, A.; Al-Mukaimi, A.; Alkandery, O.; Akhtar, S. Exposure to Environmental Tobacco Smoke and Prevalence of Atopic Dermatitis among Adolescents in Kuwait. Dermatology 2018, 234, 186–191. [Google Scholar] [CrossRef] [PubMed]
- Gilhooley, E.; O’Grady, C.; Roche, D.; Mahon, J.M.; Hambly, R.; Kelly, A.; Dhonncha, E.N.; Moriarty, B.; Connolly, M.; Kirby, B.; et al. High Levels of Psychological Distress, Sleep Disturbance, and Alcohol Use Disorder in Adults With Atopic Dermatitis. Dermatitis 2021, 32, S33–S38. [Google Scholar] [CrossRef] [PubMed]
- Linneberg, A.; Gonzalez-Quintela, A. The Unsolved Relationship of Alcohol and Asthma. Int. Arch. Allergy Immunol. 2016, 171, 155–157. [Google Scholar] [CrossRef] [PubMed]
- Thomsen, S.F. Atopic Dermatitis: Natural History, Diagnosis, and Treatment. ISRN Allergy 2014, 2014, 354250. [Google Scholar] [CrossRef] [PubMed]
- Frazier, W.; Bhardwaj, N. Atopic Dermatitis: Diagnosis and Treatment. Am. Fam. Physician 2020, 101, 590–598. [Google Scholar]
- Drucker, A.M.; Lam, M.; Flohr, C.; Thyssen, J.P.; Kabashima, K.; Bissonnette, R.; Dlova, N.C.; Aoki, V.; Chen, M.; Yu, J.; et al. Systemic Therapy for Atopic Dermatitis in Older Adults and Adults With Comorbidities: A Scoping Review and International Eczema Council Survey. Dermatitis 2022, 33, 200–206. [Google Scholar] [CrossRef]
- Choi, E.; Cook, A.; Phuan, C.; Martin, A.; Yang, S.; Aw, D.; Chandran, N.S. Outcomes of Prolonged and Low-Dose Ciclosporin in an Asian Population. J. Dermatol. Treat. 2021, 32, 432–437. [Google Scholar] [CrossRef]
- Adam, D.N.; Gooderham, M.J.; Beecker, J.R.; Hong, C.H.; Jack, C.S.; Jain, V.; Lansang, P.; Lynde, C.W.; Papp, K.A.; Prajapati, V.H.; et al. Expert Consensus on the Systemic Treatment of Atopic Dermatitis in Special Populations. J. Eur. Acad. Dermatol. Venereol. 2023, 37, 1135–1148. [Google Scholar] [CrossRef] [PubMed]
- Foley, R.N.; Collins, A.J. The USRDS: What You Need to Know about What It Can and Can’t Tell Us about ESRD. Clin. J. Am. Soc. Nephrol. 2013, 8, 845–851. [Google Scholar] [CrossRef] [PubMed]
- Hsu, D.Y.; Dalal, P.; Sable, K.A.; Voruganti, N.; Nardone, B.; West, D.P.; Silverberg, J.I. Validation of International Classification of Disease Ninth Revision Codes for Atopic Dermatitis. Allergy 2017, 72, 1091–1095. [Google Scholar] [CrossRef] [PubMed]
- Egeberg, A.; Andersen, Y.M.F.; Gislason, G.H.; Skov, L.; Thyssen, J.P. Prevalence of Comorbidity and Associated Risk Factors in Adults with Atopic Dermatitis. Allergy 2017, 72, 783–791. [Google Scholar] [CrossRef]
Final Model | ||||||
---|---|---|---|---|---|---|
Variable | Level | Overall | Atopic Dermatitis Diagnosis | No Atopic Dermatitis Diagnosis | aRR (95% CI) | p-Value |
Age | 63.5 (14.9) | 62.6 (14.7) | 63.5 (14.9) | |||
Race | Black | 425,522 (27.9) | 643 (28.1) | 424,879 (27.9) | 1.05 (0.95–1.15) | <0.0001 |
Other | 93,724 (6.1) | 218 (9.5) | 93,506 (6.1) | 1.84 (1.56–2.12) | ||
White | 1,007,020 (66.0) | 1429 (62.4) | 1,005,591 (66.0) | |||
Sex | Female | 652,671 (42.8) | 1096 (47.9) | 651,575 (42.8) | 1.36 (1.25–1.47) | <0.0001 |
Male | 873,595 (57.2) | 1194 (52.1) | 872,401 (57.3) | |||
Ethnicity | Hispanic | 230,162 (15.1) | 335 (14.6) | 229,827 (15.1) | 1.19 (1.05–1.34) | 0.0059 |
Non-Hispanic | 1,296,104 (84.9) | 1955 (85.4) | 1,294,149 (84.9) | |||
Dialysis | HD | 1,525,477 (99.9) | 2290 (100.0) | 1,523,187 (99.9) | ||
PD | 789 (0.1) | 0 (0.0) | 789 (0.1) | |||
Access type | Catheter | 1,232,845 (80.7) | 1734 (75.7) | 1,231,111 (80.8) | 0.75 (0.68–0.83) | <0.0001 |
Graft | 49,771 (3.3) | 102 (4.5) | 49,669 (3.3) | 1.05 (0.84–1.30) | ||
AVF | 243,650 (16.0) | 454 (19.8) | 243,196 (16) | |||
Tobacco | Yes | 273,814 (17.9) | 928 (40.5) | 272,886 (17.9) | 3.24 (2.98–3.53) | <0.0001 |
No | 1,252,452 (82.1) | 1362 (59.5) | 1,251,090 (82.1) | |||
Alcohol dependence | Yes | 42,412 (2.8) | 114 (5.0) | 42,298 (2.8) | 1.28 (1.06–1.56) | 0.0111 |
No | 1,483,854 (97.2) | 2176 (95.0) | 1,481,678 (97.2) |
Infectious Outcome | Atopic Dermatitis vs. No Atopic Dermatitis aRR (95% CI) |
---|---|
Bacteremia | 0.96 (0.89–1.05) |
Septicemia | 1.02 (0.98–1.08) |
Cellulitis | 1.39 (1.31–1.47) |
Herpes zoster | 1.67 (1.44–1.94) |
Conjunctivitis | 0.97 (0.70–1.34) |
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Momin, R.I.; Baer, S.L.; Waller, J.L.; Young, L.; Tran, S.; Taskar, V.; Bollag, W.B. Atopic Dermatitis and the Risk of Infection in End-Stage Renal Disease. Medicina 2023, 59, 2145. https://doi.org/10.3390/medicina59122145
Momin RI, Baer SL, Waller JL, Young L, Tran S, Taskar V, Bollag WB. Atopic Dermatitis and the Risk of Infection in End-Stage Renal Disease. Medicina. 2023; 59(12):2145. https://doi.org/10.3390/medicina59122145
Chicago/Turabian StyleMomin, Rushan I., Stephanie L. Baer, Jennifer L. Waller, Lufei Young, Sarah Tran, Varsha Taskar, and Wendy B. Bollag. 2023. "Atopic Dermatitis and the Risk of Infection in End-Stage Renal Disease" Medicina 59, no. 12: 2145. https://doi.org/10.3390/medicina59122145
APA StyleMomin, R. I., Baer, S. L., Waller, J. L., Young, L., Tran, S., Taskar, V., & Bollag, W. B. (2023). Atopic Dermatitis and the Risk of Infection in End-Stage Renal Disease. Medicina, 59(12), 2145. https://doi.org/10.3390/medicina59122145