Analysis of Hepatitis B and C Seroprevalence and Anti-Hbs Antibody Titers in Type 2 Diabetic Patients with and without Diabetic Foot Ulcers

Öz

Background: Infection with parenterally transmitted viruses, such as hepatitis B and C viruses, is tho-ught to be more common in patients with type 2 diabetes for several reasons. Diabetic foot ulcers are a serious complication of diabetes that can lead to more frequent hospital admissions, longer hospital stays and the need for more invasive procedures. Given their complicated conditions, we hypothesized that the prevalence of hepatitis B and C infections might be higher in patients with diabetic foot ul-cers. Materials and Methods: A total of 440 patients with type 2 diabetes, 220 with diabetic foot ulcers (group 1) and 220 without (group 2), who were tested for hepatitis B surface antigen (HBsAg), anti-HBs and anti-hepatitis C antibodies (anti-HCV), were retrospectively included in the study. Anti-HBs titers <10 IU/mL were defined as lack of protective immunity, titers of 10-99 IU/mL were considered protec-tive, and titers of ≥100 IU/mL were considered high immunity. Results: HBsAg seropositivity was detected in 7 patients (3.2%), both in group 1 and group 2 (p=1.0). The presence of anti-HCV seropositivity was detected in 5 patients (2.3%) in group 1 and in 3 patients (1.4%) in group 2 (p=0.724). A titer of less than 10 mIU/mL of anti-HBs antibody was found in 118 (55.4%) patients in group 1 and in 112 (52.6%) patients in group 2 (p=0.609). Conclusions: No significant differences were observed in HBsAg, anti-HCV, or relative anti-HBs seroposi-tivity between type 2 diabetic patients with and without diabetic foot ulcer. It was found that 54.0% of patients with type 2 diabetes had anti-HBs antibody titers below 10 mIU/mL.

Anahtar Kelimeler

• type 2 diabetes mellitus
• hepatitis B
• hepatitis C
• anti-HBs

Diyabetik Ayak Ülseri Olan ve Olmayan Tip 2 Diyabetli Hastalarda Hepatit B ve C’nin Seroprevalansı ile Anti-Hbs Antikor Titrelerinin Analizi

Öz

Amaç: Tip 2 diyabetli bireylerde, hepatit B ve C virüsleri gibi parenteral yolla bulaşan virüslerin neden olduğu enfeksiyonlar daha yaygın görülebilmektedir. Diyabetik ayak ülserleri, artan sayıda hastaneye yatış ihtiyacı, invaziv prosedür gereksinimi ve uzayan yatış süreleri ile ilişkili olan diyabetin kronik ve ciddi bir komplikasyonudur. Komplike durumları göz önüne alındığında, diyabetik ayak ülserli bireyler-de hepatit B ve C enfeksiyonlarının prevalansının daha yüksek olabileceğini varsayarak bu çalışmaya planladık. Materyal ve Metod: HBV yüzey antijeni (HBsAg), anti-HBs ve anti-hepatit C antikor (anti-HCV) düzeyleri bakılmış olan 220’si diyabetik ayak ülseri olan (grup 1) ve olmayan 220 kişi (grup 2) olmak üzere toplam 440 tip 2 diyabet hastası, retrospektif olarak çalışmaya dahil edildi. Anti-HBs titrelerinin <10 IU/mL olması bağışıklığın yokluğu, 10-99 IU/mL olması koruyucu bağışıklık ve ≥100 IU/mL titreler ise yüksek bağışıklığın varlığı olarak kabul edildi. Bulgular: HBsAg seropozitifliği her iki grupta benzer bir şekilde 7’şer hastada (%3.2) tespit edildi (p=1.0). Grup 1'de 5 hastada (%2.3), grup 2'de ise 3 hastada (%1.4) anti-HCV seropozitifliği saptandı (p=0.724). Grup 1'de 118 (%55.4) hastada, grup 2'de ise 112 (%52.6) hastada anti-HBs antikor titrelerinin 10 mIU/mL'nin altında seyrettiği tespit edildi (p=0.609). Sonuç: Diyabetik ayak ülseri olan ve olmayan tip 2 diyabet hastaları arasında HBsAg, anti-HCV veya göreceli anti-HBs antikor seropozitifliği açısından anlamlı bir fark saptanmadı. Hastaların önemli bir kısmında (%54.0) anti-HBs antikor titrelerinin düşük (10 mIU/mL'nin altında) olduğu tespit edildi.

Anahtar Kelimeler

• tip 2 diyabetes mellitus
• hepatit B
• hepatit C
• anti-HBs

Kaynakça

1. 1. Kanda T, Goto T, Hirotsu Y, Moriyama M, Omata M. Mole-cular Mechanisms Driving Progression of Liver Cirrhosis towards Hepatocellular Carcinoma in Chronic Hepatitis B and C Infections: A Review. Int J Mol Sci. 2019;20:1358.
2. 2. GBD 2019 Hepatitis B Collaborators. Global, regional, and national burden of hepatitis B, 1990-2019: a systematic analysis for the Global Burden of Disease Study 2019. Lan-cet Gastroenterol Hepatol. 2022;7(9):796-829.
3. 3. Cui F, Blach S, Manzengo Mingiedi C, Gonzalez MA, Sabry Alaama A, Mozalevskis A, et al. Global reporting of prog-ress towards elimination of hepatitis B and hepatitis C. Lancet Gastroenterol Hepatol. 2023;8(4):332-342.
4. 4. Tozun N, Ozdogan O, Cakaloglu Y, Idilman R, Karasu Z, Akarca U, et al. Seroprevalence of hepatitis B and C virus infections and risk factors in Turkey: a fieldwork TURHEP study. Clin Microbiol Infect. 2015;21:1020–1026.
5. 5. Tosun S, Balık İ, Tabak F, Saltoğlu N, Örmeci N, Şencan İ, et al. Evaluation of risk factors associated with HBsAg and anti- HCV seropositivity: Results of a nationwide popula-tion-based epidemiological survey study in Turkey. Medi-terr J Infect Microb Antimicrob, 2018; 7: 34.
6. 6. Kaya SY, Kaya A. Age Specific Hepatitis B Surface Antigen (Bag) and Anti-HBs Seroprevalence among Patients Admit-ted to a State Hospital. Viral Hepat J. 2020;26: 85-87.
7. 7. Ndako JA, Nwankiti OO, Olorundare JO, Ojo SKS, Okolie CE, Olatinsu O, et al. Studies on the serological markers for hepatitis B virus infection among type 2 diabetic patients. J Clin Lab Anal. 2021;35:e23464.
8. 8. Zhang X, Zhu X, Ji Y, Li H, Hou F, Xiao C, et al. Increased risk of hepatitis B virus infection amongst individuals with dia-betes mellitus. Biosci Rep. 2019;39:BSR20181715.

9. 9. Reilly ML, Schillie SF, Smith E, Poissant T, Vonderwahl CW, Gerard K, et al. Increased risk of acute hepatitis B among adults with diagnosed diabetes mellitus. J Diabetes Sci Technol. 2012;6:858-866.
10. 10. Gulcan A, Gulcan E, Toker A, Bulut I, Akcan Y. Evaluation of risk factors and seroprevalence of hepatitis B and C in dia-betic patients in Kutahya, Turkey. J Investig Med. 2008;56:858-863.
11. 11. Gisi K, Cetinkaya A, Ozkaya M, Kantarceken B, Gisi G, Ko-roglu S. Hepatitis B and C seroprevalence in patients with diabetes mellitus and its relationship with microvascular complications. Prz Gastroenterol. 2017;12(2):105-110.
12. 12. Korkmaz H, Kesli R, Onder Pamuk B, Ipekci SH, Terzi Y, Kebapcilar L. Assessment of evidence for positive associa-tion and seroprevalence of hepatitis B and C in diabetic pa-tients in a developing country. J Investig Med. 2015;63(2):251-257.
13. 13. Jadoon NA, Shahzad MA, Yaqoob R, Hussain M, Ali N. Seroprevalence of hepatitis C in type 2 diabetes: evidence for a positive association. Virol J. 2010;7:304.
14. 14. Ba-Essa EM, Mobarak EI, Al-Daghri NM. Hepatitis C virus infection among patients with diabetes mellitus in Dam-mam, Saudi Arabia. BMC Health Serv Res. 2016;16:313.
15. 15. Saeed MJ, Olsen MA, Powderly WG, Presti RM. Diabetes Mellitus is Associated With Higher Risk of Developing De-compensated Cirrhosis in Chronic Hepatitis C Patients. J Clin Gastroenterol. 2017;51:70–76.
16. 16. Huang YW, Wang TC, Lin SC, Chang HY, Chen DS, Hu JT, et al. Increased risk of cirrhosis and its decompensation in chronic hepatitis B patients with newly diagnosed diabe-tes: a nationwide cohort study. Clin Infect Dis. 2013;57:1695-1702.
17. 17. Chen L, Sun S, Gao Y, Ran X. Global mortality of diabetic foot ulcer: A systematic review and meta-analysis of ob-servational studies. Diabetes Obes Metab. 2023;25:36-45.
18. 18. Pondé RAA. Expression and detection of anti-HBs antibo-dies after hepatitis B virus infection or vaccination in the context of protective immunity. Arch Virol. 2019;164:2645-2658.
19. 19. Wong GL, Hui VW, Yip TC, Liang LY, Zhang X, Tse YK, et al. Universal HBV vaccination dramatically reduces the preva-lence of HBV infection and incidence of hepatocellular car-cinoma. Aliment Pharmacol Ther. 2022;56:869-877.
20. 20. Miglietta A, Quinten C, Lopalco PL, Duffell E. Impact of hepatitis B vaccination on acute hepatitis B epidemiology in European Union/European Economic Area countries, 2006 to 2014. Euro Surveill. 2018;23:17-00278.
21. 21. Hepatitis B vaccines: WHO position paper – July 2017. Wkly Epidemiol Rec. 2017;92:369-392.
22. 22. Conners EE, Panagiotakopoulos L, Hofmeister MG, Sprad-ling PR, Hagan LM, Harris AM, et al. Screening and Testing for Hepatitis B Virus Infection: CDC Recommendations - United States, 2023. MMWR Recomm Rep. 2023;72:1-25.
23. 23. Schillie S, Harris A, Link-Gelles R, Romero J, Ward J, Nel-son N. Recommendations of the Advisory Committee on Immunization Practices for Use of a Hepatitis B Vaccine with a Novel Adjuvant. MMWR Morb Mortal Wkly Rep. 2018;67:455-458.
24. 24. Madihi S, Syed H, Lazar F, Zyad A, Benani A. A systematic review of the current hepatitis B viral infection and hepa-tocellular carcinoma situation in Mediterranean Countries. BioMed Res Int. 2020;2020:7027169.
25. 25. Akarca US, Baykam N, Güner R, Günşar F, İdilman R, Kay-makoğlu S, et al. Eliminating Viral Hepatitis in Turkey: Ac-hievements and Challenges. Viral Hepat J. 2022;28:47-54.
26. 26. Schillie SF, Spradling PR, Murphy TV. Immune response of hepatitis B vaccine among persons with diabetes: a syste-matic review of the literature. Diabetes Care. 2012;35:2690-2697.
27. 27. Van Der Meeren O, Peterson JT, Dionne M, Beasley R, Ebeling PR, Ferguson M, et al. Prospective clinical trial of hepatitis B vaccination in adults with and without type-2 diabetes mellitus. Hum Vaccin Immunother. 2016;12:2197-2203.
28. 28. Guclu E, Ogutlu A, Karabay O. A Study on the Age-Related Changes in Hepatitis B and C Virus Serology. Eurasian J Med. 2016;48:37-41.