Proinflammatory Cytokines Associated with InvA and PagC Genes of Salmonella typhi Isolated from Patients Undergoing Cholecystectomy

Ali J.  Eidan

doi:10.33192/Smj.2022.97

Authors

Ali J. Eidan Department of Basic Science, Faculty of Nursing, University of Kufa, Al-Najaf

DOI:

https://doi.org/10.33192/Smj.2022.97

Keywords:

Typhoid, cytokine, TNF-α, IFN-γ, InvA, PagC

Abstract

Objective: Cholecystectomy is the surgical removal of the gallbladder. The gallbladder is often colonized by Salmonella during typhoid fever. The association between cytokine and virulence genes of Salmonella is not well known. The current study aims to identify the association between proinflammatory cytokines, TNF-α and IFN-γ, and two virulence genes, InvA and PagC, extracted from S. typhi isolates obtained from patients undergoing cholecystectomy.

Materials and Methods: One hundred and fifty clinical specimens, including gallbladder tissues and blood, were collected from patients undergoing cholecystectomy at AL-Sadder Medical City and AL-Furat General Hospital/Iraq from December 2019 to September 2020. A Monoplex PCR technique was used to detect InvA and PagC, and an enzyme-linked immunosorbent assay was used to measure serum levels of TNF-α and IFNγ.

Results: From a total of 66 S. typhi isolates, the prevalence of InvA and PagC was (84.8% and 69.6%) respectively. Even after adjusting for potential confounding factors, serum levels of TNF-α and INF-γ were statistically significantly higher in PagC detected in S. typhi isolates compared to PagC not detected (p-value<0.001), but there was no significant difference between InvA detected in S. typhi isolates and InvA not detected (p-value > 0.05).

Conclusion: The virulence genes of S. typhi, especially PagC, may be considered a potent inducer of proinflammatory cytokine secretion. Further studies are needed to present the patient‘s additional clinical course according to cytokine level.

References

Waitayawinyu P, Siriwannasandha B, Namwong A. Incidence and Risk Factors of Moderate to Severe Pain in 24 hours after Laparoscopic Cholecystectomy. Siriraj Med J. 2020;64(4):119-22.

Deeprasertvit A, Deeprasertvit P, Netcharussaeng N. Postoperative Pain Reduction After Additional Intraperitoneal Suction Following Laparoscopic Cholecystectomy: A Prospective Randomized Controlled Study. Siriraj Med J. 2018;70(1):1-5.

Noppakunsomboon N, Swangsri J, Sirivatanauksorn Y, Kongkaewpaisan N. Outcomes of an Early Laparoscopic Cholecystectomy in Acute Cholecystitis, Grades I and II. Siriraj Med J. 2022;74(8):495-501.

Fusheini A, Gyawu SK. Prevalence of Typhoid and Paratyphoid Fever in the Hohoe Municipality of the Volta Region, Ghana: A Five-Year Retrospective Trend Analysis. Ann Glob Health. 2020;86(1):111.

Appiah GD, Chung A, Bentsi-Enchill AD, Kim S, Crump JA, Mogasale V, et al. Typhoid Outbreaks, 1989–2018: Implications for Prevention and Control. Am J Trop Med Hyg. 2020;102(6):1296-305.

Shubbar MA, Zighair SM. Incidence of Typhoid Fever and the Validity of the Widal Test in Some Districts in Iraq. ANB Med J. 2020;16(1):12-16.

Baker S, Blohmke CJ, Maes M, Johnston PI, Darton TC. The Current Status of Enteric Fever Diagnostics and Implications for Disease Control. Clin Infect Dis. 2020;71(Suppl 2):S64-S70.

Menendez A, Arena ET, Guttman JA, Thorson L, Vallance BA, Vogl W, et al. Salmonella infection of gallbladder epithelial cells drives local inflammation and injury in a model of acute typhoid fever. J Infect Dis. 2009;200(11):1703-13.

Bourgeois JS, Wang L, Rabino AF, Everitt J, Alvarez MI, Awadia S, et al. ARHGEF26 enhances Salmonella invasion and inflammation in cells and mice. PLoS Pathog. 2021;17(7):e1009713.

Akiyama T, Khan AA, Cheng CM, Stefanova R. Molecular characterization of Salmonella enterica serovar Saintpaul isolated from imported seafood, pepper, environmental and clinical samples. Food Microbiol. 2011;28(6):1124-8.

Bhuiyan S, Sayeed A, Khanam F, Leung DT, Rahman Bhuiyan T, Sheikh A, et al. Cellular and cytokine responses to Salmonella enterica serotype Typhi proteins in patients with typhoid fever in Bangladesh. Am J Trop Med Hyg. 2014;90(6):1024-30.

Ajayi A, Smith S, Ibidunni BS, Coulibaly KJ, Funbi JT, Adeleye AI. Serotype Distribution and Virulence Profile of Salmonella enterica Serovars Isolated from Food Animals and Humans in Lagos Nigeria. Microbiology and Biotechnology Letters. 2019;47(2):310-6.

Skyberg JA, Logue CM, Nolan LK. Virulence genotyping of Salmonella spp. with multiplex PCR. Avian Dis. 2006;50(1):77-81.

Marcus SL, Brumell JH, Pfeifer CG, Finlay BB. Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect. 2000;2(2):145-56.

Kumar A, Balachandran Y, Gupta S, Khare S, Suman. Quick PCR based diagnosis of typhoid using specific genetic markers. Biotechnol Lett. 2010;32(5):707-12.

Lu J, Li L, Pan F, Zuo G, Yu D, Liu R, et al. PagC is involved in salmonella pullorum OMVs production and affects biofilm production. Vet Microbiol. 2020;247:108778.

Srisanga S, Angkititrakul S, Sringam P, Le Ho PT, Vo ATT, Chuanchuen R. Phenotypic and genotypic antimicrobial resistance and virulence genes of Salmonella enterica isolated from pet dogs and cats. J Vet Sci. 2017;18(3):273-81.

Torkan S, Bahadoranian M, Khamesipour F, Anyanwu M. Detection of virulence and antimicrobial resistance genes in Escherichia coli isolates from diarrhoiec dogs in Iran. Arch Med Vet. 2016;48:181-90.

Aburesha RA MM, Abd Al-Kareem K , Almayahi BA, Al-Jumaa ZM. Determination IL6, INF-γ Levels in Typhoid Fever Patients. Prensa Med Argent. 2020;106(3):1-6.

Febriza A, Natzir R, Hatta M, As’ad S, Budu, Kaelan C, et al. The Role of IL-6, TNF-a, and VDR in Inhibiting the Growth of Salmonella Typhi: in vivo Study. The Open Microbiology Journal. 2020;14:65-71.

Wyant TL, Tanner MK, Sztein MB. Salmonella typhi flagella are potent inducers of proinflammatory cytokine secretion by human monocytes. Infect Immun. 1999;67(7):3619-24.

Wyant TL, Tanner MK, Sztein MB. Potent immunoregulatory effects of Salmonella typhi flagella on antigenic stimulation of human peripheral blood mononuclear cells. Infect Immun. 1999;67(3):1338-46.

Thowprasert W, Orrapin S. The Predictive Factors Associated with Longer Operative Time in Single-Incision Laparoscopic Cholecystectomy. Siriraj Med J. 2021;73(10):672-9.

Warnnissorn N, Atisook K, Lohsirirwat D, Ratanarapee S, Laohaudomphan P, Netsakhon S. Isospora belli infection associated with Chronic Cholecystitis and Sclerosing Cholangitis in Immuncompetent Host : A Case Report. Siriraj Med J. 2003;55(7):419-24.

Friedland JS, Hartley JC, Hartley CG, Shattock RJ, Griffin GE. Inhibition of ex vivo proinflammatory cytokine secretion in fatal Mycobacterium tuberculosis infection. Clin Exp Immunol. 1995;100(2):233-8.

Bhutta ZA, Mansoorali N, Hussain R. Plasma cytokines in paediatric typhoidal salmonellosis: correlation with clinical course and outcome. J Infect. 1997;35(3):253-6.

Eidan AJ, Al-Harmoosh RA, Al-Amarei HM. Estimation of IL-6, INFγ, and Lipid Profile in Suicidal and Nonsuicidal Adults with Major Depressive Disorder.J Interferon Cytokine Res. 2019;39(3):181-9.

McGhee JR, Wyant TL, Tanner MK, Sztein MB. Salmonella typhi Flagella Are Potent Inducers of Proinflammatory Cytokine Secretion by Human Monocytes. Infect Immun. 1999;67(7):3619-24.

Yamamoto Y, Klein TW, Friedman H. Induction of cytokine granulocyte-macrophage colony-stimulating factor and chemokine macrophage inflammatory protein 2 mRNAs in macrophages by Legionella pneumophila or Salmonella typhimurium attachment requires different ligand-receptor systems. Infect Immun. 1996;64(8):3062-8.

Hack CE, Aarden LA, Thus LG. Role of Cytokines in Sepsis. In: Dixon FJ, editor. Advances in Immunology. 66: Academic Press; 1997.p.101-95.