Molecular detection of <i>Salmonella typhi</i> from gallbladder tissue of cholecystitis patients and its relation to gallstone formation

Bashar A. Abdul Hassan; Jabbar S. Hassan; Ali Nayyef Umayra; Thanaa R. Abdulrahman; Bashar A. Abdul Hassan; Jabbar S. Hassan; Ali Nayyef Umayra; Thanaa R. Abdulrahman

doi:10.3934/medsci.2024026

AIMS Medical Science

2024, Volume 11, Issue 4: 378-387. doi: 10.3934/medsci.2024026

Previous Article Next Article

Research article

Molecular detection of Salmonella typhi from gallbladder tissue of cholecystitis patients and its relation to gallstone formation

Running title: Salmonella typhi and its relation to gallstone formation

1.
Department of Surgery, College of Medicine, Al-Nahrain University, Baghdad, Iraq
2.
Department of Microbiology, College of Medicine, Al-Nahrain University, Baghdad, Iraq
3.
Department of Environmental Health, College of Environmental Sciences, Al-Qasim Green University, Babylon, Iraq

Received: 25 June 2024 Revised: 13 September 2024 Accepted: 23 September 2024 Published: 30 September 2024

The gallbladder is often colonized by Salmonella during typhoid fever, and cholelithiasis contributes to many factors one of them is cholecystitis, which results from bacterial infections. This study aims to detect Salmonella typhi in the tissue of the gallbladder and find out its role in cholelithiasis. A total of 55 patients undergoing clinical and ultrasound examination were enrolled in this study, 43 with cholelithiasis and 12 without cholelithiasis, in which the gallbladder was taken as part of the surgical treatment for morbid obesity. DNA from tissue was extracted using QIAamp DNA Mini kit (Qiagen GmbH, Hilden, Germany) according to the manufacturer's recommendations; primer sets were used in this study that targeted fliC and SopB genes. A considerable number of cholelithiasis patients, 35 (81%), presented with multiple stone formation, while 8 (18.6%) presented with single stone formation. As many as 43 (78.1%) of cases presented with chronic cholecystitis, while only 12 (21.8%) of cases presented with acute cholecystitis by sonographic gallbladder; out of 55 samples, 10 (18.1%) were positive for the fliC gene in amplification of 367 bp. All 10 positive samples for Salmonella typhi showed gallbladder stone formation. However, out of 10 positive tissue samples for Salmonella typhi 10 (100%), of them were positive for the SopB gene. The findings in this study add to the body of knowledge around the occurrence rate of Salmonella typhi in gallbladder tissue samples obtained from patients with cholecystitis.
- Salmonella,
- cholelithiasis,
- cholecystitis,
- fliC gene,
- SopB gene
Citation: Bashar A. Abdul Hassan, Jabbar S. Hassan, Ali Nayyef Umayra, Thanaa R. Abdulrahman. Molecular detection of Salmonella typhi from gallbladder tissue of cholecystitis patients and its relation to gallstone formation[J]. AIMS Medical Science, 2024, 11(4): 378-387. doi: 10.3934/medsci.2024026

Related Papers:

Abstract

The gallbladder is often colonized by Salmonella during typhoid fever, and cholelithiasis contributes to many factors one of them is cholecystitis, which results from bacterial infections. This study aims to detect Salmonella typhi in the tissue of the gallbladder and find out its role in cholelithiasis. A total of 55 patients undergoing clinical and ultrasound examination were enrolled in this study, 43 with cholelithiasis and 12 without cholelithiasis, in which the gallbladder was taken as part of the surgical treatment for morbid obesity. DNA from tissue was extracted using QIAamp DNA Mini kit (Qiagen GmbH, Hilden, Germany) according to the manufacturer's recommendations; primer sets were used in this study that targeted fliC and SopB genes. A considerable number of cholelithiasis patients, 35 (81%), presented with multiple stone formation, while 8 (18.6%) presented with single stone formation. As many as 43 (78.1%) of cases presented with chronic cholecystitis, while only 12 (21.8%) of cases presented with acute cholecystitis by sonographic gallbladder; out of 55 samples, 10 (18.1%) were positive for the fliC gene in amplification of 367 bp. All 10 positive samples for Salmonella typhi showed gallbladder stone formation. However, out of 10 positive tissue samples for Salmonella typhi 10 (100%), of them were positive for the SopB gene. The findings in this study add to the body of knowledge around the occurrence rate of Salmonella typhi in gallbladder tissue samples obtained from patients with cholecystitis.

Acknowledgments

The authors highly appreciate all patients enrolled in this study and the efforts of all staff in Al-Imammian Al-Kadhimein Medical City during sample collection.

Ethics approval of research and informed consent

The current study was approved by the Institutional Review Board (I.R.B.) in Al-Nahrain University College of Medicine” (in: Jan.-10th-2023/No.96), and we confirm that we have obtained the patients' informed consent and Ethical approval prior to study.

Data availability

Further data is available from the corresponding author on reasonable request.

Conflict of interest

The authors declare no conflict of interest.

References

[1]	Nagaraja V, Eslick GD (2014) Systematic review with meta-analysis: the relationship between chronic Salmonella typhi carrier status and gall-bladder cancer. Aliment Pharmacol Ther 39: 745-750. https://doi.org/10.1111/apt.12655
[2]	Gunn JS, Marshall JM, Baker S, et al. (2014) Salmonella chronic carriage: epidemiology, diagnosis, and gallbladder persistence. Trends Microbiol 22: 648-655. https://doi.org/10.1016/j.tim.2014.06.007
[3]	Baker S, Blohmke CJ, Maes M, et al. (2020) The current status of enteric fever diagnostics and implications for disease control. Clin Infect Dis 71: S64-S70. https://doi.org/10.1093/cid/ciaa503
[4]	Gonzalez-Escobedo G, Gunn JS (2013) Gallbladder epithelium as a niche for chronic Salmonella carriage. Infect Immun 81: 2920-2930. https://doi.org/10.1128/IAI.00258-13
[5]	Neiger MR, González JF, Gonzalez-Escobedo G, et al. (2019) Pathoadaptive alteration of Salmonella biofilm formation in response to the gallbladder environment. J Bacteriol 201. https://doi.org/10.1128/JB.00774-18
[6]	González JF, Tucker L, Fitch J, et al. (2019) Human bile-mediated regulation of Salmonella curli fimbriae. J Bacteriol 201. https://doi.org/10.1128/JB.00055-19
[7]	Kurtz JR, Nieves W, Bauer DL, et al. (2020) Salmonella persistence and host immunity are dictated by the anatomical microenvironment. Infect Immun 88. https://doi.org/10.1128/IAI.00026-20
[8]	Sandala JL, Eichar BW, Kuo LG, et al. (2020) A dual-therapy approach for the treatment of biofilm-mediated Salmonella gallbladder carriage. PLoS Pathog 16: e1009192. https://doi.org/10.1371/journal.ppat.1009192
[9]	Sohi MJ, Bidhendi SM, Khaki P (2023) Assessment of Stn, SipB and SopB virulence genes in various Salmonella serovars. Arch Razi Inst 78: 1615-1623. https://doi.org/10.22092/ARI.2023.78.5.1615
[10]	Levy H, Diallo S, Tennant SM, et al. (2008) PCR method to identify Salmonella enterica serovars Typhi, Paratyphi A, and Paratyphi B among Salmonella isolates from the blood of patients with clinical enteric fever. J Clin Microbiol 46: 1861-1866. https://doi.org/10.1128/JCM.00109-08
[11]	Shekarchi B, Rafsanjani SZH, Fomani NSR, et al. (2018) Emergency department bedside ultrasonography for diagnosis of acute cholecystitis; a diagnostic accuracy study. Emerg 6: e11.
[12]	Wertz JR, Lopez JM, Olson D (2018) Comparing the diagnostic accuracy of ultrasound and CT in evaluating acute cholecystitis. AJR Am J Roentgenol 211: W92-W97. https://doi.org/10.2214/AJR.17.18884
[13]	Monstein HJ, Jonsson Y, Zdolsek J, et al. (2002) Identification of Helicobacter pylori DNA in human cholesterol gallstones. Scand J Gastroenterol 37: 112-119. https://doi.org/10.1080/003655202753387455
[14]	Haque A, Haque A, Sarwar Y, et al. (2005) Identification of drug resistance genes in clinical isolates of Salmonella typhi for development of diagnostic multiplex PCR. Pak J Med Sci 21: 402-407.
[15]	Soto SM, Rodríguez I, Rodicio MR (2006) Detection of virulence determinants in clinical strains of Salmonella enterica serovar Enteritidis and mapping on macro restriction profiles. J Med Microbiol 55: 365-373. https://doi.org/10.1099/jmm.0.46257-0
[16]	Higginson EE, Nkeze J, Permala-Booth J, et al. (2022) Detection of Salmonella typhi in bile by quantitative real-time PCR. Microbiol Spectr 10: 1-11. https://doi.org/10.1128/spectrum.00249-22
[17]	Crawford RW, Rosales-Reyes R, Ramirez-Aguilar ML, et al. (2010) Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proc Natl Acad Sci 107: 4353-4358. https://doi.org/10.1073/pnas.1000862107
[18]	Dua A, Dua A, Desai SS, et al. (2013) Gender based differences in management and outcomes of cholecystitis. Am J Surg 206: 641-646. https://doi.org/10.1016/j.amjsurg.2013.07.011
[19]	Bailey KS, Marsh W, Daughtery L, et al. (2022) Sex disparities in the presentation of gallbladder disease. Am Surg 88: 201-204. https://doi.org/10.1177/0003134821989044
[20]	Ćwik G, Skoczylas T, Wyroślak-Najs J, et al. (2013) The value of percutaneous ultrasound in predicting conversion from laparoscopic to open cholecystectomy due to acute cholecystitis. Surg Endosc 27: 2561-2568. https://doi.org/10.1007/s00464-013-2787-9
[21]	Khan I, Yadav P, Saran RK, et al. (2023) A study of the degree of gall bladder wall thickness and its impact on patients undergoing laparoscopic cholecystectomy. Cureus 15: e38990. https://doi.org/10.7759/cureus.38990
[22]	Al-Zuharri OAR (2011) Isolation and identification of bacteria from patients with cholecystits and cholelithiasis undergoing cholecystectomy. Al-Kufa J Biol 3.
[23]	Sattar I, Aziz A, Rasul S, et al. (2007) Frequency of infection in cholelithiasis. J Coll Physicians Surg Pak 17: 48-50.
[24]	Singh VK, Jaswal BS, Sharma J, et al. (2020) Analysis of stones formed in the human gall bladder and kidney using advanced spectroscopic techniques. Biophys Rev 12: 647-668. https://doi.org/10.1007/s12551-020-00697-2
[25]	Nesland JM (2004) Chronic cholecystitis. Ultrastruct Pathol 28: 121. https://doi.org/10.1080/01913120490489441
[26]	Wilkins T, Agabin E, Varghese J, et al. (2017) Gallbladder dysfunction: cholecystitis, choledocholithiasis, cholangitis, and biliary dyskinesia. Prim Care 44: 575-597. https://doi.org/10.1016/j.pop.2017.07.002
[27]	Janssen ERI, Hendriks T, Natroshvili T, et al. (2020) Retrospective analysis of non-surgical treatment of acute cholecystitis. Surg Infect 21: 428-432. https://doi.org/10.1089/sur.2019.261
[28]	Sadeq Noomi B, Ayad Majeed K (2018) Investigation of carrier persons of Salmonella typhi in cholelithias is patients in Kirkuk province. KUJSS 13: 40-48.
[29]	Mansour MA, Zaher T, Ibrahim A, et al. (2012) Role of gallstone in typhoid carriage in Egyptian patients. J Microbiol Infect Dis 2: 142-149. https://doi.org/10.5799/jmid.123127
[30]	Uddin MN, Mukhtiar A, Khan M, et al. (2022) Antibiogram analysis of Salmonella paratyphi A isolated from gall bladder patients in district Peshawar, Pakistan. BioScientific Rev 4: 57-72. https://doi.org/10.32350/BSR.44.03
[31]	Medhat AR, Aljanaby AAJ (2022) Epidemiology of typhoid fever in Balad city, Iraq. Int J Health Sci 6: 1049-1063. https://doi.org/10.53730/ijhs.v6nS1.4834
[32]	Irfan B, Yasin I, Kirschner D (2024) Extensive drug-resistant typhoid fever prevention and management in Pakistan: a challenge to public health. Univ Michigan Undergrad Res J 17. https://doi.org/10.3998/umurj.5505
[33]	Khaltabadi RF, Shahrokhi N, Ebrahimi-Rad M, et al. (2019) Salmonella typhimurium in Iran: contribution of molecular and IS 200 PCR methods in variants detection. PLoS One 14: e0213726. https://doi.org/10.1371/journal.pone.0213726
[34]	Khaled A, Moselhy WA, Ibrahim MA, et al. (2019) Current trend on the economic and public health significance of salmonellosis in Iraq. Adv Anim Vet Sci 7: 492-497.
[35]	Raffatellu M, Wilson RP, Chessa D, et al. (2005) SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun 73: 146-154. https://doi.org/10.1128/iai.73.1.146-154.2005
[36]	Boyle EC, Brown NF, Finlay BB (2006) Salmonella enterica serovar typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function. Cell Microbiol 8: 1946-1957. https://doi.org/10.1111/j.1462-5822.2006.00762.x
[37]	Darkahi B, Sandblom G, Liljeholm H, et al. (2014) Biliary microflora in patients undergoing cholecystectomy. Surg Infect 15: 262-265. https://doi.org/10.1089/sur.2012.125
[38]	Hirata BHN, Sasagawa S, Navarini A, et al. (2023) Comparison of bacterial profile of gallbladder with gallstones from patients undergoing cholecystectomy due to complicated and uncomplicated cholelithiasis: changes in the epidemiological scenario. Rev Col Bras Cir 50: e20233474. https://doi.org/10.1590/0100-6991e-20233474-en
[39]	Grigor'eva IN, Romanova TI (2020) Gallstone disease and microbiome. Microorganisms 8: 835. https://doi.org/10.3390/microorganisms8060835

Reader Comments

Your name:*

Email:*
© 2024 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)