Prevalence of anterior nares colonization of Palestinian diabetic patients with Staphylococcus aureus or methicillin-resistant Staphylococcus aureus
Main Article Content
Keywords
Palestine, diabetes, S. aureus, MRSA, antibiotic resistance, anterior nares colonization
Abstract
Staphylococcus aureus (S. aureus) is an opportunistic pathogen that colonizes the anterior nares of about one-third of the human population. Anterior nares colonization with S. aureus or methicillin-resistant S. aureus (MRSA) allows these pathogens to colonize the skin and other anatomical locations. Accordingly, these pathogens may cause different types of endogenous infections. To investigate the prevalence of nasal carriage of S. aureus or MRSA among Palestinian diabetic patients, nasal swabs were taken from 151 diabetic patients, about to undergo invasive surgeries. Thirty-five patients (35.1% of the total patients) were found to be colonized with S. aureus, of which 14 (9.7% of the total patients) were found to be colonized with MRSA. These proportions were higher than those described for the general population (30% and 1.3%, respectively) or even for Palestinian patients in general (25.9% and 2%, respectively). In addition, the proportion of nasal carriage of S. aureus or MRSA among Palestinian diabetic patients was found to be higher than that described for diabetic patients in other countries. Meanwhile, 30 of the 53 isolates (57% of the total isolates) were also found to be multidrug-resistant. Accordingly, the proportion of anterior nares colonization with S. aureus or MRSA in Palestinian diabetic patients was remarkably high.
References
Abu Taha, A., Abu-Zaydeh, A.H.R.A., Ardah, S.W., Al-Jabi, W.M., Sweileh, R. and Awang, S.H. 2016. Public knowledge and attitudes regarding the use of antibiotics and resistance: findings from a cross-sectional study among Palestinian adults. Zoonoses Public Health 63(6): 449–457. 10.1111/zph.12249
Adwan, K. 2014. Fast DNA isolation and PCR protocols for detection of methicillin-resistant staphylococci. Folia Microbiology (Praha) 59(1): 5–8. 10.1007/s12223-013-0259-1
Akbari, M. and Hassan-Zadeh, V. 2018. Hyperglycemia affects the expression of inflammatory genes in peripheral blood mononuclear cells of patients with type 2 diabetes. Immunological Investigations 47(7): 654–665. 10.1080/08820139.2018.1480031
Al Sabbah, H., Vereecken, C., Kolsteren, P., Abdeen, Z. and Maes, L. 2007. Food habits and physical activity patterns among Palestinian adolescents: findings from the national study of Palestinian schoolchildren (HBSC-WBG2004). Public Health Nutrition 10(7): 739–746. 10.1017/S1368980007665501
Alvarez, C.A., Yomayusa, N., Leal, A.L., Moreno, J., Mendez-Alvarez, S., Ibañez, M. and Vanegas, N. 2010. Nosocomial infections caused by community-associated methicillin-resistant Staphylococcus aureus in Colombia. American Journal of Infection Control 38(4): 315–318. 10.1016/j.ajic.2009.05.013
Anafo, R.B., Atiase, Y., Kotey, F.C.N., Dayie, N.T.K.D., Tetteh-Quarcoo, P.B., Duodu, S. et al. 2021. Methicillin-resistant Staphylococcus aureus (MRSA) nasal carriage among patients with diabetes at the Korle Bu Teaching Hospital. PLoS One 16(9): e0257004. 10.1371/journal.pone.0257004
Aswani, V.H. and Shukla, S.K. 2011. Prevalence of Staphylococcus aureus and lack of its lytic bacteriophages in the anterior nares of patients and healthcare workers at a rural clinic. Clinical Medical Research 9(2): 75–81. 10.3121/cmr.2010.954
Banerjee, T. and Anupurba, S. 2012. Colonization with vancomycin-intermediate Staphylococcus aureus strains containing the vanA resistance gene in a tertiary-care center in north India. Journal of Clinical Microbiology 50(5): 1730–1732. 10.1128/JCM.06208-11
Berbudi, A., Rahmadika, N., Tjahjadi, A.I. and Ruslami, R. 2020. Type 2 diabetes and its impact on the immune system. Current Diabetes Review 16(5): 442–449. 10.2174/1573399815666191024085838
Berman, D.S. and Eisner, W. 1993. Community-acquired methicillin-resistant Staphylococcus aureus infection. New England Journal of Medicine 329(25): 1896. 10.1056/NEJM199312163292517
Birkenhauer, E., Neethirajan, S. and Birkenhauer, E. 2014. Collagen and hyaluronan at wound sites influence early polymicrobial biofilm adhesive events. BMC Microbiology 14: 191. 10.1186/1471-2180-14-191
Brown, A.F., Leech, J.M. and Brown, A.F. 2014. Staphylococcus aureus colonization: modulation of host immune response and impact on human vaccine design. Frontiers in Immunology 4: 507. 10.3389/fimmu.2013.00507
Carek, P.J., Dickerson, L.M. and Sack, J.L. 2001. Diagnosis and management of osteomyelitis. American Family Physician 63(12): 2413–2420.
Clinical Laboratory Standards Institute (CLSI). 2020. Performance standards for antimicrobial susceptibility testing. Available at: https://www.nih.org.pk/wp-content/uploads/2021/02/CLSI-2020.pdf (Accessed February, 2021).
Cui, G., Zhao, K., You, K., Gao, Z., Kakuchi, T., Feng, B. and Duan, Q. 2020. Synthesis and characterization of phenylboronic acid-containing polymer for glucose-triggered drug delivery+. Science and Technology of Advanced Materials 21(1): 1–10. 10.1080/14686996.2019.1700394
Dawaiwala, I., Awaghade, S., Kolhatkar, P., Pawar, S. and Barsode, S. 2021. Microbiological pattern, antimicrobial resistance and prevalence of MDR/XDR organisms in patients with diabetic foot infection in an Indian tertiary care hospital. International Journal of Lower Extremity Wounds 12(3): 47–53. 10.1177/15347346211038090
El Sayed, N., Ashour, M. and Amine, A.E.K. 2018. Vancomycin resistance among Staphylococcus aureus isolates in a rural setting, Egypt. Germs 8(3): 134–139. 10.18683/germs.2018.1140
Essigmann, H.T., Hanis, C.L., DeSantis, S.M., Perkison, W.B., Aguilar, D.A., Jun, G.D. and Robinson, A. and Brown, E.L. 2022. Worsening glycemia increases the odds of intermittent but not persistent Staphylococcus aureus nasal carriage in two cohorts of Mexican-American adults. Microbiology Spectrum 10(3): e0000922. 10.1128/spectrum.00009-22
Fernández Guerrero, M.L., González López, J.J., Goyenechea, A., Fraile, J. and de Górgolas, M. 2009. Endocarditis caused by Staphylococcus aureus: a reappraisal of the epidemiologic, clinical, and pathologic manifestations with analysis of factors determining outcome. Medicine (Baltimore) 88(1): 1–22. 10.1097/MD.0b013e318194da65
Foolchand, A. and Ghazi, T. 2022. Malnutrition and dietary habits alter the immune system which may consequently influence SARS-CoV-2 virulence: a review. International Journal of Molecular Sciences 23(5): 46–53. 10.3390/ijms23052654
Fowler, V.G., Olsen, M.K. and Corey, G.R. 2003. Clinical identifiers of complicated Staphylococcus aureus bacteremia. Archives of Internal Medicine 163(17): 2066–2072. 10.1001/archinte.163.17.2066
Gao, G., Pan, X., Shao, J., Jiang, X., Su, Z., Jin, K. and Ye, J. 2022. Automatic interpretation and clinical evaluation for fundus fluorescein angiography images of diabetic retinopathy patients by deep learning. British Journal of Ophthalmology 15(2): 36–46. 10.1136/bjo-2022-321472
Geerlings, S.E. and Hoepelman, A.I. 1999. Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunology and Medical Microbiology 26(3–4): 259–265. 10.1111/j.1574-695X.1999.tb01397.x
Gorak, E.J., Yamada, S.M. and Brown, J.D. 1999. Community-acquired methicillin-resistant Staphylococcus aureus in hospitalized adults and children without known risk factors. Clinical Infectious Diseases 29(4): 797–800. 10.1086/520437
Gould, J.C. and Cruikshank, J.D. 1957. Staphylococcal infection in general practice. Lancet 273(7006): 1157–1161. 10.1016/S0140-6736(57)92063-9
Guariguata, L., Whiting, D.R., Hambleton, I., Beagley, J., Linnenkamp, U. and Shaw, J.E. 2014. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Research and Clinical Practice 103(2): 137–149. 10.1016/j.diabres.2013.11.002
Harris, L.G., Foster, S.J. and Richards, R.G. 2002. An introduction to Staphylococcus aureus, and techniques for identifying and quantifying S. aureus adhesins in relation to adhesion to biomaterials: review. European Cells & Materials 4: 39–60. 10.22203/ecm.v004a04
Herold, B.C., Immergluck, L.C. and Maranan, M.C. 1998. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. Journal of American Medical Association (JAMA) 279(8): 593–598. 10.1001/jama.279.8.593
Howard, D.H. 1956. The preservation of bacteria by freezing in glycerol broth. Journal of Bacteriology 71(5): 625. 10.1128/jb.71.5.625-625.1956
Hu, B., Das, P., Lv, D., Shi, M., Aa, J., Wang, K. et al. 2022. Effects of healthy’fecal microbiota transplantation against the deterioration of depression in fawn-hooded rats. Msystems 7(3): e00218–e00222. 10.1128/msystems.00218-22
Hunt, J.L., Purdue, G.F. and Tuggle, D.W. 1988. Morbidity and mortality of an endemic pathogen: methicillin-resistant Staphylococcus aureus. American Journal of Surgery 156(6): 524–528. 10.1016/S0002-9610(88)80545-2
Husseini, A., Abu-Rmeileh, N.M.E., Mikki, N. and Ramahi, TM. 2009. Cardiovascular diseases, diabetes mellitus, and cancer in the occupied Palestinian territory. Lancet 373(9668): 1041–1049. 10.1016/S0140-6736(09)60109-4
Jauneikaite, E., Ferguson, T., Mosavie, M., Fallowfield, J.L., Davey, T., Thorpe, N. et al. 2020. Staphylococcus aureus colonization and acquisition of skin and soft tissue infection among Royal Marines recruits: a prospective cohort study. Clinical Micro-biology and Infection 26(3): 381 e381–381 e386. 10.1016/j.cmi.2019.07.014
Kaibni, M.H., Farraj, M.A., Adwan, K. and Essawi, T.A. 2009. Community-acquired meticillin-resistant Staphylococcus aureus in Palestine. Journal of Medical Microbiology 58(Pt 5): 644–647. 10.1099/jmm.0.007617-0
Kalan Farmanfarma, K.H., Ansari-Moghaddam, A., Zareban, I. and Adineh, H.A. 2020. Prevalence of type 2 diabetes in Middle-East: systematic review & meta-analysis. Primary Care Diabetes 14(4): 297–304. 10.1016/j.pcd.2020.01.003
Kluytmans, J. van Belkum, A. and Verbrugh, H. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clinical Microbiology Reviews 10(3): 505–520. 10.1128/CMR.10.3.505
Koupahi, H., Jahromy, S.H. and Rahbar, M. 2016. Evaluation of different phenotypic and genotypic methods for detection of methicillin-resistant Staphylococcus aureus (MRSA). Iranian Journal of Pathology 11(4): 370–376.
Lakhundi, S. and Zhang, K. 2018. Methicillin-resistant Staphylo-coccus aureus: molecular characterization, evolution, and epidemiology. Clinical Microbiology Reviews 31(4): 25–36. 10.1128/CMR.00020-18
Lavery, L.A., La Fontaine, J., Bhavan, K., Kim, P.J., Williams, J.R. and Hunt, N.A. 2014. Risk factors for methicillin-resistant Staphylococcus aureus in diabetic foot infections. Diabetic Foot & Ankle 5(1): 25–36. 10.3402/dfa.v5.23575
Lin, J., Xu, P., Peng, Y., Lin, D., Ou, D., Zhang, T., Bai, C. et al. 2017. Prevalence and characteristics of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus nasal colonization among a community-based diabetes population in Foshan, China. Journal of Diabetes Investigation 8(3): 383–391. 10.1111/jdi.12591
Lin, S-Y., Lin, N-Y., Huang, Y-Y., Hsieh, C-C. and Huang, Y-C. 2020. Methicillin-resistant Staphylococcus aureus nasal carriage and infection among patients with diabetic foot ulcer. Journal of Microbiology, Immunology and Infection 53(2): 292–299. 10.1016/j.jmii.2018.03.005
Lipsky, B.A., Pecoraro, R.E., Chen, M.S. and Koepsell, T.D. 1987. Factors affecting staphylococcal colonization among NIDDM outpatients. Diabetes Care 10(4): 483–486. 10.2337/diacare.10.4.483
Lopez Plaza, B. and Bermejo Lopez, L.M. 2017. Nutrition and immune system disorders. Nutrición Hospitalaria 34(Suppl 4): 68–71. 10.20960/nh.1575
Lowy, F.D. 1998. Staphylococcus aureus infections. New England Journal of Medicine 339(8): 520–532. 10.1056/NEJM199808203390806
Coles, G.A., Faller, B., Slingeneyer, A., Dah, G.A., Briat, C. et al. 1990. Staphylococcus aureus nasal carriage and infection in patients on continuous ambulatory peritoneal dialysis. New England Journal of Medicine 322(8): 505–509. 10.1056/NEJM199002223220804
Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G. et al. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection 18(3): 268–281. 10.1111/j.1469-0691.2011.03570.x
Mascaro, V., Squillace, L., Nobile, C.G.A., Papadopoli, R., Bosch, T., Schouls, L.M. et al. 2019. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) carriage and pattern of anti-biotic resistance among sheep farmers from southern Italy. Infection and Drug Resistance 12: 2561–2571. 10.2147/IDR.S211629
McGuinness, W.A., Malachowa, N. and DeLeo, F.R. 2017. Vancomycin resistance in Staphylococcus aureus. Yale Journal of Biology and Medicine 90(2): 269–281.
Medina, E. and Pieper, D.H. 2016. Tackling threats and future problems of multidrug-resistant bacteria. Current Topics in Microbiology and Immunology 398: 3–33. 10.1007/82_2016_492
Mikki, N., Abdul-Rahim, H.F., Shi, Z. and Holmboe-Ottesen, G. 2010. Dietary habits of Palestinian adolescents and associated sociodemographic characteristics in Ramallah, Nablus and Hebron governorates. Public Health Nutrition 13(9): 1419–1429. 10.1017/S1368980010000662
Mlynarczyk-Bonikowska, B., Kowalewski, C., Krolak-Ulinska, A. and Marusza, W. 2022. Molecular mechanisms of drug resistance in Staphylococcus aureus. International Journal of Molecular Science 23(15): 8088. 10.3390/ijms23158088
Munteanu, C. and Schwartz, B. 2022. The relationship between nutrition and the immune system. Frontiers in Nutrition 9: 1082500. 10.3389/fnut.2022.1082500
Nguyen, R. et al. 2022. Bacitracin topical. StatPearls, Treasure Island, FL.
Ontario, H. 2022. Pre-surgical nasal decolonization of Staphylo-coccus aureus: a health technology assessment. Ontario Health Technology Assessment 22(4): 1–165.
Pantosti, A., Sanchini, A. and Monaco, M. 2007. Mechanisms of antibiotic resistance in Staphylococcus aureus. Future in Microbiology 2(3): 323–334. 10.2217/17460913.2.3.323
Pate, K.R., Nolah, R.L., Bannerman, T.L. and Feldman, S. 1995. Methicillin-resistant Staphylococcus aureus in the community. Lancet 346(8980): 978. 10.1016/S0140-6736(95)91605-9
Patel, N., Gold, J., Brown, N.J., Abraham, M., Beyer, R.S., Yang, C. et al. 2022. Staphylococcus aureus swabbing and decolonization before neuromodulation procedures: a systematic review and meta-analysis. Neuromodulation 26(5): 928–937. 10.1016/j.neurom.2022.07.013
Patricia, M. 2017. Bailey & Scott’s diagnostic microbiology. Elsevier, St Louis, MO.
Qin, X., Zhang, K., Fan, Y., Fang, H., Nie, Y. and Wu, X-L. 2022. The bacterial MtrAB two-component system regulates the cell wall homeostasis responding to environmental alkaline stress. Microbiology Spectrum 10(5): e02311–e02322. 10.1128/spectrum.02311-22
Rahim, H.F.A., Sibai, A., Khader, Y., Hwalla, N., Fadhil, I., Alsiyabi, H., et al. 2014. Non-communicable diseases in the Arab world. Lancet 383(9914): 356–367. 10.1016/S0140-6736(13)62383-1
Saklayen, M.G. 2018. The global epidemic of the metabolic syndrome. Current Hypertension Reports 20(2): 12. 10.1007/s11906-018-0812-z
Sakr, A., Brégeon, F., Mège, J-L., Rolain, J-M., Blin, O. 2018. Staphylococcus aureus nasal colonization: an update on mechanisms, epidemiology, risk factors, and subsequent infections. Frontiers in Microbiology 9: 2419. 10.3389/fmicb.2018.02419
Salgado, C.D., Farr, B.M. and Calfee, D.P. 2003. Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clinical Infectious Diseases 36(2): 131–139. 10.1086/345436
Sami, W., Ansari, T., Butt, N.S. and Ab Hamid, M.R. 2017. Effect of diet on type 2 diabetes mellitus: a review. International Journal of Health Sciences (Qassim) 11(2): 65–71.
Schlesinger, L.S., Stephen, C.R. and Dennis, R.G. 1987. Staphylo-coccus aureus meningitis: a broad-based epidemiologic study. Medicine (Baltimore) 66(2): 148–156. 10.1097/00005792-198703000-00006
Singer, A.J. and Talan, D.A. 2014. Management of skin abscesses in the era of methicillin-resistant Staphylococcus aureus. New England Journal of Medicine 370(11): 1039–1047. 10.1056/NEJMra1212788
Stacey, H.J., Clements, C.S., Welburn, S.C. and Jones, J.D. 2019. The prevalence of methicillin-resistant Staphylococcus aureus among diabetic patients: a meta-analysis. Acta Diabetology 56(8): 907–921. 10.1007/s00592-019-01301-0
Sujatha, S. and Praharaj, I. 2012. Glycopeptide resistance in gram-positive cocci: a review. Interdisciplinary Perspectives on Infectious Diseases 2012: 781679. 10.1155/2012/781679
Szymanek-Majchrzak, K., Mlynarczyk, A. and Mlynarczyk, G. 2018. Characteristics of glycopeptide-resistant Staphylococcus aureus strains isolated from inpatients of three teaching hospitals in Warsaw, Poland. Antimicrobial Resistance & Infection Control 7: 105. 10.1186/s13756-018-0397-y
Tamer, A., Karabay, O. and Ekerbicer, H. 2006. Staphylococcus aureus nasal carriage and associated factors in type 2 diabetic patients. Japan Journal of Infectious Diseases 59(1): 10–14.
Tarai, B., Das, P. and Kumar, D. 2013. Recurrent challenges for clinicians: emergence of methicillin-resistant Staphylococcus aureus, vancomycin resistance, and current treatment options. Journal of Laboratory Physicians 5(2): 71–78. 10.4103/0974-2727.119843
Teufel, F., Seiglie, J.A., Geldsetzer, P., Theilmann, M., Marcus, M.E., Ebert, C., Arboleda, W.A.L. et al. 2021. Body-mass index and diabetes risk in 57 low-income and middle-income countries: a cross-sectional study of nationally representative, individual-level data in 685 616 adults. Lancet 398(10296): 238–248. 10.1016/S0140-6736(21)00844-8
Tian, Z., Zhang, Y., Zheng, Z., Zhang, M., Zhang, T., Jin, J. et al. 2022. Gut microbiome dysbiosis contributes to abdominal aortic aneurysm by promoting neutrophil extracellular trap formation. Cell Host & Microbe 30(10): 1450–1463. e1458. 10.1016/j.chom.2022.09.004
van der Berg, J.D., Stehouwer, C.D.A., Bosma, H., van der Velde, J.H.P.M., Willems, P.J.B., Savelberg, H.H.C.M. et al. 2016. Associations of total amount and patterns of sedentary behaviour with type 2 diabetes and the metabolic syndrome: the Maastricht study. Diabetologia 59(4): 709–718. 10.1007/s00125-015-3861-8
Vandenesch, F., Naimi, T., Enright, M.C., Lina, G., Nimmo, G.R., Heffernan, H. et al. 2003. Community-acquired methicillin-resistant Staphylococcus aureus carrying panton-valentine leukocidin genes: worldwide emergence. Emerging Infectious Diseases 9(8): 978–984. 10.3201/eid0908.030089
Ventola, C.L. 2015. The antibiotic resistance crisis: part 1: causes and threats. Physical Therapy 40(4): 277–283.
Wertheim, H.F., Melles, D.C., Vos, M.C., van Leeuwen, W., van Belkum, A., Verbrugh, H.A. and Nouwen, J.L. 2005. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infectious Diseases 5(12): 751–762. 10.1016/S1473-3099(05)70295-4
Yang, R., Hou, E., Cheng, W., Yan, X., Zhang, T., Li, S. et al. 2022. Membrane-targeting neolignan-antimicrobial peptide mimic conjugates to combat methicillin-resistant Staphylococcus aureus (MRSA) infections. Journal of Medicinal Chemistry 65(24): 16879–16892. 10.1021/acs.jmedchem.2c01674
Zhang, N., Lu, D., Sheng, H., Xia, J., Kan, P., Yao, Z. et al. 2023. Constructed wetlands as hotspots of antibiotic resistance genes and pathogens: evidence from metagenomic analysis in Chinese rural areas. Journal of Hazardous Materials 447: 130778. 10.1016/j.jhazmat.2023.130778
Zheng, Y., Ley, S.H. and Hu, F.B. 2018. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nature Reviews Endocrinology 14(2): 88–98. 10.1038/nrendo.2017.151
Zimmet, P.Z., Magliano, D.J., Herman, W.H. and Shaw, J.E. 2014. Diabetes: a 21st century challenge. Lancet Diabetes and Endocrinology 2(1): 56–64. 10.1016/S2213-8587(13)70112-8
Zyoud, S.H., Taha, A.A., Araj, K.F., Abahri, I.A., Sawalha, A.F., Sweileh, W.M. et al. 2015. Parental knowledge, attitudes and practices regarding antibiotic use for acute upper respiratory tract infections in children: a cross-sectional study in Palestine. BMC Pediatrics 15: 176. 10.1186/s12887-015-0494-5