Empirical antimicrobial therapy based on active surveillance cultures in ICU patients
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Published:
Jun 20, 2023
Keywords:
Intensive Care Units, Mass screening, Evidence-Based Pharmacy Practice, Pharmaceutical Services
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Abstract
Objective: To assess the predictive value of prior carbapenem-resistant Acinetobacter baumannii (CRAB) and Pseudomonas aeruginosa (CRPA) colonization established in surveillance cultures for subsequent infection by these pathogens in ICU patients. Methods: A cohort study was performed with patients admitted to the intensive care unit for at least 48 h. Negative and positive predictive values, sensitivity, and specificity of surveillance cultures in CRAB and CRPA were measured. Results: 693 infected patients were included. Patients previously colonized by CRAB and CRPA were more likely to be infected by these pathogens: adjusted OR: 10.34 (6.58 - 16.45; p < 0.001) and 2.30 (3.88 - 10.26; p < 0.001), respectively. We found high negative predictive values of surveillance cultures for CRAB (87.18%) and CRPA (88.30%) and high specificity 91.96% and 90.13%, respectively. Conclusions: Patients not colonized by CRAB and CRPA were less prone to infection by these pathogens. These findings may contribute to the choice of empirical antimicrobial therapy and discourage the prescription of antibiotics against these pathogens in patients without previous colonization.
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1.
Ramos Silva A, Nagem Lopes LP, Fernandez-Llimos F, Costa Lima E. Empirical antimicrobial therapy based on active surveillance cultures in ICU patients. Health Sci J [Internet]. 2023Jun.20 [cited 2024Apr.30];13(2):19-4. Available from: https://portalrcs.hcitajuba.org.br/index.php/rcsfmit_zero/article/view/1379
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References
1. Provenzani A, Hospodar AR, Meyer AL, Leonardi Vinci D, Hwang EY, Butrus CM, et al. Multidrug-resistant gram-negative organisms: a review of recently approved antibiotics and novel pipeline agents. Int J Clin Pharm 2020;42(4):1016-25. https://doi.org/10.1007/s11096-020-01089-y
2. Centers for Disease Control and Prevention. Antibiotic Resistance Threatens Everyone. Centers for Disease Control and Prevention [Internet]. [cited 24 Jun 2024]. Available from: https://www.cdc.gov/drugresistance/index.html
3. World Health Organization. Guidelines on core components of infection prevention and control programmes at the national and acute health care facility level [Internet]. 1 Nov 2016 [cited 25 May 2023] Available at https://www.who.int/publications-detail-redirect/9789241549929
4. Biswal M, Angrup A, Kanaujia R. Role of surveillance cultures in infection control. Indian J Med Microbiol. 2020;38(3 & 4):277-283. https://doi.org/10.4103/ijmm.IJMM_20_129
5. Karaiskos I, Lagou S, Pontikis K, Rapti V, Poulakou G. The "Old" and the "New" Antibiotics for MDR Gram-Negative Pathogens: For Whom, When, and How. Front Public Health. 2019;7:151. https://doi.org/10.3389/fpubh.2019.00151
6. Iskandar K, Murugaiyan J, Hammoudi Halat D, Hage SE, Chibabhai V, Adukkadukkam S, Roques C, Molinier L, Salameh P, Van Dongen M. Antibiotic Discovery and Resistance: The Chase and the Race. Antibiotics (Basel). 2022;11(2):182. https://doi.org/10.3390/antibiotics11020182
7. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, et al; WHO Pathogens Priority List Working Group. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318-327. https://doi.org/10.1016/S1473-3099(17)30753-3
8. Mulani MS, Kamble EE, Kumkar SN, Tawre MS, Pardesi KR. Emerging Strategies to Combat ESKAPE Pathogens in the Era of Antimicrobial Resistance: A Review. Front Microbiol. 2019;10:539. https://doi.org/10.3389/fmicb.2019.00539
9. Agência Nacional de Vigilância Sanitária Imprensa. Boletim Segurança do Paciente e Qualidade em Serviços de Saúde no 23 - Avaliação Nacional dos indicadores de IRAS e RM – 2020 [Internet]. 30 Dec 2016 [updated 23 Oct 2020; cited 25 May 2023]. Available from: https://bit.ly/3qcHV7P
10. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A. 2018;115(15):E3463-E3470. https://doi.org/10.1073/pnas.1717295115
11. Sartelli M, C Hardcastle T, Catena F, Chichom-Mefire A, Coccolini F, Dhingra S, et al. Antibiotic Use in Low and Middle-Income Countries and the Challenges of Antimicrobial Resistance in Surgery. Antibiotics (Basel). 2020;9(8):497. https://doi.org/10.3390/antibiotics9080497
12. Evans L, Rhodes A, Alhazzani W, Antonelli M, Coopersmith CM, French C, et al. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock 2021. Intensive Care Med. 2021;47(11):1181-1247. https://doi.org/10.1007/s00134-021-06506-y
13. da Fonseca Pestana Ribeiro JM, Park M. Less empiric broad-spectrum antibiotics is more in the ICU. Intensive Care Med. 2020;46(4):783-786. https://doi.org/10.1007/s00134-019-05863-z
14. Yoshida H, Motohashi T, De Bus L, De Waele J, Takaba A, Kuriyama A, et al. Use of broad-spectrum antimicrobials for more than 72 h and the detection of multidrug-resistant bacteria in Japanese intensive care units: a multicenter retrospective cohort study. Antimicrob Resist Infect Control. 2022;11(1):119. https://doi.org/10.1186/s13756-022-01146-3
15. Golli AL, Cristea OM, Zlatian O, Glodeanu AD, Balasoiu AT, Ionescu M, et al. Prevalence of Multidrug-Resistant Pathogens Causing Bloodstream Infections in an Intensive Care Unit. Infect Drug Resist. 2022;15:5981-5992. https://doi.org/10.2147/IDR.S383285
16. Mathew P, Ranjalkar J, Chandy SJ. Challenges in Implementing Antimicrobial Stewardship Programmes at Secondary Level Hospitals in India: An Exploratory Study. Front Public Health. 2020;8:493904. https://doi.org/10.3389/fpubh.2020.493904
17. Agência Nacional de Vigilância Sanitária. Confira dados sobre gerenciamento do uso de antimicrobianos [Internet]. 24 Nov 2020 [updated 3 Nov 2022; cited 25 May 2023]. Available from: https://bit.ly/3ozsyWA
18. Spoto S, Daniel Markley J, Valeriani E, Abbate A, Argemi J, Markley R, et al. Active Surveillance Cultures and Procalcitonin in Combination With Clinical Data to Guide Empirical Antimicrobial Therapy in Hospitalized Medical Patients With Sepsis. Front Microbiol. 2022;13:797932. https://doi.org/10.3389/fmicb.2022.797932
19. Rottier WC, Bamberg YR, Dorigo-Zetsma JW, van der Linden PD, Ammerlaan HS, Bonten MJ. Predictive value of prior colonization and antibiotic use for third-generation cephalosporin-resistant enterobacteriaceae bacteremia in patients with sepsis. Clin Infect Dis. 2015;60(11):1622-30. https://doi.org/10.1093/cid/civ121
20. Dunaway S, Orwig KW, Arbogast ZQ, Myers ZL, Sizemore JA, Giancola SE. Evaluation of a pharmacy-driven methicillin-resistant Staphylococcus aureus surveillance protocol in pneumonia. Int J Clin Pharm. 2018;40(3):526-532. https://doi.org/10.1007/s11096-018-0647-3
21. Arpad D. Colonization and infection. Cent European J Urol. 2014;67(1):86-7. https://doi.org/10.5173/ceju.2014.01.art19
22. Kawamura T. Interpretação de um teste sob a visão epidemiológica: eficiência de um teste [The interpretation of a test under an epidemiological view point. Test efficiency]. Arq Bras Cardiol. 2002;79(4):437-41. Portuguese. https://doi.org/10.1590/S0066-782X2002001300015
23. Mandell GL, Bennett JE, Dolin, R. - Principles and Practice of Infectious Diseases, 8th ed. Churchill Livingdtone: Philadelphia, PA; 2014.
24. Saharman YR, Karuniawati A, Sedono R, Aditianingsih D, Qi H, Verbrugh HA, Severin JA. Multimodal intervention to reduce acquisition of carbapenem-non-susceptible Gram-negative bacteria in intensive care units in the National Referral Hospital of Indonesia: An interrupted time series study. J Crit Care. 2021;64:237-244. https://doi.org/10.1016/j.jcrc.2021.04.016
25. Massart N, Camus C, Benezit F, Moriconi M, Fillatre P, Le Tulzo Y. Incidence and risk factors for acquired colonization and infection due to extended-spectrum beta-lactamase-producing Gram-negative bacilli: a retrospective analysis in three ICUs with low multidrug resistance rate. Eur J Clin Microbiol Infect Dis. 2020;39(5):889-895.https://doi.org/10.1007/s10096-019-03800-y
26. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373-83. https://doi.org/10.1016/0021-9681(87)90171-8
27. Silva Junior JM, Malbouisson LM, Nuevo HL, Barbosa LG, Marubayashi LY, Teixeira IC, et al. Applicability of the simplified acute physiology score (SAPS 3) in Brazilian hospitals. Rev Bras Anestesiol. 2010;60(1):20-31. https://doi.org/10.1590/S0034-70942010000100003
28. Lee SY, An SH. Impact of pharmacist intervention in antibiotic stewardship programmes for critically ill neonates: A systematic review and meta-analysis. J Clin Pharm Ther. 2022;47(4):430-444. https://doi.org/10.1111/jcpt.13553
29. Will E, Kristen P, Ronald T. Pharmacist-driven methicillin-resistant Staphylococcus aureus screening protocol and the impact on vancomycin exposure in hospitalized patients with pneumonia. J Am Coll Clin Pharm. 2021;4(12):1548-53. https://doi.org/10.1002/jac5.1530
30. Harris AD, Furuno JP, Roghmann MC, Johnson JK, Conway LJ, Venezia RA, et al. Targeted surveillance of methicillin-resistant Staphylococcus aureus and its potential use to guide empiric antibiotic therapy. Antimicrob Agents Chemother. 2010;54(8):3143-8. https://doi.org/10.1128/AAC.01590-09
31. Baba H, Nimmo GR, Allworth AM, Boots RJ, Hayashi Y, Lipman J, et al. The role of surveillance cultures in the prediction of susceptibility patterns of Gram-negative bacilli in the intensive care unit. Eur J Clin Microbiol Infect Dis. 2011;30(6):739-44. https://doi.org/10.1007/s10096-010-1146-1
32. Alsadoon A, Alhamwah M, Alomar B, Alsubaiel S, Almutairi AF, Vishwakarma RK, et al. Association of Antibiotics Administration Timing With Mortality in Children With Sepsis in a Tertiary Care Hospital of a Developing Country. Front Pediatr. 2020;8:566. https://doi.org/10.3389/fped.2020.00566
33. Arulappen AL, Danial M, Ng LW, Teoh JC. The Impact of Antibiotics Administration on Mortality for Time in Sepsis and Septic Shock Patients including Possible Reasons for Delayed Administration in Malaysia. Antibiotics (Basel). 2022;11(9):1202. https://doi.org/10.3390/antibiotics11091202
34. Andersson M, Östholm-Balkhed Å, Fredrikson M, Holmbom M, Hällgren A, Berg S, Hanberger H. Delay of appropriate antibiotic treatment is associated with high mortality in patients with community-onset sepsis in a Swedish setting. Eur J Clin Microbiol Infect Dis. 2019;38(7):1223-1234. https://doi.org/10.1007/s10096-019-03529-8
35. Andersson M, Östholm-Balkhed Å, Fredrikson M, Holmbom M, Hällgren A, Berg S, et al. Delay of appropriate antibiotic treatment is associated with high mortality in patients with community-onset sepsis in a Swedish setting. Eur J Clin Microbiol Infect Dis. 2019;38(7):1223-1234. https://doi.org/10.1186/s13756-022-01146-3
36. Monaghan TF, Rahman SN, Agudelo CW, Wein AJ, Lazar JM, Everaert K, et al. Foundational Statistical Principles in Medical Research: Sensitivity, Specificity, Positive Predictive Value, and Negative Predictive Value. Medicina (Kaunas). 2021;57(5):503. https://doi.org/10.3390/medicina57050503
37. MacFadden DR, Coburn B, Shah N, Robicsek A, Savage R, Elligsen M, Daneman N. Utility of prior cultures in predicting antibiotic resistance of bloodstream infections due to Gram-negative pathogens: a multicentre observational cohort study. Clin Microbiol Infect. 2018;24(5):493-499. https://doi.org/10.1016/j.cmi.2017.07.032
38. Saharman YR, Karuniawati A, Severin JA, Verbrugh HA. Infections and antimicrobial resistance in intensive care units in lower-middle income countries: a scoping review. Antimicrob Resist Infect Control. 2021;10(1):22. https://doi.org/10.1186/s13756-020-00871-x
39. Dreischulte T, van den Bemt B, Steurbaut S; European Society of Clinical Pharmacy. European Society of Clinical Pharmacy definition of the term clinical pharmacy and its relationship to pharmaceutical care: a position paper. Int J Clin Pharm. 2022;44(4):837-842. https://doi.org/10.1007/s11096-022-01422-7
40. Iskandar K, Molinier L, Hallit S, Sartelli M, Hardcastle TC, Haque M, et al. Surveillance of antimicrobial resistance in low- and middle-income countries: a scattered picture. Antimicrob Resist Infect Control. 2021;10(1):63. https://doi.org/10.1186/s13756-021-00931-w
2. Centers for Disease Control and Prevention. Antibiotic Resistance Threatens Everyone. Centers for Disease Control and Prevention [Internet]. [cited 24 Jun 2024]. Available from: https://www.cdc.gov/drugresistance/index.html
3. World Health Organization. Guidelines on core components of infection prevention and control programmes at the national and acute health care facility level [Internet]. 1 Nov 2016 [cited 25 May 2023] Available at https://www.who.int/publications-detail-redirect/9789241549929
4. Biswal M, Angrup A, Kanaujia R. Role of surveillance cultures in infection control. Indian J Med Microbiol. 2020;38(3 & 4):277-283. https://doi.org/10.4103/ijmm.IJMM_20_129
5. Karaiskos I, Lagou S, Pontikis K, Rapti V, Poulakou G. The "Old" and the "New" Antibiotics for MDR Gram-Negative Pathogens: For Whom, When, and How. Front Public Health. 2019;7:151. https://doi.org/10.3389/fpubh.2019.00151
6. Iskandar K, Murugaiyan J, Hammoudi Halat D, Hage SE, Chibabhai V, Adukkadukkam S, Roques C, Molinier L, Salameh P, Van Dongen M. Antibiotic Discovery and Resistance: The Chase and the Race. Antibiotics (Basel). 2022;11(2):182. https://doi.org/10.3390/antibiotics11020182
7. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, et al; WHO Pathogens Priority List Working Group. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318-327. https://doi.org/10.1016/S1473-3099(17)30753-3
8. Mulani MS, Kamble EE, Kumkar SN, Tawre MS, Pardesi KR. Emerging Strategies to Combat ESKAPE Pathogens in the Era of Antimicrobial Resistance: A Review. Front Microbiol. 2019;10:539. https://doi.org/10.3389/fmicb.2019.00539
9. Agência Nacional de Vigilância Sanitária Imprensa. Boletim Segurança do Paciente e Qualidade em Serviços de Saúde no 23 - Avaliação Nacional dos indicadores de IRAS e RM – 2020 [Internet]. 30 Dec 2016 [updated 23 Oct 2020; cited 25 May 2023]. Available from: https://bit.ly/3qcHV7P
10. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A. 2018;115(15):E3463-E3470. https://doi.org/10.1073/pnas.1717295115
11. Sartelli M, C Hardcastle T, Catena F, Chichom-Mefire A, Coccolini F, Dhingra S, et al. Antibiotic Use in Low and Middle-Income Countries and the Challenges of Antimicrobial Resistance in Surgery. Antibiotics (Basel). 2020;9(8):497. https://doi.org/10.3390/antibiotics9080497
12. Evans L, Rhodes A, Alhazzani W, Antonelli M, Coopersmith CM, French C, et al. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock 2021. Intensive Care Med. 2021;47(11):1181-1247. https://doi.org/10.1007/s00134-021-06506-y
13. da Fonseca Pestana Ribeiro JM, Park M. Less empiric broad-spectrum antibiotics is more in the ICU. Intensive Care Med. 2020;46(4):783-786. https://doi.org/10.1007/s00134-019-05863-z
14. Yoshida H, Motohashi T, De Bus L, De Waele J, Takaba A, Kuriyama A, et al. Use of broad-spectrum antimicrobials for more than 72 h and the detection of multidrug-resistant bacteria in Japanese intensive care units: a multicenter retrospective cohort study. Antimicrob Resist Infect Control. 2022;11(1):119. https://doi.org/10.1186/s13756-022-01146-3
15. Golli AL, Cristea OM, Zlatian O, Glodeanu AD, Balasoiu AT, Ionescu M, et al. Prevalence of Multidrug-Resistant Pathogens Causing Bloodstream Infections in an Intensive Care Unit. Infect Drug Resist. 2022;15:5981-5992. https://doi.org/10.2147/IDR.S383285
16. Mathew P, Ranjalkar J, Chandy SJ. Challenges in Implementing Antimicrobial Stewardship Programmes at Secondary Level Hospitals in India: An Exploratory Study. Front Public Health. 2020;8:493904. https://doi.org/10.3389/fpubh.2020.493904
17. Agência Nacional de Vigilância Sanitária. Confira dados sobre gerenciamento do uso de antimicrobianos [Internet]. 24 Nov 2020 [updated 3 Nov 2022; cited 25 May 2023]. Available from: https://bit.ly/3ozsyWA
18. Spoto S, Daniel Markley J, Valeriani E, Abbate A, Argemi J, Markley R, et al. Active Surveillance Cultures and Procalcitonin in Combination With Clinical Data to Guide Empirical Antimicrobial Therapy in Hospitalized Medical Patients With Sepsis. Front Microbiol. 2022;13:797932. https://doi.org/10.3389/fmicb.2022.797932
19. Rottier WC, Bamberg YR, Dorigo-Zetsma JW, van der Linden PD, Ammerlaan HS, Bonten MJ. Predictive value of prior colonization and antibiotic use for third-generation cephalosporin-resistant enterobacteriaceae bacteremia in patients with sepsis. Clin Infect Dis. 2015;60(11):1622-30. https://doi.org/10.1093/cid/civ121
20. Dunaway S, Orwig KW, Arbogast ZQ, Myers ZL, Sizemore JA, Giancola SE. Evaluation of a pharmacy-driven methicillin-resistant Staphylococcus aureus surveillance protocol in pneumonia. Int J Clin Pharm. 2018;40(3):526-532. https://doi.org/10.1007/s11096-018-0647-3
21. Arpad D. Colonization and infection. Cent European J Urol. 2014;67(1):86-7. https://doi.org/10.5173/ceju.2014.01.art19
22. Kawamura T. Interpretação de um teste sob a visão epidemiológica: eficiência de um teste [The interpretation of a test under an epidemiological view point. Test efficiency]. Arq Bras Cardiol. 2002;79(4):437-41. Portuguese. https://doi.org/10.1590/S0066-782X2002001300015
23. Mandell GL, Bennett JE, Dolin, R. - Principles and Practice of Infectious Diseases, 8th ed. Churchill Livingdtone: Philadelphia, PA; 2014.
24. Saharman YR, Karuniawati A, Sedono R, Aditianingsih D, Qi H, Verbrugh HA, Severin JA. Multimodal intervention to reduce acquisition of carbapenem-non-susceptible Gram-negative bacteria in intensive care units in the National Referral Hospital of Indonesia: An interrupted time series study. J Crit Care. 2021;64:237-244. https://doi.org/10.1016/j.jcrc.2021.04.016
25. Massart N, Camus C, Benezit F, Moriconi M, Fillatre P, Le Tulzo Y. Incidence and risk factors for acquired colonization and infection due to extended-spectrum beta-lactamase-producing Gram-negative bacilli: a retrospective analysis in three ICUs with low multidrug resistance rate. Eur J Clin Microbiol Infect Dis. 2020;39(5):889-895.https://doi.org/10.1007/s10096-019-03800-y
26. Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40(5):373-83. https://doi.org/10.1016/0021-9681(87)90171-8
27. Silva Junior JM, Malbouisson LM, Nuevo HL, Barbosa LG, Marubayashi LY, Teixeira IC, et al. Applicability of the simplified acute physiology score (SAPS 3) in Brazilian hospitals. Rev Bras Anestesiol. 2010;60(1):20-31. https://doi.org/10.1590/S0034-70942010000100003
28. Lee SY, An SH. Impact of pharmacist intervention in antibiotic stewardship programmes for critically ill neonates: A systematic review and meta-analysis. J Clin Pharm Ther. 2022;47(4):430-444. https://doi.org/10.1111/jcpt.13553
29. Will E, Kristen P, Ronald T. Pharmacist-driven methicillin-resistant Staphylococcus aureus screening protocol and the impact on vancomycin exposure in hospitalized patients with pneumonia. J Am Coll Clin Pharm. 2021;4(12):1548-53. https://doi.org/10.1002/jac5.1530
30. Harris AD, Furuno JP, Roghmann MC, Johnson JK, Conway LJ, Venezia RA, et al. Targeted surveillance of methicillin-resistant Staphylococcus aureus and its potential use to guide empiric antibiotic therapy. Antimicrob Agents Chemother. 2010;54(8):3143-8. https://doi.org/10.1128/AAC.01590-09
31. Baba H, Nimmo GR, Allworth AM, Boots RJ, Hayashi Y, Lipman J, et al. The role of surveillance cultures in the prediction of susceptibility patterns of Gram-negative bacilli in the intensive care unit. Eur J Clin Microbiol Infect Dis. 2011;30(6):739-44. https://doi.org/10.1007/s10096-010-1146-1
32. Alsadoon A, Alhamwah M, Alomar B, Alsubaiel S, Almutairi AF, Vishwakarma RK, et al. Association of Antibiotics Administration Timing With Mortality in Children With Sepsis in a Tertiary Care Hospital of a Developing Country. Front Pediatr. 2020;8:566. https://doi.org/10.3389/fped.2020.00566
33. Arulappen AL, Danial M, Ng LW, Teoh JC. The Impact of Antibiotics Administration on Mortality for Time in Sepsis and Septic Shock Patients including Possible Reasons for Delayed Administration in Malaysia. Antibiotics (Basel). 2022;11(9):1202. https://doi.org/10.3390/antibiotics11091202
34. Andersson M, Östholm-Balkhed Å, Fredrikson M, Holmbom M, Hällgren A, Berg S, Hanberger H. Delay of appropriate antibiotic treatment is associated with high mortality in patients with community-onset sepsis in a Swedish setting. Eur J Clin Microbiol Infect Dis. 2019;38(7):1223-1234. https://doi.org/10.1007/s10096-019-03529-8
35. Andersson M, Östholm-Balkhed Å, Fredrikson M, Holmbom M, Hällgren A, Berg S, et al. Delay of appropriate antibiotic treatment is associated with high mortality in patients with community-onset sepsis in a Swedish setting. Eur J Clin Microbiol Infect Dis. 2019;38(7):1223-1234. https://doi.org/10.1186/s13756-022-01146-3
36. Monaghan TF, Rahman SN, Agudelo CW, Wein AJ, Lazar JM, Everaert K, et al. Foundational Statistical Principles in Medical Research: Sensitivity, Specificity, Positive Predictive Value, and Negative Predictive Value. Medicina (Kaunas). 2021;57(5):503. https://doi.org/10.3390/medicina57050503
37. MacFadden DR, Coburn B, Shah N, Robicsek A, Savage R, Elligsen M, Daneman N. Utility of prior cultures in predicting antibiotic resistance of bloodstream infections due to Gram-negative pathogens: a multicentre observational cohort study. Clin Microbiol Infect. 2018;24(5):493-499. https://doi.org/10.1016/j.cmi.2017.07.032
38. Saharman YR, Karuniawati A, Severin JA, Verbrugh HA. Infections and antimicrobial resistance in intensive care units in lower-middle income countries: a scoping review. Antimicrob Resist Infect Control. 2021;10(1):22. https://doi.org/10.1186/s13756-020-00871-x
39. Dreischulte T, van den Bemt B, Steurbaut S; European Society of Clinical Pharmacy. European Society of Clinical Pharmacy definition of the term clinical pharmacy and its relationship to pharmaceutical care: a position paper. Int J Clin Pharm. 2022;44(4):837-842. https://doi.org/10.1007/s11096-022-01422-7
40. Iskandar K, Molinier L, Hallit S, Sartelli M, Hardcastle TC, Haque M, et al. Surveillance of antimicrobial resistance in low- and middle-income countries: a scattered picture. Antimicrob Resist Infect Control. 2021;10(1):63. https://doi.org/10.1186/s13756-021-00931-w