Impact of Antimicrobial-Resistant Bacterial Pneumonia on In-Hospital Mortality and Length of Hospital Stay: A Retrospective Cohort Study in Spain
Abstract
1. Introduction
- Critical priority group—The highest threat to public health due to limited treatment options: Enterobacterales carbapenem-resistant, Enterobacterales third-generation cephalosporin-resistant, Acinetobacter baumannii carbapenem-resistant, and Mycobacterium tuberculosis rifampicin-resistant.
- High priority group—AMR pathogens that are significantly difficult to treat: Salmonella typhi fluoroquinolone-resistant, Shigella spp. fluoroquinolone-resistant, Enterococcus faecium vancomycin-resistant, Pseudomonas aeruginosa carbapenem-resistant, non-typhoidal Salmonella fluoroquinolone-resistant, Neisseria gonorrhoeae third-generation cephalosporin and/or fluoroquinolone-resistant, and Staphylococcus aureus methicillin-resistant (MRSA).
- Medium priority group—AMR pathogens that are associated with moderate difficulty for treatment): Group A Streptococci macrolide-resistant, Streptococcus pneumoniae macrolide-resistant, Haemophilus influenzae ampicillin-resistant, and Group B Streptococci penicillin-resistant.
2. Results
Sensitivity Analysis
3. Discussion
3.1. Strengths
3.2. Limitations
3.3. Conclusions
3.4. Key Recommendations and Future Directions
4. Materials and Methods
4.1. Study Design
4.2. Patients
- All patients under 18 years of age.
- All cases of pneumonia due to bacteria from the Mycobacteriales and Spirochaetales orders.
- All patients with bacterial pneumonia and any other concurrent bacterial infectious disease.
- All cases coded with bacterial pneumonia attributed to more than one causative agent.
- All cases coded with a diagnosis of bacterial pneumonia in which the causative agent was not specified or not identified.
- Patients codified with diagnosis codes for very unusual bacterial pneumonias, e.g., pneumonia due to typhoidal salmonella, pneumonia due to non-typhoidal Salmonella pneumonia, pneumonic plague, glanders, and melioidosis.
4.3. Procedures
- Administrative variables: Year of the registry, center, and anonymized patient ID number.
- Sociodemographic variables: Date of birth, sex (male/female/not specified), and country of birth. Sex data are collected in RAE-CMBD as recorded in the patient’s medical history during admission according to the patient’s self-reported information.
- Clinical variables: Date of hospital admission, date of discharge, type of discharge (death/home/transfer to another hospital/voluntary discharge/transfer to social-health center), intensive care unit (ICU) admission (yes/no), length of ICU stay (in days), main diagnosis (ICD-10-CM), secondary diagnoses (ICD-10-CM), procedures 1 to 20 (ICD-10-CM), all patient-refined diagnosis-related groups (APR-DRG) severity level (null/minor/moderate/major/extreme), and APR-DRG mortality risk level (low/medium/high/extreme).
4.4. Outcomes
4.5. Statistical Analysis
4.6. Sensitivity Analysis
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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| Fiscal Year | Total Cases | AMR Cases | Prevalence (%) |
|---|---|---|---|
| 2017 | 17,561 | 1028 | 5.85 |
| 2018 | 21,462 | 1089 | 5.07 |
| 2019 | 22,930 | 1121 | 4.89 |
| 2020 | 19,098 | 935 | 4.90 |
| 2021 | 15,016 | 868 | 5.78 |
| 2022 | 20,834 | 976 | 4.68 |
| Variable | Bacterial Pneumonia Hospitalizations Without AMR Bacteria Code (n = 110,884) | Bacterial Pneumonia Hospitalizations With AMR Bacteria Code (n = 6017) | p-Value |
|---|---|---|---|
| Age (years), median (IQR) | 72 (59–83) | 75 (64–84) | <0.0001 a |
| Sex, n (%) | |||
| Men | 69,255 (62.46) | 4255 (70.72) | <0.0001 b |
| Women | 41,628 (37.54) | 1762 (29.28) | <0.0001 b |
| EVCI score, median (IQR) | 5 (0–12) | 8 (3–15) | <0.0001 a |
| Severity of illness APR-DRG, n (%) | |||
| Null | 84 (0.08) | 18 (0.13) | <0.0001 b |
| Minor | 11,160 (10.06) | 155 (2.58) | <0.0001 b |
| Moderate | 26,582 (23.97) | 808 (13.43) | <0.0001 b |
| Major | 46,086 (41.56) | 2415 (40.14) | <0.0001 b |
| Extreme | 26,972 (24.32) | 2631 (43.73) | <0.0001 b |
| Risk of mortality APR-DRG, n (%) | |||
| Null | 84 (0.08) | 8 (0.13) | <0.0001 b |
| Low | 18,830 (16.98) | 293 (4.87) | <0.0001 b |
| Medium | 27,043 (24.39) | 1258 (20.91) | <0.0001 b |
| High | 43,363 (39.11) | 2643 (43.93) | 0.2910 b |
| Extreme | 21,564 (19.45) | 1815 (30.16) | <0.0001 b |
| Viral pneumonia co-infection, n (%) | 10,547 (9.51) | 597 (9.92) | <0.0001 b |
| Fungal pneumonia co-infection, n (%) | 1456 (1.31) | 226 (3.76) | <0.0001 b |
| Sepsis, n (%) | 18,590 (16.77) | 1297 (21.56) | <0.0001 b |
| ICU admission, n (%) | 15,692 (14.15) | 1336 (22.20) | <0.0001 b |
| Mechanical ventilation, n (%) | 8785 (7.92) | 964 (16.02) | <0.0001 b |
| Ventilator-associated pneumonia, n (%) | 1108 (1.00) | 180 (2.99) | <0.0001 b |
| Extracorporeal membrane oxygenation, n (%) | 221 (0.20) | 24 (0.40) | <0.0010 b |
| Nosocomial condition | 3164 (2.85) | 628 (10.44) | <0.0001 b |
| Length of stay (days), median (IQR) | 8 (5–13) | 14 (8–24) | <0.0001 a |
| ICU length of stay (days), median (IQR) | 8 (3–17) | 13 (5–26) | <0.0001 a |
| In-hospital mortality, n (%) | 11,147 (10.05) | 1111 (18.46) | <0.0001 b |
| Microbial Etiology | Non-AMR Code, n (%) | AMR Code, n (%) | Total Bacterial Etiology, n (%) | Total AMR Bacterial, n (%) |
|---|---|---|---|---|
| Gram-positive cocci group | ||||
| Streptococcus pneumoniae | 69,697 (99.13) | 615 (0.87) | 70,312 (60.15) | 615 (10.22) |
| Streptococcus group B | 136 (94.44) | 8 (5.56) | 144 (0.12) | 8 (0.13) |
| Streptococcus, other | 1821 (97.59) | 45 (2.41) | 1866 (1.60) | 45 (0.75) |
| Staphylococcus aureus | 3509 (56.72) | 2678 (43.28) | 6187 (5.29) | 2,678 (44.52) |
| Staphylococcus, other | 794 (91.58) | 73 (8.42) | 867 (0.74) | 73 (1.21) |
| Staphylococcus, unspecified | 288 (92.60) | 23 (7.40) | 311 (0.27) | 23 (0.38) |
| Total Gram-positive cocci group | 76,245 (95.68) | 3442 (4.32) | 79,687 (68.17) | 3442 (57.20) |
| Gram-negative bacilli group | ||||
| Pseudomonas aeruginosa | 7438 (89.65) | 859 (10.35) | 8297 (7.10) | 859 (14.28) |
| Haemophilus influenzae | 5430 (96.36) | 205 (3.64) | 5635 (4,82) | 205 (3.41) |
| Klebsiella pneumoniae | 3321 (85.61) | 558 (14.39) | 3879 (3.32) | 558 (9.27) |
| Escherichia coli | 2560 (84.80) | 459 (15.20) | 3019 (2.58) | 459 (7.63) |
| Gram-negative aerobic bacteria, other | 4441 (91.62) | 406 (8.38) | 4847 (4.15) | 406 (6.75) |
| Bordetella pertussis/Bordetella parapertussis (Whooping cough) | 27 (93.10) | 2 (6.90) | 29 (0.02) | 2 (0.03) |
| Total Gram-negative bacilli group | 30,673 (92.42) | 2514 (7.58) | 33,187 (28.39) | 2514 (41.78) |
| Other bacteria group | ||||
| Legionella pneumophila | 7456 (99.67) | 25 (0.33) | 7481 (6.40) | 25 (0.42) |
| Actinomyces spp. (Pulmonary actinomycosis) | 264 (97.06) | 8 (2.94) | 272(0.23) | 8 (0.13) |
| Mycoplasma pneumoniae | 1444 (99.59) | 6 (0.41) | 1450 (1.24) | 6 (0.10) |
| Chlamydophila pneumoniae | 1095 (99.10) | 10 (0.90) | 1105 (0.95) | 10 (0.17) |
| Nocardia spp. (Pulmonary nocardiosis) | 635 (95.49) | 30 (4.51) | 665 (0.57) | 30 (0.50) |
| Coxiella burnetii (Q fever) | 461 (98.72) | 6 (1.28) | 467 (0.40) | 6 (0.10) |
| Brucella spp. (Brucellosis) | 33 (97.06) | 1 (2.94) | 34 (0.03) | 1 (0.02) |
| Neisseria gonorrhoeae (Gonococcal pneumonia) | 21 (100.00) | 0 (0.00) | 21 (0.02) | 0 (0.00) |
| Francisella tularensis (Pulmonary tularaemia) | 12 (100.00) | 0 (0.00) | 12 (0.01) | 0 (0.00) |
| Bacillus anthracis (Pulmonary anthrax) | 1 (100.00) | 0 (0.00) | 1 (0.00) | 0 (0.00) |
| Total other bacteria group | 3966 (98.49) | 61 (1.51) | 4027 (3.44) | 61 (1.01) |
| Total bacteria | 110,884 (100.00) | 6,017 (100.00) | 116,901 (100.00) | 6017 (100.00) |
| Adjusted OR | 95% CI, Lower Limit | 95% CI, Upper Limit | p > |z| | |
|---|---|---|---|---|
| Pneumonia due AMR GPC | 1.62 | 1.48 | 1.78 | <0.0001 |
| Pneumonia due to AMR GNB | 1.41 | 1.26 | 1.58 | <0.0001 |
| Pneumonia due to other AMR bacteria | 0.70 | 0.27 | 1.81 | =0.4650 |
| Age at admission quintile 2 a | 1.68 | 1.55 | 1.80 | <0.0001 |
| Age at admission quintile 3 a | 2.14 | 1.99 | 2.31 | <0.0001 |
| Age at admission quintile 4 a | 2.55 | 2.36 | 2.75 | <0.0001 |
| Age at admission quintile 5 a | 4.06 | 3.76 | 4.39 | <0.0001 |
| Female sex | 0.87 | 0.83 | 0.90 | <0.0001 |
| EVCI quintile 2 b | 1.22 | 1.13 | 1.33 | <0.0001 |
| EVCI quintile 3 b | 1.81 | 1.69 | 1.95 | <0.0001 |
| EVCI quintile 4 b | 2.57 | 2.39 | 2.76 | <0.0001 |
| EVCI quintile 5 b | 3.64 | 3.41 | 3.90 | <0.0001 |
| Fungal pneumonia co-infection | 2.85 | 2.53 | 3.21 | <0.0001 |
| Viral pneumonia co-infection | 1.91 | 1.80 | 2.03 | <0.0001 |
| Sepsis | 2.64 | 2.52 | 2.76 | <0.0001 |
| VAP | 2.22 | 1.95 | 2.54 | <0.0001 |
| ICU admission | 0.39 | 0.37 | 0.41 | <0.0001 |
| In-Hospital Mortality | Length of Hospital Stay | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Adj. IRR | Robust Std. Err | 95% CI, Lower Limit | 95% CI, Upper Limit | p > |z| | Adj. IRR | Robust Std. Err. | 95% CI, Lower Limit | 95% CI, Upper Limit | p > |z| | |
| AMR Bacterial | 1.34 | 0.0374 | 1.26 | 1.41 | <0.0001 | 1.46 | 0.0220 | 1.41 | 1.50 | <0.0001 |
| Pneumonia due GPC | 1.25 | 0.0777 | 1.11 | 1.42 | <0.0001 | 0.74 | 0.0106 | 0.72 | 0.76 | <0.0001 |
| Pneumonia due to GNB | 1.65 | 0.1034 | 1.46 | 1.86 | 0.0010 | 1.10 | 0.0179 | 1.06 | 1.13 | <0.0001 |
| Age at admission quintile 2 a | 1.49 | 0.0479 | 1.40 | 1.59 | <0.0001 | 1.00 | 0.0152 | 0.98 | 1.04 | =0.7220 |
| Age at admission quintile 3 a | 1.80 | 0.0577 | 1.70 | 1.93 | <0.0001 | 0.97 | 0.0147 | 0.94 | 1.00 | 0.0260 |
| Age at admission quintile 4 a | 2.13 | 0.0734 | 2.00 | 2.29 | <0.0001 | 0.90 | 0.0143 | 0.87 | 0.93 | <0.0001 |
| Age at admission quintile 5 a | 3.23 | 0.1192 | 3.00 | 3.47 | <0.0001 | 0.83 | 0.0129 | 0.80 | 0.85 | <0.0001 |
| Female sex | 0.91 | 0.0163 | 0.88 | 0.94 | <0.0001 | 0.97 | 0.0072 | 0.95 | 0.98 | <0.0001 |
| EVCI quintile 2 b | 1.20 | 0.0454 | 1.11 | 1.30 | <0.0001 | 1.11 | 0.0143 | 1.08 | 1.14 | <0.0001 |
| EVCI quintile 3 b | 1.70 | 0.0557 | 1.60 | 1.81 | <0.0001 | 1.22 | 0.0161 | 1.19 | 1.26 | <0.0001 |
| EVCI quintile 4 b | 2.26 | 0.0727 | 2.12 | 2.41 | <0.0001 | 1.34 | 0.0205 | 1.30 | 1.38 | <0.0001 |
| EVCI quintile 5 b | 2.92 | 0.0902 | 2.75 | 3.11 | <0.0001 | 1.43 | 0.0177 | 1.40 | 1.47 | <0.0001 |
| Fungal pneumonia co-infection | 1.83 | 0.0702 | 1.70 | 1.97 | <0.0001 | 1.52 | 0.0376 | 1.45 | 1.60 | <0.0001 |
| Viral pneumonia co-infection | 1.65 | 0.0378 | 1.57 | 1.72 | <0.0001 | 1.20 | 0.0131 | 1.18 | 1.23 | <0.0001 |
| Sepsis | 2.17 | 0.0494 | 2.07 | 2.27 | <0.0001 | 1.29 | 0.0162 | 1.26 | 1.32 | <0.0001 |
| VAP | 1.49 | 0.0649 | 1.36 | 1.62 | <0.0001 | 2.11 | 0.0558 | 2.00 | 2.22 | <0.0001 |
| ICU admission | 0.49 | 0.0228 | 0.45 | 0.53 | <0.0001 | 0.68 | 0.0135 | 0.66 | 0.70 | <0.0001 |
| Coefficient | Std. Err. | 95% CI, Lower Limit | 95% CI, Upper Limit | p > |z| | |
|---|---|---|---|---|---|
| In-hospital mortality | |||||
| ATET, % | 4.01 | 0.0051 | 3.02 | 5.00 | <0.0001 |
| ATE, % | 3.82 | 0.0048 | 2.87 | 4.77 | <0.0001 |
| Length of hospital stay | |||||
| ATET, days | 5.93 | 0.2975 | 5.34 | 6.51 | <0.0001 |
| ATE, days | 6.06 | 0.3155 | 5.44 | 6.68 | <0.0001 |
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Oterino-Moreira, I.; Pérez-Encinas, M.; Candel-González, F.J.; Lorenzo-Martínez, S. Impact of Antimicrobial-Resistant Bacterial Pneumonia on In-Hospital Mortality and Length of Hospital Stay: A Retrospective Cohort Study in Spain. Antibiotics 2025, 14, 1006. https://doi.org/10.3390/antibiotics14101006
Oterino-Moreira I, Pérez-Encinas M, Candel-González FJ, Lorenzo-Martínez S. Impact of Antimicrobial-Resistant Bacterial Pneumonia on In-Hospital Mortality and Length of Hospital Stay: A Retrospective Cohort Study in Spain. Antibiotics. 2025; 14(10):1006. https://doi.org/10.3390/antibiotics14101006
Chicago/Turabian StyleOterino-Moreira, Iván, Montserrat Pérez-Encinas, Francisco J. Candel-González, and Susana Lorenzo-Martínez. 2025. "Impact of Antimicrobial-Resistant Bacterial Pneumonia on In-Hospital Mortality and Length of Hospital Stay: A Retrospective Cohort Study in Spain" Antibiotics 14, no. 10: 1006. https://doi.org/10.3390/antibiotics14101006
APA StyleOterino-Moreira, I., Pérez-Encinas, M., Candel-González, F. J., & Lorenzo-Martínez, S. (2025). Impact of Antimicrobial-Resistant Bacterial Pneumonia on In-Hospital Mortality and Length of Hospital Stay: A Retrospective Cohort Study in Spain. Antibiotics, 14(10), 1006. https://doi.org/10.3390/antibiotics14101006

