Severity assessment in melioidosis pneumonia: validity of PSI, CURB-65, and SMART-COP scoring criteria

Introduction

Melioidosis caused by Burkholderia pseudomallei (an environmental gram-negative bacterium) is an endemic disease in tropical countries, especially in Southeast Asia and Northern Australia. The number of melioidosis patients has increased recently in Vietnam, predominantly in the rainy season (1). Its mortality rate is still high, varying from 9% to 70% based on previously published studies (2). A score for predicting mortality in acute melioidosis patients included features such as age, presence of pneumonia, lymphocyte count, serum bicarbonate, urea, creatinine, and serum bilirubin was proposed (3). Besides, thrombocytopenia occurred frequently in severe melioidosis patients and is associated with death outcome (4,5). Early identification severe melioidosis patients has significantly clinical impacts such as choosing appropriately caring unit (general ward or intensive care unit), prompt resuscitation support in the combination with aggressive antibiotic therapy. However, this issue was concerned inadequate in previous time because it was difficult to confirm a melioidosis case immediately at the admission (diagnosis of melioidosis was established on the basis of culture result which took 3–5 days to isolate B. pseudomallei). Along with the development of melioidosis rapid diagnostic tests in clinical practice, for instance the active melioidosis detection plus test (6), it results in the essential need of melioidosis prognosis.

Pulmonary melioidosis (symptom duration <2 months as acute/sub-acute and ≥2 months as chronic) is the most common clinical entity of melioidosis, accounting for ≥50% melioidosis cases (7,8). The evidence showed that acute/sub-acute pulmonary melioidosis had worse outcomes than chronic pulmonary melioidosis and melioidosis without pulmonary abnormality (9,10). In this article, we used the term “melioidosis pneumonia” with the meaning of acute/sub-acute pulmonary melioidosis, excluding chronic melioidosis. Melioidosis pneumonia (MP) could be considered as a special entity of pneumonia because of its distinguished progression and high mortality. Prognostic assessment for MP patients is an urgent requirement in clinical practice. In addition to the general mortality prognostic score for acute melioidosis, we believe that SMART-COP (acronym for systolic blood pressure, multilobar infiltrates, albumin, respiratory rate, tachycardia, confusion, oxygen and pH), pneumonia severity index (PSI), and CURB-65 (acronym for confusion, urea, respiratory rate, blood pressure and age ≥65 years) scores, and American Thoracic Society (ATS)/Infectious Diseases Society of America (IDSA) 2007 criteria for severe pneumonia could be useful in severity assessment of MP patients (11,12). Nevertheless, the evidence relating to the validity of these tools have still been lacking and an answer for the question “what is the most appropriate score or factor?” is very necessary. Therefore, we conducted this study to evaluate the validity of relating factors and the mentioned scores in predicting the need for intensive respiratory or vasopressor support (IRVS) and the death outcome among MP patients. We present this article in accordance with the STROBE reporting checklist (available at https://amj.amegroups.com/article/view/10.21037/amj-24-33/rc).

Methods

A prospective cross-sectional study was conducted from October 2019 to February 2022 at the Respiratory Department, Cho Ray’s Hospital, Ho Chi Minh, Vietnam (the largest central hospital in Southern Vietnam). MP case was determined on the basis of the following criteria (12,13):

• The patient had clinical symptoms associated with pneumonia (fever, productive cough, pleuritic chest pain, dyspnea, hemoptysis);
• Radiographic findings were consistent with pneumonia;
• B. pseudomallei was isolated from any biomedical specimens (sputum, blood, lesion fluid, pleural fluid, bronchial lavage fluid, joint fluid, cerebrospinal fluid, etc.).

All adult MP patients (age ≥18 years) hospitalized with a medical history ≤2 months were enrolled conveniently and consecutively. With estimated area under receiver operating characteristic (ROC) curve (AUC) 0.8, proportion of sample having IRVS need or death outcome 0.33, width of confidence interval 0.25, and confidence level 0.95, we calculated the sample size at least 64 cases (14). We excluded cases with isolated multiple pathogens (B. pseudomallei and another bacterial pathogen, even Mycobacterium tuberculosis), human immunodeficiency virus infection, and pregnancy. Severe cases with undetermined outcome after discharging 48 hours were also excluded.

All pneumonia cases were treated according to the ATS/IDSA guidelines 2019 (15), especially the empiric antimicrobial therapy depending on individual characteristics of each case. The inappropriate initiation of antibiotics was defined when antimicrobial therapy did not include all following intravenous antibiotics: meropenem, imipenem, ceftazidime, and amoxicillin/clavulanic acid.

Findings on chest X-ray (CXR) were evaluated independently by the radiologist and the pulmonologist with more than five years of experience and they made the agreement in the final conclusion. The culture and isolation process of B. pseudomallei was suggested in the article of Nguyen-Ho Lam et al. (16). We collected all of the following features: demographic characteristics, co-morbidities, vital signs at admission, and the results of blood tests (cell blood count, glucose level, kidney function, and electrolytes) to calculate the score for PSI, CURB-65, SMART-COP, pneumonia severity according to ATS/IDSA criteria (17), and score for predicting mortality in acute melioidosis. Clinical signs and the results of laboratory tests at admission were used to calculate these scores, with the exception of the level of serum bilirubin, arterial blood gas, and serum albumin which could be implemented after isolating B. pseudomallei. Hypoxemia was defined as arterial partial pressure of oxygen (PaO₂) <60 mmHg or peripheral capillary oxygen saturation (SpO₂) ≤90%, likewise lymphopenia (<0.8 K/mm³), thrombocytopenia (<150 K/mm³), and hyponatremia (<135 mmol/L). Two researchers calculated them separately and made the agreement in the final score. SMART-COP score was assigned based on features such as age, multi-lobar involvement on CXR, serum albumin level, respiratory rate, tachycardia, confusion, respiratory failure, and blood pH to stratify risk groups of IRVS (0–2: low; 3–4: moderate; 5–6: high; ≥7: very high). It was calculated via the website https://www.mdcalc.com/calc/3914/smart-cop-score-pneumonia-severity. PSI score included features such as age, co-morbid disease, abnormal physical findings, and abnormal laboratory results to stratify risk groups (≤90: low risk; 91–130: moderate risk; >130: high risk). It was calculated via the website https://www.mdcalc.com/calc/33/psi-port-score-pneumonia-severity-index-cap. CURB-65 score included features such as confusion, blood urea nitrogen, respiratory rate, blood pressure, and age to stratify risk groups of mortality (0–1: low risk; 2: moderate risk; 3–5: high risk). It was calculated via the website https://www.mdcalc.com/calc/324/curb-65-score-pneumonia-severity. The score for predicting melioidosis mortality was calculated with the reference of Allen C. Cheng et al. (3).

Statistical analysis

Two important outcomes to analyze the validity of these scores included (I) the IRVS need defined as having invasive or noninvasive mechanical ventilation or using vasopressors for blood pressure support (11) and (II) the outcome at discharged time (improvement or death). All severe cases whose family required discharge before death were followed more at most 48 hours via phone call to confirm the final outcome. The AUC was used to determine the validity of these scores in predicting these outcomes and the Youden index was applied to determine optimal cut-off values of pneumonia scoring systems. Interpretation of AUC values was suggested as follows: AUC ≥0.9: excellent; 0.9> AUC ≥0.8: considerable; 0.8> AUC ≥0.7: fair; 0.7> AUC ≥0.6: poor; and 0.6> AUC ≥0.5: fail (18). Previous study showed that primary MP patients had more severity of disease than secondary MP patients with extra-pulmonary presentations (developing septic shock or die) (9). We divided into two MP groups with and without extra-pulmonary lesion (liver abscess, spleen abscess, adrenal abscess, parotid abscess, soft tissue or joint infections). Kolmogorov-Smirnov test was used to determine the normal distribution of continuous variables. The Chi-squared test or Fisher’s test was used to compare qualitative variables between two groups. The Student’s t-test was used to compare the mean values between two groups. A two-sided P value <0.05 was considered statistically significant. IBM software was used to enter and analyze the data.

Ethical considerations

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics committee of University of Medicine and Pharmacy at Ho Chi Minh City (No. 547/HĐĐĐ-ĐHYD) and informed consent was taken from all individual participants.

Results

Demographic and clinical characteristics and the results of laboratory tests

We enrolled 66 hospitalized MP cases (only one case was excluded because of the result of culture isolating both B. pseudomallei and Acinetobacter baumannii, Figure 1) with mean age of 51±11 years, and male gender accounted 86.4% (57/66). The majority (56.06%) were freelance workers and 16.67% were farmers. Subjects in our study have been living widespread southern provinces, Vietnam, especially in Ho Chi Minh City 9 cases (13.63%), Binh Thuan province 9 cases (13.63%), Binh Phuoc province 5 cases (7.58%), Tay Ninh province 5 cases (7.58%), Dong Nai province 4 cases (6.06%), Long An province 4 cases (6.06%), and Kien Giang province 4 cases (6.06%). Clinical manifestation of acute pulmonary melioidosis (symptom duration <1 month) was recorded in 89.39% cases. Patients who had extra-pulmonary lesion accounted for 43.94%. Clinical features and the results of laboratory tests of 66 subjects are presented in Table 1. Lymphopenia, thrombocytopenia, and hyponatremia were documented in 53.84%, 30.30%, and 84.85%, respectively.

Figure 1 A flow chart to present the process of enrollment.

Pneumonia scores, score for predicting mortality in acute melioidosis patient, and the outcomes

Based on the ATS/IDSA 2007 criteria, we had 33.33% of melioidosis cases with severe pneumonia. Medium scores and interquartile range (IQR) for CURB-65, SMART-COP, and PSI were 1 (0–2), 3.0 (1.0–4.25), and 91.50 (73.75–116.50), respectively. Medium score and IQR for the score predicting mortality was 4 [3–6]. There was no significant difference when comparing the calculated scores (including CURB-65, SMART-COP, PSI, and score for predicting mortality) between two MP groups with extra-pulmonary lesion and those without (all P values >0.05). The rate for the IRVS need was 34.8% and the mortality at discharged was 25.8% in our study. The numbers of total patients, patients requiring IRVS, and death patients for each level of pneumonia severity according to the respective scores are showed in Figure 2. There was also no significant difference between the two MP groups with and without extra-pulmonary lesion for the IRVS need (P=0.11) and the mortality (P=0.16).

Figure 2 Numbers of patients requiring intensive respiratory or vasopressor support and death patients for each level of pneumonia severity. CURB-65 score (0–1: low risk; 2: moderate risk; 3–5: high risk). PSI score (risk class I, II, III: low risk; risk class IV: moderate risk; risk class V: high risk). SMART-COP score (0–2: low; 3–4: moderate; 5–6: high; ≥7: very high). Score for predicting melioidosis mortality (≤3: low risk; ≥4: high risk). IRVS, intensive respiratory or vasopressor support; PSI, pneumonia severity index; CURB-65, acronym for confusion, urea, respiratory rate, blood pressure and age ≥65 years; SMART-COP, acronym for systolic blood pressure, multilobar infiltrates, albumin, respiratory rate, tachycardia, confusion, oxygen and pH.

Scores and factors associated with the outcomes of MP patients

CURB-65, SMART-COP, and PSI showed the validity in predicting the IRVS need and the mortality at the discharged time among MP patients. The AUCs of PSI, CURB-65, and SMART-COP in predicting the IRVS need were 0.813 [95% confidence interval (CI): 0.684–0.943, P<0.001], 0.868 (95% CI: 0.767–0.969, P<0.001), and 0.910 (95% CI: 0.825–0.994, P<0.001), respectively. The AUCs of PSI, CURB-65, SMART COP, and the mortality score of acute melioidosis in predicting the death outcome were 0.698 (95% CI: 0.536–0.857, P=0.02), 0.797 (95% CI: 0.665–0.928, P<0.001), 0.797 (95% CI: 0.673–0.920, P<0.001), and 0.663 (95% CI: 0.524–0.801, P=0.05), respectively. Figure 3 describes the ROC curves for PSI, CURB-65, SMART-COP, and mortality score. Sensitivity, specificity, positive predictive value, negative predictive value, and positive likelihood ratio for scoring systems and ATS/IDSA 2007 criteria are presented in Table 2.

Figure 3 ROC curve for prediction of IRVS and mortality using CURB-65 and SMART-COP in patients with melioidosis pneumonia. IRVS, intensive respiratory or vasopressor support; PSI, pneumonia severity index; CURB-65, acronym for confusion, urea, respiratory rate, blood pressure and age ≥65 years; SMART-COP, acronym for systolic blood pressure, multilobar infiltrates, albumin, respiratory rate, tachycardia, confusion, oxygen and pH; AUC, area under receiver operating characteristic curve; CI, confidence interval; ROC, receiver operating characteristic.

Neutrophil-to-lymphocyte ratio (NLR, defined as the neutrophil count divided by lymphocyte count), the lymphocyte count, and the appropriate initiation of antibiotics for B. pseudomallei during the first 48 hours after admission showed no difference between groups with or without the outcomes (the IRVS need or the death outcome). However, the platelets count was different significantly to the IRVS need (P=0.01) but not to the death outcome (P=0.09). Hypoxemia at admission was also different with the IRVS need (47.50% vs. 15.38%, P=0.007) and the death outcome (35.0% vs. 11.54%, P=0.03). Hyponatremia was common in MP patients (84.85%) but those with the IRVS need or the death outcome had the higher level of serum sodium (132.87±7.01 vs. 127.33±3.93 mmol/L, P<0.001 and 133.18±7.09 vs. 127.90±4.64 mmol/L, P=0.001, respectively).

Discussion

MP in our study developed more commonly in patients aged 40 to 60, predominantly in male patients with underlying diabetes mellitus. Fever is the most common symptom and MP patients often had hypoxic respiratory failure. Radiological abnormalities occurred frequently in the upper lobe and diffuse (affecting more than two lobes or both lung fields) with findings such as nodules, mass, infiltration, cavity, and pleural effusion. These features were similar to those of MP studies from Thailand (10), Cambodia (13), Malaysia (19), Taiwan (20), India (21), and Australia (9). Primary MP caused abnormality in the upper lobe more frequently than secondary pneumonia in the melioidosis study in Australia. Our study divided into two groups with and without extra-pulmonary lesion and showed no difference. A small sample size can be a reason for this result.

B. pseudomallei is one of the pathogens causing severe community-acquired pneumonia (CAP), especially in endemic regions (7,12). Our study documented 33.33% of severe pneumonia consistent with the ATS/IDSA 2007 criteria. Through evaluating pneumonia scores, 21.21% with CURB-65 score ≥3, 24.24% with SMART-COP score ≥5, and 51.51% with PSI class IV and V were recorded. The study of Reechaipichitkul in Thailand also showed the rate of severe MP 43.37% according to the ATS/IDSA 2007 criteria (10). The mortality in the published MP studies ranged from 20.0% to 66.7% (9,10,13,20,21). This is similar to our study (25.8%) and independent of the appropriate antibiotic initiation during the first 48 hours after admission. All aforementioned features emphasized that MP is a severe condition which requires personalized therapy comprehensively rather than only with the early appropriate antibiotics. In detail, timely interventional measures during first 24 hours admission including hemodynamic support, respiratory support, corticosteroid, and multidiscipline cooperation (respiratory department, emergency department, and intensive care unit) in combination with appropriate antibiotic treatment help to reduce mortality (22), which need to be applied for severe MP.

There are many previous studies to compare pneumonia scores but no study on MP subjects was carried out. Our study showed that CURB-65, SMART-COP, and PSI had the validity in predicting the IRVS need and the discharged death outcome among MP patients. Although the score for predicting mortality was established separately for melioidosis patients but had less validity than pneumonia scores in our study. Moreover, another study conducted in Australia showed that SMART-COP was a simple useful tool to determine CAP patients requiring IRVS (11). Our study also showed that it was more useful in predicting the IRVS need and the mortality. Australia is an endemic country for melioidosis condition (12), this can be potential reason for the same conclusion.

CURB-65 score is simple and advantageous in evaluating CAP patients in clinical practice. Our study proved its validity in MP patients. It showed non-inferior to SMART-COP and ATS/IDSA criteria in predicting the IRVS need and mortality. Comparison to CAP recommendations (23), our study found out that MP patients with this score ≥2 should be treated as a severe condition. On the other hand, recent evidence revealed adding the hypoxia status at admission to improve the validity of CURB-65 in evaluating mild CAP patients (24). Therefore, from our result it should be considered in combination with CURB-65 for predicting the outcomes of MP.

The results of previously published studies showed that platelets count, lymphocyte count, and NLR had associated with the outcomes of melioidosis patients (5,25,26). Thrombocytopenia is associated with a decreasing immune response against B. pseudomallei that results in a more severe condition (4) and melioidosis patients with lymphopenia have a higher mortality (26). However, these factors showed no difference to the outcome aspect of MP patients in our study. MP is a severe clinical entity with higher rates of bacteremia, septic shock, and death in the study of Meumann et al. (9). This can be a plausible reason for no significant difference when analyzing in only the severe group. The same reason explained for less usefulness of the mortality score for acute melioidosis in our study.

Hyponatremia is common in patients with infection status, accounted for 84.85% of patients in our study. It has an impact on mortality and the long-term hospital stay among infectious patients, including melioidosis patients (27). Our study showed that a higher level of serum sodium at admission (level of serum sodium ≤145 mmol/L) was recorded in the group with the IRVS need and the death outcome. The study of Rao et al. concluded that the severe hyponatremia (<120 mmol/L) associated with the death outcome, intensive care unit admission, and mechanical ventilation (27). This discrepancy could be related to differences in the study populations (general melioidosis vs. MP) and the time point evaluating the level of serum sodium.

Our study had several limitations. (I) The sample size was small. (II) This study only focused on hospitalized MP patients which can cause bias in evaluating comprehensively all levels of severity. Nonetheless, this study was conducted at the largest central hospital in Southern Vietnam where many MP patients were transferred from provincial hospitals (86.36% of patients not living in Ho Chi Minh City) because of non-responsive treatment or failure in diagnosing the nature of lung mass. Moreover, 39.39% with non-hypoxia pneumonia was documented in our study. We believed that this study could evaluate all levels of severity, proved by presented data in Figure 2. (III) This study only focused on the death outcome at discharged but not the 30-day mortality. The treatment duration for MP is different from common CAP, the intensive stage sometimes requires 6 weeks and the eradicating stage able to prolong to 6 months. MP should be considered as a special entity of CAP. (IV) Our study was conducted at a single Centre with a small sample size which could limit generalizability of our results.

Conclusions

MP could present as mild to severe clinical scenario with high mortality among severe MP cases. The exact assessment of pneumonia severity at admission is essential to combine timely therapeutic measures (hemodynamic support, respiratory support, corticosteroid, multidiscipline collaboration) along with early appropriate initiation of antibiotics to reduce the mortality. The CURB-65 score could be simple to use in clinical practice and useful in predicting the IRVS need and the death outcome among MP patients when score ≥2.

Acknowledgments

We thank all colleagues at the Respiratory Department, Cho Ray Hospital for taking care of patients with melioidosis pneumonia. We also thank Dr. Nguyen Dinh Loc who assisted to edit the English of this manuscript.

Funding: None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://amj.amegroups.com/article/view/10.21037/amj-24-33/rc

Data Sharing Statement: Available at https://amj.amegroups.com/article/view/10.21037/amj-24-33/dss

Peer Review File: Available at https://amj.amegroups.com/article/view/10.21037/amj-24-33/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://amj.amegroups.com/article/view/10.21037/amj-24-33/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics committee of University of Medicine and Pharmacy at Ho Chi Minh City (No. 547/HĐĐĐ-ĐHYD) and informed consent was taken from all individual participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. Trinh TT, Nguyen LDN, Nguyen TV, et al. Melioidosis in Vietnam: Recently Improved Recognition but still an Uncertain Disease Burden after Almost a Century of Reporting. Trop Med Infect Dis 2018;3:39. [Crossref] [PubMed]
2. Gassiep I, Armstrong M, Norton R. Human Melioidosis. Clin Microbiol Rev 2020;33:e00006-19. [Crossref] [PubMed]
3. Cheng AC, Jacups SP, Anstey NM, et al. A proposed scoring system for predicting mortality in melioidosis. Trans R Soc Trop Med Hyg 2003;97:577-81. [Crossref] [PubMed]
4. Birnie E, Claushuis TAM, Koh GCKW, et al. Thrombocytopenia Impairs Host Defense Against Burkholderia pseudomallei (Melioidosis). J Infect Dis 2019;219:648-59. [Crossref] [PubMed]
5. Kirby P, Smith S, Ward L, et al. Clinical Utility of Platelet Count as a Prognostic Marker for Melioidosis. Am J Trop Med Hyg 2019;100:1085-7. [Crossref] [PubMed]
6. Currie BJ, Woerle C, Mayo M, et al. What is the Role of Lateral Flow Immunoassay for the Diagnosis of Melioidosis? Open Forum Infect Dis 2022;9:ofac149. [Crossref] [PubMed]
7. Mukhopadhyay A, Lee KH, Tambyah PA. Bacteraemic melioidosis pneumonia: impact on outcome, clinical and radiological features. J Infect 2004;48:334-8. [Crossref] [PubMed]
8. Virk HS, Mukhopadhyay C, Wiersinga WJ. Melioidosis: A Neglected Cause of Community-Acquired Pneumonia. Semin Respir Crit Care Med 2020;41:496-508. [Crossref] [PubMed]
9. Meumann EM, Cheng AC, Ward L, et al. Clinical features and epidemiology of melioidosis pneumonia: results from a 21-year study and review of the literature. Clin Infect Dis 2012;54:362-9. [Crossref] [PubMed]
10. Reechaipichitkul W. Clinical manifestation of pulmonary melioidosis in adults. Southeast Asian J Trop Med Public Health 2004;35:664-9. [PubMed]
11. Charles PG, Wolfe R, Whitby M, et al. SMART-COP: a tool for predicting the need for intensive respiratory or vasopressor support in community-acquired pneumonia. Clin Infect Dis 2008;47:375-84. [Crossref] [PubMed]
12. Douglas MW, Lum G, Roy J, et al. Epidemiology of community-acquired and nosocomial bloodstream infections in tropical Australia: a 12-month prospective study. Trop Med Int Health 2004;9:795-804. [Crossref] [PubMed]
13. Rammaert B, Beauté J, Borand L, et al. Pulmonary melioidosis in Cambodia: a prospective study. BMC Infect Dis 2011;11:126. [Crossref] [PubMed]
14. Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 1982;143:29-36. [Crossref] [PubMed]
15. Metlay JP, Waterer GW, Long AC, et al. Diagnosis and Treatment of Adults with Community-acquired Pneumonia. An Official Clinical Practice Guideline of the American Thoracic Society and Infectious Diseases Society of America. Am J Respir Crit Care Med 2019;200:e45-e67. [Crossref] [PubMed]
16. Lam NH, Huyen DT, Hoa L, et al. Cavitary lung disease in hospitalized patients: Differences between melioidosis and tuberculosis. Trop Doct 2022;52:427-30. [Crossref] [PubMed]
17. Mandell LA, Wunderink RG, Anzueto A, et al. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis 2007;44:S27-S72. [Crossref] [PubMed]
18. Çorbacıoğlu ŞK, Aksel G. Receiver operating characteristic curve analysis in diagnostic accuracy studies: A guide to interpreting the area under the curve value. Turk J Emerg Med 2023;23:195-8. [Crossref] [PubMed]
19. Yazid MB, Fauzi MH, Hasan H, et al. An 11-Year Analysis of Emergency Presentations of Melioidosis in Northeastern Malaysia. J Immigr Minor Health 2017;19:774-7. [Crossref] [PubMed]
20. Kung CT, Li CJ, Hung SC, et al. Acute melioid community-acquired pneumonia. Int J Infect Dis 2011;15:e627-e630. [Crossref] [PubMed]
21. Patra S, Shaw T, Eshwara VK, et al. Pulmonary melioidosis: an experience over years from a tertiary care hospital from southwest India. Indian J Med Sci 2017;69:21-6.
22. Phua J, Dean NC, Guo Q, et al. Severe community-acquired pneumonia: timely management measures in the first 24 hours. Crit Care 2016;20:237. [Crossref] [PubMed]
23. Lim WS, van der Eerden MM, Laing R, et al. Defining community acquired pneumonia severity on presentation to hospital: an international derivation and validation study. Thorax 2003;58:377-82. [Crossref] [PubMed]
24. Sanz F, Restrepo MI, Fernández E, et al. Hypoxemia adds to the CURB-65 pneumonia severity score in hospitalized patients with mild pneumonia. Respir Care 2011;56:612-8. [Crossref] [PubMed]
25. Dao-Thi NH, Nguyen-Tiet A, Nguyen-Ho L. Melioidosis Presenting Predominantly as Thoracic Empyema. J Glob Infect Dis 2022;14:87-9. [Crossref] [PubMed]
26. Gassiep I, Ganeshalingam V, Chatfield MD, et al. Melioidosis: Laboratory Investigations and Association with Patient Outcomes. Am J Trop Med Hyg 2021;106:54-9. [Crossref] [PubMed]
27. Rao IR, Shaw T, Prabhu RA, et al. Hyponatremia in Melioidosis: Analysis of 10-year Data from a Hospital-Based Registry. J Glob Infect Dis 2022;14:64-8. [Crossref] [PubMed]