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Comparison of bacteraemic & non-bacteraemic brucellosis: A retrospective analysis of 2 years
For correspondence: Dr Enes Erbağci, Department of İnfectious Diseases and Clinical Microbiology, Nizip State Hospital, Gaziantep 27000, Turkey e-mail: enes_erbagci@hotmail.com
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Received: ,
Accepted: ,
Abstract
Background & objectives
Brucellosis is a zoonotic infectious disease that affects both humans and animals, with diagnosis traditionally confirmed by bacteriological culture of blood or tissue samples. This study aimed to identify clinical, epidemiological, and laboratory parameters that predict culture positivity in brucellosis cases.
Methods
We conducted a retrospective, single-centre study including 130 patients with brucellosis diagnosed between January 2023 and December 2024. Patients were classified as bacteraemic (n=60) and non-bacteraemic (n=70). Demographic characteristics, clinical features, laboratory parameters, and treatment outcomes were compared between the two groups.
Results
Patients with bacteraemia had higher rates of summer admissions, more frequent exposure to animal husbandry, and shorter symptom duration. Clinical manifestations such as back pain, headache, weight loss, and abdominal pain were more common in them. Laboratory findings showed lower leukocyte and, neutrophil counts, lower haemoglobin, lower platelet counts, in bacteraemic patients. Erythrocyte sedimentation rate, C-reactive protein, alanine aminotransferase, and aspartate aminotransferase levels were significantly higher in bacteraemic vs non-bacteraemic patients. Receiver operating characteristic analysis indicated that AST had the highest diagnostic accuracy (AUC: 0.841, 95% CI: 0.758–0.924), with an optimal cut-off of 27.3 U/L, yielding 67.2 per cent sensitivity and 84.1 per cent specificity. Binary logistic regression analysis demonstrated that exposure history (OR=5.5), residence in a high-incidence geographic location (OR=10.0), and clinical features such as back pain (OR = 9.4), together with low haemoglobin and elevated AST levels, were independent predictors of blood culture positivity in brucellosis.
Interpretation & conclusions
It may be possible to predict bacteraemia in brucellosis by using a combination of epidemiology, clinical, and laboratory criteria.
Keywords
Bacteraemia
blood culture
brucellosis
markers
risk factors
Brucellosis is a zoonotic infectious disease that affects both animals and humans1. The most common presenting symptoms in man include fever, fatigue, weight loss, night sweats, and musculoskeletal pain2. The gold standard for diagnosis is isolation of the pathogen by culture from blood or other relevant clinical specimens. Additional diagnostic methods include serological tests and polymerase chain reaction (PCR)3. Because Brucella spp. are intracellular pathogens, treatment requires prolonged combination antibiotic therapy4.
Several studies have reported that the treatment of bacteraemia cases is more challenging5-7. Therefore, detecting culture positivity in brucellosis cases is of particular importance. One study in children reported that patients with bacteraemia were younger and had a higher incidence of fever, arthralgia, hepatomegaly, and splenomegaly, as well as elevated C-reactive protein (CRP), aspartate aminotransferase (AST), and alanine aminotransferase (ALT) levels8. Another study found that fever was more common in bacteraemia cases, and that CRP, AST, and ALT levels were significantly higher9. Another study reported that bacteraemia patients were younger and more frequently presented with fever, weight loss, sweating, nausea, and vomiting, in addition to having higher erythrocyte sedimentation rate (ESR), AST, ALT, lactate dehydrogenase (LDH), and ferritin levels10. A previous study from our centre reported the overall epidemiological, clinical, and laboratory characteristics of patients with brucellosis in a comprehensive cohort11. However, that study did not focus on the specific comparison between bacteraemia and nonbacteraemic cases.
We conducted this study to identify the epidemiological, clinical, and laboratory parameters that may predict bacteraemia by comparing bacteraemic and non-bacteraemic brucellosis. Treatment outcomes were also evaluated.
Materials & Methods
This single-centre retrospective study evaluated patients admitted to the department of Infectious Diseases and Clinical Microbiology Clinic of Agri Training and Research Hospital between January 1, 2023 and December 31, 2024. This study was conducted in accordance with the principles of the Declaration of Helsinki and was approved by the Agri İbrahim Çeçen University Clinical Research Ethics Committee.
Patient selection and parameters examined
A total of 130 patients aged ≥18 yr with acute or subacute brucellosis were included. Eligibility criteria required that blood cultures be obtained prior to treatment initiation and that there was no history of previous brucellosis therapy. Patients were excluded if they were pregnant or breastfeeding, or if they had chronic renal failure, malignancy, cirrhosis, autoimmune disease, were receiving immunosuppressive therapy, or had chronic or recurrent brucellosis.
Demographic and clinical data were obtained retrospectively from the hospital’s electronic record system. These included age, sex, place of residence, exposure history (consumption of raw milk and dairy products, animal husbandry, etc.), admission date, duration of symptoms (days), presenting symptoms, clinical classification (acute or subacute), blood culture results, serological tests (standard tube agglutination or Coombs gel test), laboratory parameters (haemogram, ESR, CRP, transaminases, glucose, urea, creatinine), complications and organ involvement, treatment regimens, and treatment outcomes. Patients were categorised into two groups: blood culture–positive (bacteraemic) and blood culture–negative (non-bacteraemic).
Clinical definitions
Suspected exposures for brucellosis included direct contact with conjunctival mucosa, damaged skin, tissues, or secretions of animals potentially infected with Brucella species; consumption of raw or unpasteurised milk and dairy products; and inhalation of infectious aerosols. Patients presenting with symptoms such as fever, malaise, anorexia, weight loss, headache, night sweats, and musculoskeletal pain were considered clinically suspicious for brucellosis.
Patients who met the diagnostic criteria for brucellosis and had symptoms for ≤8 wk were classified as acute, those with symptoms for 8–52 wk as subacute, and those with symptoms for >52 wk as chronic brucellosis12.
Focal brucellosis was defined as involvement of anatomical regions other than the haematological system. Haematological abnormalities were defined as leukopenia (leukocytes <3,800/µL), leucocytosis (leukocytes >10,400/µL), thrombocytopenia (platelets <150 × 103/µL), and anaemia (haemoglobin <11.9 g/dL for women and <13.6 g/dL for men)13. Focal involvements included osteoarticular (sacroiliitis, spondylodiscitis, peripheral arthritis), genitourinary (epididymoorchitis), organomegaly (hepatomegaly, splenomegaly), and dermatologic manifestations (erythema nodosum). The following criteria were used to define organ involvement: sacroiliitis was diagnosed in the presence of hip pain with supportive findings on radiography or magnetic resonance imaging (MRI); spondylodiscitis in patients with low back pain and compatible findings on spinal MRI; peripheral arthritis in the presence of inflammatory joint findings confirmed by radiography; epididymoorchitis based on scrotal Doppler ultrasonography; hepatosplenomegaly by abdominal ultrasonography; and skin involvement after exclusion of other possible pathologies14.
Treatment outcomes were categorised as recovery, prolonged convalescence, or relapse. Patients who showed symptomatic improvement at the end of the recommended treatment period were considered recovered. Those with decreased antibody titres but persistent symptoms without objective findings such as fever were classified as having prolonged convalescence. Relapse was defined as recurrence of symptoms within six months after previous treatment, accompanied by either positive blood cultures or a fourfold increase in the most recent serological titre. A decrease or negativity in serological titres at the end of treatment was considered a serological response. The recommended treatment duration for brucellosis was 6–8 wk for patients without organ involvement and at least 12 wk for those with organ involvement15. The standard treatment regimens for brucellosis recommended by the World Health Organization (WHO) were followed16. In our study, treatment regimens were categorised as either standard or modified, with the latter referring to regimens that were changed or extended due to side effects or treatment failure during the treatment period.
Microbiological definitions
Patients with a history of exposure and clinically suspected brucellosis were screened using the Rose Bengal test (THSK antigen, Turkey). Blood cultures were obtained from patients who tested positive on the Rose Bengal test in combination with either the standard tube agglutination test (THSK antigen, Turkey) or the Brucella Coombs gel test (BCGT, ODAK, Turkey). Brucellosis was defined as a serological titre of ≥1:160 or a fourfold increase in titre at 2-week intervals15.
Blood cultures were collected in two sets (four bottles), comprising two aerobic and two anaerobic bottles. Cultures were incubated in the Render automatic blood culture system (BC256 Blood Culture Systems, China) and identified to the species level as Brucella spp. or B. melitensis using the VITEK-2® Compact system (bioMérieux, France).
Statistical analysis
Descriptive statistics were expressed as mean±standard deviation (SD) or median for continuous variables, and as number (n) and percentage (%) for categorical variables. The normality of continuous variables was assessed using the Shapiro-Wilk test. Comparisons between independent groups were performed using the independent samples t-test for normally distributed variables and the Mann-Whitney U test for non-normally distributed variables. Categorical variables were compared using the chi-square test. For paired comparisons before and after treatment, the dependent samples t-test was used for normally distributed variables, and the Wilcoxon signed-rank test for non-normally distributed variables. Receiver operating characteristic (ROC) analysis was conducted to evaluate the predictive value of quantitative parameters against the gold standard of blood culture positivity, and sensitivity and specificity were calculated. Predictors of culture positivity were identified using binary logistic regression analysis. All statistical analyses were performed using SPSS version 26 (IBM Corp., Armonk, NY, USA), and a P value <0.05 was considered statistically significant.
Results
Demographic, clinical and laboratory findings
A total of 130 cases were included in the study, of which 60 (46.2%) were classified as bacteraemic and 70 (53.8%) as non-bacteraemic. Demographic characteristics of the cases are summarised in table I. In the Diyadin district, 34 of 37 cases (91.9%) were involved in animal husbandry, compared to 32 of 44 cases (72.7%) in the city centre. Animal husbandry was significantly more prevalent in the Diyadin district than in the city centre (P=0.027). Clinical and laboratory findings are presented in table II.
| All cases (n=130) | Bacteraemic (n=60) | Non-bacteraemic (n=70) | P value | |
|---|---|---|---|---|
| Age (µ±SD) in yr | 41.5±13.6 | 40.9±14.7 | 42.0±12.6 | 0.630 |
| Gender, n (%) | ||||
|
Female Male |
70 (53.8) 60 (46.2) |
31 (51.7) 29 (48.3) |
39 (55.7) 31 (44.3) |
0.644 |
| Clinical classification, n (%) | ||||
|
Acute Subacute |
111 (85.3) 19 (14.7) |
55 (91.7) 5 (8.3) |
56 (80) 14 (20) |
0.060 |
| Seasonal distribution, n (%) | ||||
|
Winter Spring Summer Autumn |
35 (26.8) 21 (16.2) 27 (20.8) 47 (36.2) |
5 (8.3) 10 (16.7) 18 (30) 27 (45) |
30 (42.8) 11 (15.7) 9 (12.9) 20 (28.6) |
<0.001 |
| Place of residence, n (%) | ||||
|
Centrum Patnos Diyadin Doğubayazıt Hamur Eleşkirt Taşlıçay Tutak Others |
44 (33.8) 9 (6.9) 37 (28.5) 7 (5.4) 4 (3.1) 10 (7.7) 13 (10) 3 (2.3) 3 (2.3) |
13 (21.7) 7 (11.7) 24 (40) 5 (8.3) 2 (3.3) 3 (5) 2 (3.3) 1 (1.7) 3 (5) |
31 (44.2) 2 (2.9) 13 (18.5) 2 (2.9) 2 (2.9) 7 (10) 11 (15.7) 2 (2.9) 0 (0) |
0.001 |
| Animal husbandry, n (%) | 105 (80.8) | 53 (88.3) | 52 (74.3) | 0.043 |
| Exposure history, n (%) | 112 (86.2) | 56 (93.3) | 56 (80) | 0.028 |
N, number; SD, standard deviation; µ, mean
| All cases (n=130) | Bacteraemia (n=60) | Non-bacteraemia (n=70) | P value | |
|---|---|---|---|---|
| Duration of complaints (median; day) | 18 | 16 | 20.5 | 0.002 |
| Symptoms (n, %) | ||||
| Muscle and joint pain | 120 (92.3) | 55 (91.7) | 65 (92.9) | 1 |
| Sweat | 104 (80) | 50 (83.3) | 54 (77.1) | 0.379 |
| Fatigue | 96 (73.8) | 44 (73.3) | 52 (74.3) | 0.902 |
| Back pain | 96 (73.8) | 53 (88.3) | 43 (61.4) | 0.001 |
| Anorexia | 82 (63.1) | 40 (66.7) | 42 (60) | 0.432 |
| Fever | 75 (57.7) | 40 (66.7) | 35 (50) | 0.055 |
| Headache | 75 (57.7) | 44 (73.3) | 31 (44.3) | 0.001 |
| Weight loss | 69 (53.1) | 43 (71.7) | 26 (37.1) | <0.001 |
| Nausea | 39 (30) | 21 (35) | 18 (25.7) | 0.249 |
| Stomach ache | 37 (28.5) | 26 (43.3) | 11 (15.7) | 0.001 |
| Testicular pain | 2 (1.5) | 2 (3.3) | 0 (0) | 0.211 |
| Laboratory findings (µ±SD) | ||||
| Leukocyte (/µL) | 7030±2036 | 6489±1904 | 7478±2046 | 0.001 |
| Neutrophil (/µL) | 4135±1758 | 3537±1597 | 4631±1742 | <0.001 |
| Lymphocyte (/µL) | 2263±708 | 2362±766 | 2181±651 | 0.152 |
| Monocyte (/µL) | 472±150 | 474±163 | 471±139 | 0.895 |
| MPV (fL) | 9.77±1.16 | 9.63±1.23 | 9.89±1.09 | 0.204 |
| RDW (%) | 14.1±1.8 | 14.1±1.6 | 14±1.9 | 0.248 |
| Hb (g/dL) | 13.9±1.6 | 13.2±1.5 | 14.4±1.5 | <0.001 |
| Plt (x103/µL) | 271±63 | 259±59 | 281±65 | 0.047 |
| Sedimentation (mm/h) | 31±20 | 38±16 | 26±22 | 0.006 |
| CRP (g/L) | 24.8±28.9 | 33.9±28.5 | 17.2±27.2 | <0.001 |
| ALT(U/L) | 33.4±24.2 | 40.7±25.6 | 27.3±21.2 | 0.002 |
| AST (U/L) | 31.2±21.5 | 38±18.7 | 25.5±22.2 | <0.001 |
| Glucose (mg/dL) | 96.2±19 | 94.7±20.9 | 97.5±17.3 | 0.335 |
| Urea (mg/dL) | 29.3±9.9 | 28.7±12.3 | 29.9±7.3 | 0.102 |
| Creatine (mg/dL) | 0.74±0.16 | 0.74±0.16 | 0.73±0.16 | 0.851 |
| STA titres (n, %) | 91 (70) | 37 (28.5) | 54 (41.5) | 0.055 |
| 1/160/STA taken cases | 21/91 (23.1) | 8/37 (21.6) | 13/54 (24.1) | |
| 1/320/STA taken cases | 19/91 (20.9) | 6/37 (16.2) | 13/54 (24.1) | |
| 1/640/STA taken cases | 17/91 (18.7) | 5/37 (13.5) | 12/54 (22.2) | |
| 1/1280/STA taken cases | 34/91 (37.3) | 18/37 (48.6) | 16/54 (29.6) | |
| Coombs gel titres (n, %) | 47 (36.1) | 25 (19.2) | 22 (16.9) | 0.226 |
| 1/160/Coombs gel test taken cases | 8/47 (17) | 2/25 (8) | 6/22 (27.3) | |
| 1/320/Coombs gel test taken cases | 14/47 (29.8) | 5/25 (20) | 9/22 (40.9) | |
| 1/640/Coombs gel test taken cases | 5/47 (10.6) | 3/25 (12) | 2/22 (9.1) | |
| 1/1280/Coombs gel test taken cases | 20/47 (42.6) | 15/25 (60) | 5/22 (22.7) | |
| Presence of complications (n, %) | 53 (41.1) | 28 (46.7) | 25 (35.7) | 0.177 |
| Presence of focal involvement (n, %) | 34 (41) | 16 (26.7) | 18 (25.7) | 0.902 |
| Sacroiliitis | 10/34 (29.4) | 7/16 (43.7) | 3/18 (16.6) | |
| Spondylodiscitis | 8/34 (23.5) | 3/16 (18.7) | 5/18 (27.7) | |
| Peripheral arthritis | 7/34 (20.5) | 1/16 (6.2) | 6/18 (33.3) | |
| Splenomegaly | 4/34 (11.6) | 3/16 (18.7) | 1/18 (5.5) | |
| Hepatomegaly | 3/34 (8.7) | 1/16 (6.2) | 2/18 (11.1) | |
| Epididymoorchitis | 3/34 (8.7) | 2/16 (12.5) | 1/18 (5.5) | |
| Erythema nodosum | 2/34 (5.6) | 2/16 (12.5) | 0/18 (0) |
ALT, alanine aminotransferase; AST, aspartate aminotransferase; CRP, C-reactive protein; dL, decilitre; fL, femtolitre; g, gram; Hb, haemoglobin; mg, milligram; mm, millimetre; MPV, mean platelet volume; L, litre; N, number; Plt, platelet; RDW, red cell distribution width; SD, standard deviation; STA, standard tube agglutination; U, unit; µL, microlitre; µ, mean
Treatment outcome findings
A total of 99 cases (76.1%) were successfully followed during treatment and for six months thereafter. Of the 51 patients (51.6%) who received the standard regimen, 22 (43.1%) were bacteraemic, while 19 (39.5%) of the 48 patients (48.4%) who received the modified regimen were bacteraemic. There was no significant difference between the two treatment groups (P=0.720). Relapse occurred in 5 (12.2%) bacteraemic and 4 (6.9%) non-bacteraemic cases (P=0.483)
After excluding relapse cases, the remaining 90 cases were analysed. Recovery was more frequent in non-bacteraemic cases (36/54, 66.7%), whereas prolonged convalescence was more common in bacteraemic cases (20/36, 55.6%) (P=0.037). At the end of treatment, the Rose Bengal test was available for 84 (64.6%) cases. Among bacteraemic patients, Rose Bengal negativity (P=0.038) and serological response (P=0.005) were less common compared to non-bacteraemia patients.
Results of ROC analysis and binary logistic regression analysis
The results of the ROC analysis are shown in the figure, and sensitivity and specificity values are presented in table III. No single parameter demonstrated sufficient sensitivity and specificity independently. A predictive model was developed using binary logistic regression analysis, which explained 78 per cent of the variance. According to the model, blood culture positivity was associated with an 8.5-fold increase for those with exposure history, a 9.4-fold increase for patients reporting back pain, and a 10-fold increase for individuals residing in the Diyadin district. Shorter symptom duration was associated with a 52.1 per cent probability of culture positivity, decreased haemoglobin with a 70.2 per cent probability, and elevated AST levels with a 52.2 per cent probability of culture positivity.
- ROC curves and area under the curves for (A) duration of complaints (day), (B) Coombs gel test titres, (C) haematological parameters and (D) biochemical parameters. Graph created using IBM SPSS Statistics (version 26.0, IBM Corp., Armonk, NY, USA;
https://www.ibm.com/products/spss-statistics
). ALT, alanine aminotransferase; AST, aspartate aminotransferase; AUC, area under the curve; CI, confidence interval; CRP, C-reactive protein; Hb, haemoglobin; Plt, platelet; S.e, standard error.
| Parameters | Threshold | Sensitivity (%) | Specificity (%) |
|---|---|---|---|
| Duration of complaints (days) | 18.5 | 61.4 | 65 |
| Coombs gel test titre | 1/640 | 72 | 68.2 |
| Leukocyte (/µL) | 6860 | 64.3 | 70.7 |
| Neutrophil (/µL) | 3505 | 78.6 | 70.7 |
| Haemoglobin (g/dL) | 14.25 | 57.1 | 82.8 |
| Platelet (x103/µL) | 269 | 57.1 | 58.6 |
| Sedimentation (mm/hour) | 32.5 | 70.3 | 75 |
| CRP (g/L) | 19 | 63.2 | 81.2 |
| ALT (U/L) | 31.6 | 55.2 | 79.7 |
| AST (U/L) | 27.3 | 67.2 | 84.1 |
ROC, receiver operating characteristic
Discussion
Blood cultures are not always feasible for diagnosing brucellosis, and serological tests can be difficult to interpret in endemic regions. In our study, we examined factors that may predict bacteraemia cases as alternatives to these methods. In patients with suspected brucellosis, the most important predictive factors were a history of exposure, residence in areas with a high incidence of cases, and the presence of back pain. Other significant predictive factors included a short duration of symptoms, low haemoglobin, and elevated AST levels.
Brucella species typically cause transient bacteraemia in the early stages of infection before localising to the reticuloendothelial system, which makes blood culture positivity more likely in patients presenting early3,17,18. Seasonal variation has also been reported, with higher incidence in spring and summer, attributed to increased human–animal contact during breeding periods19. Consistent with these findings, we observed that bacteraemia cases were more frequent in summer and presented earlier, possibly due to more severe symptoms, whereas non-bacteraemia cases were more common in winter.
Higher case concentrations have been reported in the northern and northeastern regions of Iraq, where animal husbandry is prevalent19. Similarly, Agri province is one of the leading livestock-producing areas in Türkiye20. Consistent with these observations, our study found that bacteraemia cases were concentrated in the Diyadin district, a region characterised by intensive animal husbandry.
The predominant clinical manifestations of bacteraemic brucellosis appear to vary across studies. One investigation highlighted the combined role of fever, back pain, and headache as predictors of bacteremia21. Another identified headache and myalgia as independent risk factors22. An inverse association between myalgia and bacteraemia has also been reported23. These discrepancies likely reflect differences in study design, geographic factors, and the clinical characteristics of the populations investigated.
Our findings regarding hematologic and biochemical parameters in bacteraemic cases are consistent with previous reports10,21,24. Cytopenia likely results from bone marrow infiltration by Brucella spp., whereas elevations in inflammatory markers reflect systemic inflammation. Similarly, increased ALT and AST levels indicate liver involvement, consistent with the organ’s central role in the reticuloendothelial system23. These results underscore the utility of routine haematologic and biochemical parameters in distinguishing bacteraemia from non-bacteraemia brucellosis.
In bacteraemic cases, disease management is more challenging due to the increased risk of relapse, the higher likelihood of progression to chronic brucellosis, and the potential reduction in treatment effectiveness5-7. In our study, this may be explained by the higher bacterial load in bacteraemia cases, which can complicate treatment and lead to the persistence of subjective symptoms after therapy.
A study conducted in children reported areas under the curve for biochemical parameters similar to those observed in our study8. High ferritin, low eosinophil counts, and elevated ESR rates have been identified as the most important laboratory predictors of brucellosis bacteremia10. Back pain and myalgia have been reported as predictors of bacteraemia in some studies, whereas headache and myalgia have been identified as predictors in others21,22.
The main limitations of our study are that it is retrospective, single-centred, and includes only two years of data. The relationship between serological tests could not be clearly evaluated due to intermittent supply problems and the use of different tests in our hospital. Another limitation is the inability to use PCR testing. Real-time PCR has become an important diagnostic tool in recent years because of its low contamination risk, high specificity, quantitative results, rapid turnaround, and ease of use25. Additionally, retrospective evaluation limited our ability to adequately assess complications. Follow up was challenging because most local residents are engaged in animal husbandry and live in villages. Treatment adjustments were often made during follow-up based on these factors, and well-organised data were not available to systematically evaluate treatment outcomes.
Multicentre studies would be more useful to better assess the impact of demographic factors. There is also a need for prospective studies with more comprehensive evaluations to detect complications, standardised treatment regimens, and systematic assessment of treatment outcomes.
Financial support & sponsorship
None
Conflicts of Interest
None
Use of Artificial Intelligence (AI)-Assisted Technology for manuscript preparation
The authors confirm that there was no use of AI-assisted technology for assisting in the writing of the manuscript and no images were manipulated using AI.
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