Proteus species are facultatively anaerobic, Gram-negative bacilli that belong to the Enterobacteriaceae family and are frequently seen as opportunistic infections in both community and hospital settings. These bacteria are found throughout the environment, including soil, water, and decomposing organic materials, and are part of the natural flora of the human gastrointestinal system [1, 2]. Proteus mirabilis and Proteus vulgaris are the most clinically significant species in the genus Proteus, having been linked to a variety of illnesses including urinary tract infections (UTIs), wound infections, septicemia, respiratory tract infections, and soft tissue infections [3-6]. One of the distinguishing features of Proteus species is their capacity to swarm across solid medium, which facilitates identification in the laboratory [7]. They also produce urease, an enzyme that hydrolyzes urea into ammonia and carbon dioxide, creating an alkaline environment [8]. This enzyme activity is especially significant in the pathogenesis of urinary tract infections caused by Proteus species, as high pH can trigger the production of struvite and apatite stones in the urinary system, resulting in persistent and difficult infections [9]. Because of their distinct pathogenic processes and broad environmental distribution, Proteus species present a substantial barrier in clinical diagnosis and therapy [10]. The therapeutic management of infections caused by Proteus species has grown increasingly complex in recent decades as a result of the advent and rapid spread of antibiotic resistance, particularly resistance mediated by Extended-Spectrum Beta-Lactamases [11]. ESBLs are enzymes that hydrolyze and confer resistance to beta-lactam antibiotics, such as penicillins, cephalosporins (particularly third-generation cefotaxime, ceftazidime, and ceftriaxone), and aztreonam, but not cephamycins or carbapenems [12]. The creation of ESBLs by Proteus species restricts the therapeutic alternatives available, resulting in treatment failures, longer hospital stays, higher healthcare expenses, and increased morbidity and death [13]. Among the several forms of ESBL enzymes, the CTX-M group has acquired global recognition as the most common and quickly spreading. CTX-M enzymes preferentially hydrolyze cefotaxime and related cephalosporins [14, 15]. They are frequently encoded on plasmids that can be transmitted between bacterial species, allowing resistance genes to spread within and across bacterial populations [16]. The prevalence of ESBL-producing Proteus isolates is thus a serious public health concern, especially in healthcare settings where selective pressure from widespread antibiotic usage hastens resistance development [17]. The accurate and early diagnosis of ESBL-producing pathogens is critical for optimal patient care and infection control. The Clinical and Laboratory Standards Institute (CLSI) has advocated phenotypic approaches for detecting and confirming ESBL generation [18, 19]. Screening commonly entails assessing susceptibility to third-generation cephalosporins using the disc diffusion method. Isolates with reduced susceptibility are subsequently submitted to confirmatory phenotypic assays, including the Combined Disc Test (CDT), Double Disc Synergy Test (DDST), and ESBL E-test [20 & 21]. These methods are extensively utilized because they are cost-effective, relatively straightforward, and can be conducted in most clinical microbiology laboratories without the need for advanced molecular techniques [22]. Phenotypic detection of ESBL producers is crucial not only for determining optimal antibiotic therapy, but also for epidemiological surveillance and infection control [23]. It allows clinicians to avoid using ineffective antibiotics and instead employ carbapenems or beta-lactamase inhibitor combos, which are still effective against many ESBL-producing bacteria [24]. Furthermore, early detection and isolation of patients with ESBL-producing bacteria is critical for preventing horizontal transmission inside healthcare facilities [25]. Despite their clinical significance, ESBL-producing Proteus species have received less attention than other Enterobacteriaceae, such as Escherichia coli and Klebsiella pneumoniae [26, 27]. This research gap underscores the importance of conducting specific studies to determine the incidence of ESBL generation among Proteus isolates and describe their resistance characteristics. Understanding the antimicrobial susceptibility patterns of these isolates is essential for updating treatment guidelines and antibiotic stewardship strategies [28].  This study was conducted to address these gaps by screening clinical Proteus isolates for ESBL production using phenotypic methods, analyzing their antimicrobial resistance patterns, and identifying the most effective detection techniques in a tertiary care hospital setting. Such data are vital for improving diagnostic accuracy, tailoring therapy, and implementing effective infection control measures to curb the spread of resistant Proteus strains.

Study Design and Sample Collection

During the study period, 1124 clinical samples were collected from patients attending various departments at Tirunelveli Medical College, yielding 100 non-duplicate Proteus species isolates in total. Clinical specimens comprised pus, urine, sputum, tissue biopsies, and bronchial wash samples. All isolates were processed and identified using standard microbiological techniques. Isolation involves inoculating materials onto selective and differential media, such as MacConkey agar and blood agar plates, which were then incubated at 37°C for 18-24 hours. To definitively identify Proteus species, colonies with characteristic morphology and swarming motility were subjected to Gram staining and a battery of biochemical tests, including urease production, indole, citrate utilization, triple sugar iron (TSI) agar reactions, and motility tests.

Ethical Clearance

Since this study involved clinical samples obtained from human subjects, prior ethical approval was obtained from the Institutional Ethics Committee of Tirunelveli Medical College. The study adhered to ethical standards concerning the use of patient samples and confidentiality of patient information.

Informed Consent

Informed consent was obtained from all patients or their legal guardians prior to sample collection. The purpose of the study, procedure involved, and confidentiality assurances were explained in the local language to ensure voluntary participation.

Antimicrobial Susceptibility Testing

Antimicrobial susceptibility testing (AST) was performed on all Proteus isolates using the Kirby-Bauer disc diffusion method on Mueller-Hinton agar, according to the Clinical and Laboratory Standards Institute (CLSI) guidelines current at the time of the study. A standardized inoculum equivalent to 0.5 McFarland turbidity was prepared from fresh overnight cultures and uniformly spread on the Mueller-Hinton agar plates [29].

The antibiotic discs tested included:

• Amikacin (30 µg)
• Gentamicin (10 µg)
• Ciprofloxacin (5 µg)
• Cotrimoxazole (Trimethoprim-Sulfamethoxazole) (1.25/23.75 µg)
• Cefotaxime (30 µg)
• Ceftazidime (30 µg)
• Cefpodoxime (10 µg)
• Ceftriaxone (30 µg)

After incubation at 37°C for 16-18 hours, the diameters of the zones of inhibition around the antibiotic discs were measured in millimeters. The interpretation of susceptibility, intermediate resistance, or resistance was made according to CLSI breakpoints.

Phenotypic Detection of ESBL Production

Isolates exhibiting reduced susceptibility or resistance to any of the third generation cephalosporins (cefotaxime, ceftazidime, ceftriaxone, or cefpodoxime) were considered potential ESBL producers and subjected to confirmatory phenotypic tests for ESBL production [30].

The following phenotypic methods were employed:

1. Combined Disc Test (CDT)

The Combined Disc Test is based on the principle of synergy between clavulanic acid, a beta-lactamase inhibitor, and third generation cephalosporins. Two discs were placed on Mueller-Hinton agar plates inoculated with the test organism, one containing cephalosporin alone (cefotaxime 30 µg or ceftazidime 30 µg) and the other containing the same cephalosporin combined with clavulanic acid (cefotaxime/clavulanic acid 30/10 µg or ceftazidime/clavulanic acid 30/10 µg). The discs were placed 25-30 mm apart (centre to centre). After overnight incubation, an increase of ≥5 mm in the inhibition zone diameter around the disc containing clavulanic acid compared to the cephalosporin disc alone was interpreted as positive for ESBL production [31].

2. Double Disc Synergy Test (DDST)

The Double Disc Synergy Test detects ESBL production by observing the enhancement of the inhibition zone of a cephalosporin disc toward a disc containing clavulanic acid. A disc of amoxicillin-clavulanic acid (20/10 µg) was placed centrally on a Mueller-Hinton agar plate inoculated with the test isolate. Discs of third generation cephalosporins (cefotaxime 30 µg and ceftazidime 30 µg) were placed 20 mm apart (edge to edge) from the amoxicillin-clavulanic acid disc. After incubation at 37°C for 16-18 hours, a keyhole or funnel-shaped zone of inhibition between the clavulanic acid disc and any cephalosporin disc was considered indicative of ESBL production [32].

3. ESBL E-test

The ESBL E-test utilizes a strip impregnated with a gradient of cephalosporin on one end and cephalosporin plus clavulanic acid on the other. The strip was placed on Mueller-Hinton agar plates inoculated with the test strain. Following incubation at 37°C for 18-24 hours, the minimum inhibitory concentrations (MICs) for cephalosporin alone and cephalosporin with clavulanic acid were read. A ratio of MIC of cephalosporin alone to that of cephalosporin plus clavulanic acid ≥8 was interpreted as positive for ESBL production [33].

Statistical Analysis

Data were analyzed using IBM SPSS Statistics version 20. Descriptive statistics summarized demographics and isolate distribution as frequencies and percentages. Chi-square tests compared categorical variables like ESBL prevalence across age, gender, specimen type, and wards. McNemar test was used for paired categorical data, such as comparing phenotypic test results. A p-value < 0.05 was considered statistically significant.

Age and Gender Distribution

A total of 100 Proteus isolates were collected, with 68 isolates from male patients and 32 from females. The age distribution revealed that the majority of isolates (59%) were obtained from patients aged between 46 and 75 years. The mean age for males was 50.75 years, whereas for females it was 41.59 years (Table 1).

Table 1: Age and Sex Distribution of Study Isolates

Specimen Distribution

Specimen-wise analysis showed that the majority of isolates were recovered from pus samples (57%), followed by urine (37%). Small proportions were isolated from tissue (3%), sputum (2%), and bronchial wash (1%) (Table 2).

Table 2: Specimen-wise Distribution of Proteus Isolates

Ward-wise Distribution

Isolates were most frequently obtained from the surgery ward (44%), followed by the medicine ward (20%). Other wards included pediatrics (12%), urology (11%), orthopedics (5%), intensive care (5%), and obstetrics & gynecology (3%) (Table 3).

Table 3: Ward-wise Distribution of Proteus Isolates

4.5 Antimicrobial Resistance Patterns

The resistance profile showed the highest resistance to cotrimoxazole (81%), followed by gentamicin (69%), ceftazidime (61%), and cefotaxime (60%). Resistance to amikacin was the lowest at 28% (Table 4).

Table 4: Antimicrobial Resistance Pattern of Proteus Isolates

Screening and Confirmation of ESBL Production

Out of 100 isolates, 61 showed resistance to ceftazidime and were screened for ESBL production. Confirmatory testing by the Combined Disc Test (CDT) identified 47 isolates (77.4%) as ESBL producers (Table 5 & 6). These isolates were further subjected to phenotypic confirmation by DDST and E-Test.

Table 5: Susceptibility Pattern of Proteus Isolates to 3rd Generation Cephalosporins

Table 6: Detection of ESBL by Phenotypic Methods

4.7 Comparison of Phenotypic Tests for ESBL Detection

When compared with CDT, the Double Disc Synergy Test (DDST) detected 38 of the 47 CDT-positive isolates, resulting in a sensitivity of 80.8% and specificity of 100%. The positive predictive value (PPV) was 100%, and the negative predictive value (NPV) was 60.8% (Table 7). The ESBL E-Test identified 41 of the 47 CDT-positive isolates, yielding a sensitivity of 87.2% but lower specificity of 57.1%. The PPV and NPV for E-Test were 87.2% and 57.1%, respectively (Table 8).

Table 7: Comparison of DDST with CDT for ESBL Detection

Table 8: Comparison of E-Test with CDT for ESBL Detection

This study provides insights into the prevalence, phenotypic detection, and antimicrobial resistance patterns of ESBL-producing Proteus species isolated from clinical specimens at a tertiary care center in South India. The emergence of multidrug-resistant (MDR) organisms, particularly those producing Extended-Spectrum Beta-Lactamases (ESBLs), has become a major public health concern, especially in hospital settings where infections can lead to increased morbidity, prolonged hospital stays, and higher treatment costs.

Demographic and Clinical Distribution

In this study, Proteus infections were more prevalent among male patients (68%) than females (32%), with the most affected age group being 46–75 years. This age-related susceptibility aligns with the increased risk of nosocomial infections in elderly individuals due to underlying comorbidities, weakened immunity, and prolonged hospitalization. Similar demographic trends were noted by Gupta et al. (2020) [34] and Yadav et al. (2021) [35], emphasizing that older adults, especially men, are disproportionately affected by Proteus infections. The majority of isolates were Proteus mirabilis (63%), followed by Proteus vulgaris (37%). This finding is consistent with the literature, where P. mirabilis is frequently identified as the predominant species involved in urinary tract and wound infections, as reported by Taneja et al. (2012) [36] and Mohanty et al. (2023) [37]. Surgical wards accounted for the highest proportion of isolates (44%), followed by medicine (20%), indicating a strong association between Proteus infections and invasive procedures, open wounds, or catheter use. Pus (57%) and urine (37%) were the most common specimen types, highlighting the organism's role in wound and urinary tract infections. Similar patterns of specimen and ward distribution were documented by Mukherjee et al. (2013) [38] and Paterson & Bonomo (2005) [39], underscoring the relevance of these sources in hospital-acquired Proteus infections.

Antimicrobial Resistance Patterns

The resistance profile observed in this study was alarming. Cotrimoxazole showed the highest resistance rate (81%), followed by gentamicin (69%) and ciprofloxacin (58%). These results are comparable with those from Shaikh et al. (2015) [40] and Singh et al. (2021) [41], who reported similar resistance trends in tertiary care centers. The significant resistance to third-generation cephalosporins, such as ceftazidime (61%) and cefotaxime (60%), suggested the likely production of Extended-Spectrum Beta-Lactamases (ESBLs), which was later confirmed by phenotypic testing. On the other hand, amikacin was the most effective drug with a resistance rate of only 28%, a finding consistent with Kumar et al. (2019) [42], who emphasized the continued efficacy of amikacin against ESBL-producing organisms. However, the prudent use of this drug remains essential to prevent emerging resistance.

Phenotypic Detection of ESBL

Of the 61 isolates that showed resistance to third-generation cephalosporins, 47 (77.4%) were confirmed as ESBL producers by the CDT, which is endorsed by the CLSI for ESBL confirmation. This prevalence closely mirrors the ESBL rates reported by Shaikh et al. (2015) (42%) and Yadav et al. (2021) (33%), although the higher rate in our study may reflect increased antibiotic pressure or hospital-specific factors [40 & 35]. The DDST detected 38 of the 47 CDT-confirmed isolates, yielding a sensitivity of 80.8% and specificity of 100%. This corroborates findings by Drieux et al. (2008) [43], who originally described the method and acknowledged its high specificity but variable sensitivity depending on disc placement and enzyme expression levels.  The ESBL E-test, a gradient method offering MIC data, detected 41 of 47 CDT-positive isolates (sensitivity 87.2%, specificity 57.1%). These results are consistent with Rawat and Nair (2010), who reported that while the E-test offers quantitative advantages, its performance may be affected by subjective interpretation or borderline MIC values [44]. Thus, CDT remains the preferred phenotypic method due to its balance of cost, reliability, and CLSI endorsement.

Implications and Significance

This study reveals a substantial prevalence of ESBL-producing Proteus species in a tertiary care setting, reflecting a serious threat to empirical antibiotic therapy. Routine phenotypic detection of ESBLs, especially using the CDT and DDST, should be integrated into diagnostic workflows, particularly in resource-limited settings where molecular methods may not be feasible. The high resistance levels observed underscore the need for robust antimicrobial stewardship and continuous surveillance to guide empirical treatment policies and infection control measures.

Limitations

While this study provides valuable insights into ESBL prevalence and resistance trends, it was limited to phenotypic detection of ESBLs. Genotypic methods, which were performed separately for some isolates, could offer a more detailed understanding of resistance mechanisms. The sample size, though sufficient for initial surveillance, may not fully represent seasonal or long-term trends, highlighting the need for larger, multicenter studies.

his study highlights the significant prevalence of ESBL-producing Proteus species in clinical settings, with P. mirabilis being the most common isolate. A high level of resistance was observed against commonly used antibiotics, particularly third-generation cephalosporins and cotrimoxazole, indicating the growing threat of multidrug-resistant strains. Among phenotypic methods, the CDT proved to be the most reliable for ESBL confirmation, offering a balance of sensitivity and specificity. The DDST and E-test also demonstrated utility but with varying performance characteristics. These findings emphasize the need for routine ESBL screening in diagnostic laboratories, especially in resource-limited settings, to guide appropriate antibiotic therapy and contain the spread of resistance. Effective infection control measures, rational antibiotic use, and continued surveillance are essential to manage the burden of ESBL-producing Proteus and ensure optimal patient outcomes.

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