Antibacterial Effect of Lime Juice Against Streptococcus suis and Other Bacteria in Minced Pork

Abstract

Streptococcus suis is a significant zoonotic pathogen, capable of causing severe illnesses such as septicemia and meningitis in both swine and humans. Its transmission through pork consumption necessitates effective food safety measures. Lime juice, known for its antimicrobial properties, presents a potential alternative to reduce S. suis contamination in pork products. This study investigated the antibacterial efficacy of lime juice specifically against S. suis and its potential to reduce bacterial contamination in minced pork, aiming to determine optimal treatment parameters for mitigating S. suis transmission through pork consumption. Seven strains of S. suis representing serotypes known to cause zoonotic disease were cultured, and lime juice was prepared. The minimum inhibitory concentration and minimum bactericidal concentration tests consistently demonstrated the antibacterial effect of lime juice against S. suis. Survival curve analyses showed significant bacterial reduction within 15 min at 25% (v/v) lime juice concentration. In minced pork, lime juice caused a notable decrease in total bacteria and S. suis counts after 15 min. This study demonstrates the potential of lime juice as an antibacterial agent against a representative strain of S. suis in pork. However, the results also highlight that lime juice alone may not eliminate all viable bacteria. Therefore, incorporating lime juice treatment together with proper cooking practices remains crucial to ensure safe consumption of pork products.

Introduction

Streptococcus suis is a significant zoonotic pathogen capable of causing a range of illnesses including sepsis, pneumonia, endocarditis, arthritis, and meningitis in both swine and humans. Based on the antigenic properties of its capsular polysaccharides, S. suis is currently classified into 29 serotypes. Serotype 2 is predominantly associated with diseases in both pigs and humans. In addition, serotypes 1, 4, 5, 7, 9, 14, 16, 21, 24, and 31 have been identified in human infections (Hatrongjit et al., 2023; Hatrongjit et al., 2020; Liang et al., 2021).

The transmission routes of S. suis infection from pigs to humans primarily involve direct contact through skin wounds and the consumption of contaminated pork or pork products. Asymptomatic pigs can serve as a significant source of S. suis contamination in slaughterhouses, leading to increased risks for workers and consumers. Previous studies have demonstrated that S. suis strains isolated from slaughterhouse pigs are often identical or closely related to those found in diseased pigs and humans (Kerdsin et al., 2020; Lunha et al., 2024; Meekhanon et al., 2017). Inadequate identification and handling of infected animals, combined with poor meat inspection and limited access to protective equipment, can facilitate the transmission of S. suis through the contamination of pork meat (Kerdsin et al., 2022). Moreover, previous studies have consistently shown S. suis contamination in pork meat, suggesting that improper hygiene practices during carcass and pork handling contribute to cross-contamination in the supply chain (Boonyong et al., 2019; Guntala et al., 2024; Wongnak et al., 2020).

Human cases of S. suis infection have been reported worldwide, with a notable prevalence observed in Asian countries. In regions such as Thailand and Vietnam, where the traditional consumption of raw pork dishes is common, outbreaks of S. suis human infection have been frequent (Goyette-Desjardins et al., 2014). Since 2007, at least five significant outbreaks of S. suis human infections have been documented in northern and northeastern parts of Thailand. These outbreaks were linked to cultural practices involving the consumption of raw pork dishes during local festivals held in the summer months. The 2021 outbreak in northeastern Thailand (Nakhon Ratchasima province) involved 21 confirmed cases and 2 fatalities, highlighting the ongoing threat posed by S. suis in the region (Kerdsin, 2022). Epidemiological investigations and whole genome sequencing identified a raw pork dish from a single pig as the outbreak source, emphasizing the importance of food safety practices in preventing the spread of this pathogen. The outbreak strain exhibited reduced susceptibility to penicillin and resistance to multiple antibiotics, highlighting the need for ongoing antimicrobial resistance monitoring in S. suis (Brizuela et al., 2023). While the national annual incidence ranges from 0 to 0.381 per 100,000 persons, localized studies have reported higher rates, suggesting potential regional variations (Kerdsin, 2022; Praphasiri et al., 2015). These findings emphasize the necessity of exploring alternative approaches to enhance food safety, particularly through the application of natural compounds known for their antimicrobial properties.

In recent decades, there has been increasing interest in exploring natural antimicrobial agents as potential interventions to reduce bacterial contamination in food products. Citrus fruits, including lime (Citrus aurantifolia), are known for their antimicrobial properties due to the presence of bioactive compounds such as phenols, citric acid, and flavonoids (Oikeh et al., 2016). Lime juice has been reported to exhibit antibacterial activity against various pathogens (Aibinu et al., 2006), making it a promising candidate for food safety applications. However, the specific antibacterial effect of lime juice on S. suis, especially in pork, remains relatively limited. Understanding the efficacy of lime juice against S. suis and other bacterial contaminants in pork products could provide valuable insights into developing strategies to mitigate the risk of S. suis transmission through pork consumption.

Therefore, this study aims to investigate the antibacterial effectiveness of lime juice against S. suis both in vitro and in minced pork and to determine the practical concentration of lime juice required to reduce the risk of S. suis transmission through pork consumption. The findings of this study could contribute to enhancing food safety measures and reducing the risk of S. suis infections associated with pork consumption.

Materials and Methods

Bacterial isolates and preparation of inoculum

Seven strains of S. suis serotypes 2, 9, 16, and 21, isolated from both diseased and healthy carrier pigs, were used in this study. Details on the isolation process and sample information can be found in previous studies (Meekhanon et al., 2019; Meekhanon et al., 2017) and in Supplementary Table S1. These were selected as representatives of serotypes known to cause disease in both humans and animals. S. suis TRG22, identified as serotype 2 and isolated from a diseased pig, was considered the most hazardous strain among those tested, posing a potential public health risk. Consequently, it was selected as the representative strain for the survival curve analysis and antibacterial activity experiments with lime juice in minced pork.

Each isolate was cultured on 5% sheep blood agar plates (Himedia, India) and incubated at 37°C for 24 h. Subsequently, the bacterial colonies were transferred to Todd-Hewitt Broth (THB; Himedia) and thoroughly mixed. The bacterial suspension was adjusted to a concentration of approximately 1.5 × 10⁸ colony-forming unit (CFU)/mL by matching its turbidity to that of a 0.5 McFarland standard. In addition, dilutions were prepared at a 1:30 ratio to achieve a microbial concentration of 5 × 10⁶ CFU/mL for further testing.

Preparation of lime juice

In this study, lime fruits were collected from kitchen gardens in KhonKaen province, Thailand, located at latitude = 16.4408° N and longitude = 102.7516° E. The authenticity of the lime fruits was confirmed by the KhonKaen University Herbarium unit. For the preparation of lime juice, the lime fruits were initially washed with tap water and then sanitized by cleaning with 70% ethanol (Hindi and Chabuck, 2013). Subsequently, the fruits were halved using a sterile knife, and the lime juice was squeezed into a test tube using a sterilized funnel. The juice was then centrifuged at 13,751 g for 5 min, and the supernatant was transferred into a sterile 50 mL centrifuge tube. The lime juice was then filter-sterilized using a 0.45 μm pore size membrane filter and stored at −20°C for further analysis.

Antimicrobial activity of lime juice in bacterial cultures

Minimum inhibitory concentration and minimum bactericidal concentration

The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of lime juice against S. suis were determined using the broth microdilution method as described by a previous study (Mshelia et al., 2017) with lime juice concentrations ranging from 0.04% to 50% (v/v). Briefly, 100 μL of lime juice was pipetted into the first and second rows of a 96-well plate, followed by 100 μL of THB in all test wells (rows 2–12). A 100 μL solution from the second row was then transferred to the third row, mixed, and serially diluted two-fold through to the 11th row. Row 12 served as the positive control. Prepared S. suis bacterial suspensions were added to each well, with 100 μL per well. Each strain was tested across two rows (A, C, E, G), leaving rows G and H on the second plate for THB and the negative control. The plates were incubated at 37°C for 24 h.

MIC was determined by measuring the optical density (OD) at 600 nm using an Epoch Microplate Spectrophotometer (BioTek^® Instruments, USA). An OD600 reading of ≥0.08 indicated bacterial growth (Brennan-Krohn et al., 2017). Therefore, the lowest concentration of lime juice that resulted in an average OD600 difference of <0.08 compared with the negative control was considered the MIC, indicating a significant reduction in bacterial growth.

For MBC determination, a 10 μL aliquot from each well showing no visible growth in the MIC assay was plated on Todd-Hewitt Agar (THA; Himedia) and incubated at 37°C for 24 h. The MBC was defined as the lowest concentration of lime juice that prevented bacterial growth on the agar plates. Each experiment was performed in triplicate for accuracy.

Survival curve

The effect of lime juice on the survival curves of S. suis TRG22 (serotype 2) was investigated. Initially, an overnight culture suspension was prepared with a concentration of approximately 1.5 × 10⁶ CFU/mL in THB medium. This inoculum suspension was then divided into 5 mL portions and aliquoted into six test tubes. Lime juice was added to the tubes at the final concentrations of 0%, 3.125%, 6.25%, 12.50%, 25%, and 50% (v/v), with the final volume in each tube adjusted to 10 mL in THB medium. The viability of bacteria was assessed at exposure times of 0, 5, 15, 30, and 60 min by transferring 0.1 mL of the suspension onto THA for colony counting after 24 h of incubation at 37°C (Pian et al., 2016). The experiment was repeated three times to ensure reliability of results.

Antibacterial activity of lime juice in minced pork

Preparation of minced pork, bacterial cultures, and lime juice

In this study, raw pork sourced directly from the meat industry was minced using an aseptic technique. The pH of the pork was measured at the Central Laboratory (Thailand) Co., Ltd. Subsequently, the minced pork was weighed (25 ± 0.1 g) in a stomacher bag for further testing. An inoculum was prepared using the S. suis TRG22 isolate, which was previously obtained from swine clinical specimens (Meekhanon et al., 2019). The bacterial suspension was then diluted with 0.85% NaCl solution to achieve a turbidity of 0.5 McFarland standard, corresponding to a concentration of approximately 1.5 × 10⁸ CFU/mL. This suspension was further diluted to 1:360 in order to obtain an inoculum concentration of approximately 4.17 × 10⁵ CFU/mL. To prepare a lime juice solution with a 52.08% (v/v) concentration, 52.08 mL of lime juice was mixed with 47.92 mL of sterile distilled water, and the initial pH value of the resulting lime juice solution was measured.

Microbiological analysis

Prior to the inoculation, minced pork samples were analyzed to identify the initial bacterial population. A 25 g sample of minced pork was then inoculated with 1 mL of a bacterial suspension containing 4.17 × 10⁵ CFU/mL. To ensure a homogeneous distribution of the inoculum, the mixture was thoroughly homogenized. Subsequently, 24 mL of 52.08% (v/v) lime juice was added to the inoculated minced pork to achieve a final concentration of 25% (v/v). For optimal mixing, the mixture was homogenized again using a stomacher for 1 min. The samples were then exposed to lime juice at room temperature for varying time intervals of 5, 10, 15, and 30 min (Bingol et al., 2011).

The minced pork samples were then placed in sterile stomacher bags containing 200 mL of sterile saline peptone water and analyzed for the presence of S. suis through a 10-fold dilution. Six droplets of 20 μL each were plated on THA and incubated at 37°C for 48 h. Colonies growing on THA were counted within the range of 2–20 CFU/mL. Confirmation of the typical S. suis colonies on THA was achieved through PCR assay targeting the recombination/repair protein (recN) gene (Ishida et al., 2014) with viable bacterial counts assessed using the Miles and Misra methods (Miles et al., 1938). To ensure the reliability of the experiment, inoculum control, pork control, and positive control were performed.

Statistical analysis

All experiments were independently conducted three times in duplicate. To assess the effect of lime juice in minced pork samples, a one-way analysis of variance was performed, and means were compared using Duncan’s multiple range tests. Statistical analysis was carried out using SPSS version 28.00 for Windows (IBM SPSS Inc., NY, USA). Graphs were generated using GraphPad Prism version 5.0 for Windows (Graph Pad Software Inc., USA).

Results

Antibacterial effect of lime juice on S. suis cultures

The results from the MIC and MBC tests of lime juice against S. suis in all seven isolates are presented in Table 1. MIC and MBC values were consistently 0.78% or 1.56% (v/v) for all isolates, demonstrating a consistent antibacterial effect across the tested strains. The MIC50 refers to the lime juice concentration that inhibited the growth of S. suis by 50%, whereas the MBC50 represents the concentration that killed 50% of the bacterial population.

Table 1.

Minimum Inhibitory Concentration and Minimum Bactericidal Concentration Values of Lime Juice Against Seven Strains of Streptococcus suis

S. suis Strain	Serotype	Lime Juice (% v/v)
S. suis Strain	Serotype	MIC	MBC
PF9	16	1.56	1.56
PF23	9	1.56	1.56
PF71	21	1.56	1.56
SP52	2	1.56	1.56
SP74	2	1.56	1.56
SP76	2	0.78	0.78
TRG22	2	0.78	0.78

% v/v, percentage by volume; MIC, minimum inhibitory concentration; MBC, minimum bactericidal concentration.

The viability of bacterial cells decreased with lower pH of the mixture, higher concentrations of lime juice, and longer exposure times. As shown in Table 2, bacterial survival was observed at a concentration of 3.125% (v/v) for up to 60 min, whereas complete inhibition of bacteria occurred within 15 min at a concentration of 12.5% (v/v). At concentrations of 25% and 50% (v/v), total bacterial elimination was achieved within 5 min. Based on our results, the optimal concentration of lime juice to assess its antibacterial effect in minced pork was 25% (v/v).

Table 2.

The Survival of Streptococcus suis TRG22 in Lime Juice at Different Concentrations and Exposure Times

Lime Juice		Number of Survival Cells (Log CFU/mL) at Different Exposure Times
Concentrations (%v/v)	pH	0 min	5 min	15 min	30 min	60 min
0	7.58	5.32 ± 0.05^a	5.30 ± 0.01^a	5.39 ± 0.08^a	5.37 ± 0.09^a	5.31 ± 0.02^a
3.125	4.3	5.06 ± 0.03^a	4.73 ± 0.01^b	3.80 ± 0.03^c	3.55 ± 0.03^d	2.80 ± 0.04^e
6.25	3.78	5.11 ± 0.02^a	4.39 ± 0.04^b	3.43 ± 0.02^c	2.43 ± 0.06^d	0^e
12.5	3.31	5.35 ± 0.06^a	4.13 ± 0.07^b	0^c	0^c	0^c
25	2.91	5.15 ± 0.02^a	0^b	0^b	0^b	0^b
50	2.61	5.07 ± 0.04^a	0^b	0^b	0^b	0^b

Data are presented as the mean ± standard deviation (SD; n = 3). Mean values within the same row with different superscript lowercase letters (a, b, c, d, e) indicate significant differences (p < 0.05).

% v/v, percentage by volume; CFU, colony-forming unit.

Antibacterial effect of lime juice in minced pork

The antibacterial effect of 25% (v/v) lime juice against S. suis TRG22 and other bacteria in minced pork was examined at various time intervals (0, 5, 10, 15, and 30 min). The pH of the lime juice and minced pork used in this experiment were 2.3 and 6.84, respectively. The average initial bacterial concentration in the minced pork was 2.79 ± 0.07 log CFU/g. After adding 1 mL of S. suis TRG22 culture containing 5.65 ± 0.10 log CFU/mL, the total bacterial count in the minced pork increased to 3.37 ± 0.02 log CFU/g.

The results demonstrated a significant inhibitory effect at 25% (v/v) lime juice on the growth of both S. suis TRG22 and the indigenous bacterial population within the minced pork samples. As shown in Table 3, a progressive decrease in total bacterial count was observed with increasing contact time between the lime juice and the minced pork. The addition of lime juice resulted in a statistically significant reduction in total bacterial count at exposure times of 5, 10, and 15 min. However, no significant difference was observed in bacterial counts between the 15 and 30 min exposure periods (p > 0.05).

Table 3.

Efficacy of Lime Juice in Reducing Total Bacteria and Streptococcus suis TRG22 (log10 CFU/g) in Minced Pork Samples

Number of Bacterial Cells after Treatment	Exposure Times (min)
Number of Bacterial Cells after Treatment	0	5	10	15	30
Total bacteria after treatment with 25% (v/v) lime juice	3.38 ± 0.02^a	2.40 ± 0.24^b	1.84 ± 0.24^c	1.54 ± 0.07^c	1.47 ± 0.34^c
S. suis after treatment with 25% (v/v) lime juice	3.35 ± 0.31^a	2.29 ± 0.2^b	1.76 ± 0.14 ^c	0.91 ± 0.32^d	1.08 ± 0.42^d
Total bacteria in control group	3.40 ± 0.10^a	3.38 ± 0.08^a	3.37 ± 0.07^a	3.40 ± 0.09^a	3.39 ± 0.10^a

Mean values within the same row with different superscript lowercase letters (a, b, c, d) are significantly different (p < 0.05).

% v/v, percentage by volume; CFU, colony-forming unit.

Similarly, a significant reduction in viable S. suis TRG22 was observed following exposure to lime juice. Consistent with the findings of total bacteria count, statistically significant reductions were observed at exposure times of 5, 10, and 15 min (p < 0.05). Specifically, the number of S. suis after treatment with lime juice for 15 min was 0.91 ± 0.32 log10 CFU/g compared with 3.35 ± 0.31 log10 CFU/g at the beginning of the experiment (Table 3). No significant difference in S. suis counts was observed between the 15 and 30 min exposure periods (p > 0.05). Based on these observed reductions in both total bacterial count and S. suis TRG22, an exposure time of 15 min appears to be the most effective for the application of 25% (v/v) lime juice in this minced pork model. However, it is important to consider additional factors, such as the initial bacterial load and desired level of decontamination, when determining the optimal treatment time for specific applications.

Discussion

S. suis infections pose a significant public health and economic burden, particularly in Southeast Asia (Goyette-Desjardins et al., 2014). A previous study in Thailand estimated per-person losses exceeding US$36,000 due to S. suis infections (Rayanakorn et al., 2018). Therefore, effective food safety measures are crucial to prevent S. suis transmission. Our findings significantly contribute to this effort by demonstrating the potential of lime juice as a decontamination strategy in a minced pork model. We observed a notable inhibitory effect at 25% (v/v) lime juice, with a gradual decline in both the total bacterial count and viable S. suis levels over time. Using bacterial concentrations within the reported range of S. suis levels in purchased pork (2.44 to 5.94 log CFU/g) from a previous study (Wongnak et al., 2020), we observed a significant reduction in both total bacterial counts and S. suis after 15 min exposure to lime juice, highlighting its potential as an effective decontamination method for minced pork.

These findings align with previous studies emphasizing the antimicrobial properties of lime juice (Aibinu et al., 2006; Hassan et al., 2013). The organic acids present in lime juice, including citric acid, are well-recognized for their ability to reduce bacterial viability by disrupting cell membranes and altering cytoplasmic pH (Mani-López et al., 2012). This mechanism is likely responsible for the observed reduction in S. suis within the minced pork. The antimicrobial properties of lime juice suggest its potential to reduce the risk of S. suis infection among consumers by impacting the viability of this pathogen in raw pork or pork products.

Citric acid and its salts have proved to be effective in controlling pathogens in both fresh- and processed meat and poultry (Mani-López et al., 2012). However, their application may be limited by potential adverse sensory effects and the necessity to maintain low pH levels for optimal antimicrobial efficacy. In our study, while 15 min exposure time was effective in reducing S. suis in minced pork, it is important to note that this study did not address the potential presence of other foodborne pathogens such as Salmonella, Staphylococcus aureus, or helminths, which may not be effectively reduced by lime juice. Therefore, the consumption of raw or undercooked pork cannot be recommended based on these findings. In addition, factors such as temperature and pH during lime juice treatment should be explored to optimize the decontamination process and the sensory attributes of lime juice-treated meat. Further investigation is needed to assess its acceptability and potential applications in food processing.

Conclusion

Our findings demonstrate the significant inhibitory effect of lime juice on S. suis and other bacteria in minced pork. However, it is important to acknowledge that even after 30 min of exposure, complete elimination may not be achieved with lime juice alone. Therefore, for optimal food safety, lime juice treatment should be considered as part of a comprehensive strategy, potentially combined with proper cooking temperatures, to ensure the safety of pork products.

Footnotes

Authors’ Contributions

D.K.: Conceptualization, methodology, formal analysis, investigation, validation, and writing—original draft. K.S.: Formal analysis and writing—review and editing. T.K.: Resources and writing—review and editing. S.K.: Resources, supervision, writing—review and editing. N.M.: Conceptualization, methodology, validation, formal analysis, funding acquisition, resources, supervision, writing original draft, and writing—review and editing. All authors have read and approved the published version of the article.

Disclosure Statement

No competing financial interests exist.

Funding Information

This study was financially supported by the Graduate Program Scholarship from the Graduate School, Kasetsart University, Bangkok, Thailand, and the Kasetsart University Research and Development Institute, KURDI (FF(S-KU)5.66).

Supplementary Material

Supplementary Table S1

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Supplementary Material

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