
==== Front
Poult Sci
Poult Sci
Poultry Science
0032-5791
1525-3171
Elsevier

S0032-5791(24)00747-8
10.1016/j.psj.2024.104168
104168
IMMUNOLOGY, HEALTH AND DISEASE
In vitro antibacterial activity of danofloxacin against Escherichia coli isolated from pigeons and its pharmacokinetic in pigeons
Duan Ming-Hui 2
Li Ze-En 2
Zhang Yan-Ni
Jin Yang-Guang
Liu Yue
Li Xing-Ping
Yang Fan yfscau@126.com
fyang@haust.edu.cn
1
Laboratory of Veterinary Drug Development and Evaluation, College of Animal Science and Technology, Henan University of Science and Technology, Luoyang, 471023, China
1 Corresponding author: yfscau@126.comfyang@haust.edu.cn
2 Both authors contributed equally to this manuscript.

02 8 2024
10 2024
02 8 2024
103 10 10416811 6 2024
30 7 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
This experiment aimed to investigate the in vitro antimicrobial activity of danofloxacin against Escherichia coli (E. coli) isolated from pigeons, as well as the pharmacokinetics of danofloxacin in pigeons following oral (PO), intramuscular (IM), and intravenous (IV) administration. The minimum inhibitory concentration (MIC) of danofloxacin was first determined for 38 clinical E. coli strains using the micro broth dilution method. Subsequently, 30 healthy pigeons were weighed and randomly divided into 3 groups: IM, IV, and PO, with 10 pigeons in each group. Danofloxacin was given at 5 mg/kg body weight (BW) through 3 different routes. Blood was collected, and plasma was separated at various time points from 0 to 48 h. Plasma samples were analyzed for danofloxacin concentrations using a validated HPLC method. Pharmacokinetic analysis was performed using Phoenix software and a noncompartmental analytical (NCA) method. The results indicated that danofloxacin had a strong antibacterial effect on E. coli, with a MIC50 of 0.5 μg/mL. The noncompartmental analysis showed that after PO and IM administration at 5 mg/kg in pigeons, peak plasma concentrations (Cmax) of 0.61 and 1.62 μg/mL were reached at 4.5 and 0.53 h, respectively. The oral and intramuscular bioavailability (F) were 68.08% ± 24.82% and 87.82% ± 25.36%, respectively. Following IV administration, danofloxacin was widely distributed in pigeons, with volume of distribution (VZ) and volume of distribution at steady state (VSS) values of 6.11 ± 2.01 and 4.65 ± 1.62 L/kg, respectively, and was eliminated slowly, with an elimination half-life (t1/2λz) of 6.41 ± 2.15 h. Based on the calculated ratio values of AUC/MIC, the current IV, IM, and PO doses of 5 mg/kg of danofloxacin would be expected to effectively treat pigeons infected with E. coli strains with MIC values equal to or less than 0.5 μg/mL.

Key words

danofloxacin
pigeons
in vitro antibacterial activity
pharmacokinetic
Escherichia coli
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pmcINTRODUCTION

Danofloxacin, a representative drug of the third-generation fluoroquinolones intended for veterinary use, is commonly available as methanesulfonate in clinical practice (Wang et al., 2022). Its mechanism of action involves exerting a bactericidal effect by inhibiting bacterial DNA gyrase, making it effective in treating bacterial diseases in cattle, swine, and poultry (Corum et al., 2019). Despite the growing global issue of antimicrobial resistance, fluoroquinolones continue to be extensively used to treat the microbial infections (Martinez et al., 2006). Compared to the earlier generations of fluoroquinolones, danofloxacin offers the benefits of high efficacy and low toxicity. Additionally, danofloxacin demonstrates significant antibacterial activity against most Gram-negative bacteria (such as E. coli), some Gram-positive bacteria, and mycoplasma, making it an ideal drug for treating bacterial infections in poultry (Chen et al., 2024).

The pigeon industry in China has experienced rapid growth in recent years, with pigeon meat now ranking as the country's fourth largest poultry product, behind chickens, ducks, and geese (Ji et al., 2022). China produces approximately 680 million pigeons annually, surpassing countries like Canada and the United States to become the world's leading producer of pigeon meat (Kokoszyński et al., 2020). However, the expansion of breeding operations has led to challenges such as poor ventilation and bacterial growth in pigeon lofts due to high-density breeding. These conditions can compromise the pigeons' immune system and increase the risk of bacterial diseases, with Salmonella, E. coli, and other pathogens being the main culprits (Harlin and Wade, 2009).

While pharmacokinetic studies on danofloxacin have been conducted in various poultry species such as chickens (Chen et al., 2023a), turkeys (Haritova et al., 2006), ducks (Xia et al., 2018), geese (Sartini et al., 2021), and quail (Dimitrova et al., 2014), data on pigeons is notably lacking. This gap could result in ineffective treatments, and developing an efficient treatment strategy for pigeons is a significant challenge. Therefore, this study aims to assess its antibacterial activity against pigeon-derived E. coli and to investigate the pharmacokinetics of danofloxacin in pigeons following a single oral, intravenous, and intramuscular dose of 5 mg/kg.

MATERIALS AND METHODS

Ethics Statement

Ethical approval for this experiment was obtained from the Institutional Animal Care and Use Committee (IACUC) of Henan University of Science and Technology (Approval No. 20240063), ensuring compliance with ethical standards and animal welfare regulations.

Chemical and Biological Reagents

Danofloxacin mesylate reference substance (Lot No. h0201210; purity 94.2%) was sourced from the China Institute of Veterinary Drug Control (Beijing, China). The raw material of danofloxacin mesylate (Lot No. 201217-1; purity 93.06%) was generously provided by Zhejiang Guobang Pharmaceutical Co., Ltd. (Hangzhou, China). Phosphoric acid (H3PO4) and triethylamine were acquired from Shanghai Eon Chemical Technology Co., Ltd. (Shanghai, China). Chromatography-grade methanol and acetonitrile were procured from Shanghai Maclean Biochemical Technology Co., Ltd. (Shanghai, China). Additionally, 0.9% sodium chloride injection was obtained from Anhui Fengyuan Pharmaceutical Co., Ltd. (Hefei, China), and pure water was sourced from China Resources Yibao Beverage Co., Ltd. (Shenzhen, China).

Organisms

In this study, 38 strains of E. coli were clinically isolated on March 17, 2024, from the cloaca of locally reared pigeons in Luoyang. Identification was performed using Gram staining and 16S rDNA-specific primer polymerase chain reaction (PCR). The quality control strain, E. coli ATCC 25922, was supplied by the Pharmacology Laboratory of Henan University of Science and Technology (Luoyang, China). Luria Bertani (LB) broth medium and Mueller-Hinton (MHB) broth medium were obtained from Beijing Aoboxing Biotechnology Co., Ltd. (Beijing, China).

Minimum Inhibitory Concentration Assays

According to the guidelines of the Clinical and Laboratory Standards Institute (CLSI, 2023), the minimum inhibitory concentration (MIC) of danofloxacin against pigeon-origin E. coli was determined using the microbroth dilution method. Briefly, the 38 isolated strains of E. coli were each cultured in 3 mL of LB medium at 37°C for 12 h overnight with shaking. After that, 100 μL of the overnight culture was aspirated into 3 mL of MHB medium and incubated at 37°C with shaking again for 4 h. At this time, the bacteria were in the logarithmic growth phase, and then the bacteria were adjusted to reach 0.5 McFarland Standard using MHB medium. Danofloxacin was added to the A1 to H1 wells in the first column of a 96-well plate and serially diluted twofold across the subsequent columns up to the 9th column. The initial concentration of danofloxacin in the first column was set at 64 μg/mL. The bacterial solution was diluted to a concentration of 1×106 CFU/mL and added to the wells of the 96-well plate. Negative control wells (200 μL MHB medium) and positive control wells (100 μL MHB medium + 100 μL bacterial solution) were included for each strain. The 96-well plates were incubated in a constant temperature incubator at 37°C for 20 h, after which the results were observed. The MIC value of danofloxacin was determined as the lowest concentration at which no bacterial growth was observed by the naked eye. Three replications were set up for all strains.

Animal Grouping and Sample Collection

Thirty 7-wk-old healthy meat pigeons (15 male and 15 female) were purchased from a commercial farm in the suburbs of Luoyang City for the experiment. Prior to the experiment, the pigeons were housed in 3 iron cages (60 × 60 × 60 cm), with 10 pigeons per cage. During the adaptation period, the pigeons had free access to water and were fed twice daily, in the morning and evening, with feed that did not contain any antibiotics to prevent external interference. The environment was maintained at a temperature of 25 ± 2°C, with appropriate humidity and ventilation.

Thirty pigeons were weighed and randomly divided into 3 groups: intramuscular (IM), intravenous (IV), and orally administered (PO), with 10 pigeons in each group (5 males and 5 females per group). Danofloxacin mesylate was diluted into a 5 mg/mL solution using 0.9% sodium chloride injection. In the IM group, the drug was injected into the left pectoral muscle at a dose of 5 mg/kg body weight (BW). Blood samples were collected from both sides of the inferior vein at specific time points: 10, 30 min, 1, 1.5, 2, 4, 6, 8, 12, 24, 36, and 48 h. In the PO group, danofloxacin was administered orally at 5 mg/kg BW by garage. Blood samples were collected from both sides of the inferior vein at the same time points as the IM group. In the IV group, the drug was administered by intravenous injection into the left inferior vein at a dose of 5 mg/kg BW. Blood samples were collected from the opposite side of the vein at predetermined time points: 5, 15, and 30 min, 1, 2, 4, 6, 8, 12, 24, 36, and 48 h. For all 3 routes of administration, approximately 0.5 mL of blood was collected at each time point in 1.5 mL centrifuge tubes prewashed with sodium heparin solution. The samples were then centrifuged at 4,000 × g for 10 min to obtain plasma, and all plasma samples were stored at -20°C until assayed.

Plasma Sample Analysis

A previously validated HPLC assay method for chicken plasma (Wang et al., 2022) was adapted with slight modifications to determine the concentration of danofloxacin in pigeon plasma. Briefly, 100 μL of plasma was mixed with 200 μL of acetonitrile and vortexed vigorously for 3 min. The mixture was then centrifuged at 12,000 × g for 10 min. The supernatant was collected into clean 10 mL test tubes, and the extraction was repeated twice. The combined supernatants were evaporated to dryness under nitrogen at 50°C. The residue was reconstituted with 400 μL of mobile phase, vortexed for 1 min, and filtered through a 0.22 μm filter membrane. Finally, 20 μL of the prepared sample was injected into the HPLC system for detection.

For danofloxacin determination, we employed a Waters e2695 high-performance liquid chromatography system coupled with a 2,475 fluorescence detector and Empower software for peak area integration and data acquisition. Separation was performed using a Hypersil BDS C18 column (4.6 mm × 250 mm, 5 μm, Elite Analytical Instruments Co., Ltd.; Dalian, China) maintained at 30°C. The injection volume was 20 μL, and the mobile phase comprised 0.05 mol/L phosphate buffer (pH 2.7, adjusted with triethylamine) and acetonitrile (83:17, V/V). The detection time was 15 min, with an excitation wavelength of 280 nm and an emission wavelength of 450 nm. The flow rate was set at 1 mL/min. Danofloxacin mesylate standard was dissolved in methanol to yield a 500 μg/mL stock solution, subsequently diluted with the mobile phase to generate standard working solutions, promptly prepared and utilized. A standard curve was constructed using plasma samples spiked with various concentrations (0.005–5 μg/mL) of standard working solutions. To assess assay precision and accuracy, 3 replicates at 3 concentrations (0.01, 0.5, and 5 μg/mL) were analyzed over 3 d to determine coefficients of variation and recoveries, respectively. Limits of detection (LOD) and quantification (LOQ) were established based on signal-to-noise ratios (S/N) of ≥3 and ≥10, respectively.

Data Analysis

The concentration-time data of danofloxacin in each pigeon plasma were analyzed using the noncompartment model analysis (NCA) method in Phoenix WinNonLin software (Version 8.1; Pharsight, Cary, NC) to obtain pharmacokinetic parameters. For all routes of administration, the first-order rate constant associated with the terminal phase (λz) was calculated using linear regression. From this, the terminal half-life (t1/2λz) was determined as ln2/λz. The area under the drug concentration-time curve (AUC0-∞) and the first-order moment curve (AUMC0-∞) were calculated using the linear trapezoidal method and extrapolated to infinity. The mean residence time (MRT) was determined as the ratio of AUMC0-∞ to AUC0-∞. After IV administration, the initial concentration (C0) was estimated using the back-extrapolation method. Total body clearance (Cl) was calculated as the ratio of intravenous dose to AUC. The steady-state volume of distribution (VSS) was calculated as VSS = MRTIV × Cl, and the volume of distribution (VZ) was calculated as Dose/AUC/λz. After PO and IM administration, the peak concentration (Cmax) and the time to reach peak (Tmax) were directly observed from the experimental data. Absolute bioavailability (F) was calculated as the ratio of AUCPO/IM to AUCIV.

The normality of pharmacokinetic parameters was tested using the Kolmogorov-Smirnov test in SPSS software (version 26.0; IBM, Armonk, NY). Results indicated that AUMC and λz did not follow a normal distribution. Consequently, these 2 parameters were analyzed using the Kruskal-Wallis 1-way ANOVA (k-sample) nonparametric test, while the remaining parameters were evaluated using an independent samples t-test. The effect of gender on each drug administration group was also investigated. Parameters are expressed as arithmetic mean ± SD, and a P-value of <0.05 was considered statistically significant.

RESULTS AND DISCUSSION

In vitro Antibacterial Activity

We explored the in vitro antibacterial activity of danofloxacin against 38 pigeon-origin E. coli strains. Figure 1 presents the MIC values of danofloxacin for each E. coli strain. The MIC susceptibility ranged from 0.125 to 64 μg/mL. The MIC of danofloxacin against the standard E. coli strain, ATCC 25922, was 0.125 μg/mL, and the MIC50 for the pigeon-origin E. coli was 0.5 μg/mL, demonstrating a strong antibacterial effect.Figure 1 MIC (μg/mL) distribution of danofloxacin against 38 pigeon-origin Escherichia coli strains isolated on March 17, 2024, from the cloaca of locally reared pigeons in Luoyang, and the orange band represents the MIC50 value.

Figure 1

To date, there have been no reports on the MIC data of danofloxacin against pigeon-origin E. coli. Reported MIC values of danofloxacin against E. coli in different bird species are as follows: 0.03 to 0.5 μg/mL in chickens (Zhang et al., 2021; Geornaras et al., 2001; Ozawa et al., 2010; Chen et al., 2024), and 0.25 μg/mL in quail (Haritova et al., 2013).

Assay Validation

The analytical method established in this experiment showed good linearity in the concentration range of 0.005 to 5 μg/mL, with a linear equation of Y = 1E-08X + 0.003 (where X is the peak area of danofloxacin in the chromatogram and Y is the calculated concentration of danofloxacin), and an R² value of 0.999. The recoveries of danofloxacin ranged from 86.66% to 99.90%, with intraday coefficients of variation between 0.09% and 7.45% and interday coefficients of variation between 1.28% and 4.16%. The LOD and LOQ were 0.001 μg/mL and 0.005 μg/mL, respectively.

Pharmacokinetics

During the experiment, the pigeons did not show any adverse reactions such as stress or loss of appetite. The average drug concentration-time curves of danofloxacin in pigeons after administration by the 3 routes of administration are shown in Figure 2, and the main pharmacokinetic parameters are shown in Table 1.Figure 2 Mean ± SD plasma concentrations (μg/mL) of danofloxacin in pigeons following oral (PO; n = 10), intramuscular (IM; n = 10), and intravenous (IV; n = 10) administration at a single dose of 5 mg/kg BW.

Figure 2

Table 1 Pharmacokinetics parameters (mean ± SD) of danofloxacin in pigeons after oral (PO; n =10), intramuscular (IM; n =10), and intravenous (IV; n =10) administration at a single dose of 5 mg/kg BW.

Table 1Parameters	Unit	PO	IM	IV	
λz	1/h	0.11 ± 0.06a	0.1 ± 0.04a	0.13 ± 0.07a	
t1/2λz	h	7.82 ± 3.3a	7.66 ± 2.84a	6.41 ± 2.15a	
AUC0-∞	h·μg/mL	5.24 ± 1.91b	6.76 ± 1.95ab	7.7 ± 1.77a	
AUMC0-∞	h2·μg/mL	50.24 ± 26.51a	44.23 ± 29.18a	55.85 ± 29.25a	
MRT	h	9.09 ± 2.13a	6.04 ± 2.15b	7.02 ± 2.34b	
VZ	L/kg	NA	NA	6.11 ± 2.01	
VSS	L/kg	NA	NA	4.65 ± 1.62	
C0	μg/mL	NA	NA	2.52 ± 0.7	
Cl	L/h/kg	NA	NA	0.68 ± 0.14	
Tmax	h	4.5 ± 1.83a	0.53 ± 0.18b	NA	
Cmax	μg/mL	0.61 ± 0.18a	1.62 ± 0.24b	NA	
F	%	68.08 ± 24.82a	87.82 ± 25.36a	NA	
In the same row, values marked with different superscript letters indicate significant differences (P < 0.05).

Abbreviations: AUC0-∞, the area under the drug concentration-time curve from the time of administration to infinity; AUMC0-∞, the area under first-order moment curve from administration to infinity; C0, initial concentration after intravenous injection; Cl, total body clearance; Cmax, peak concentration; F, absolute bioavailability; MRT, mean residence time; NA, not available; t1/2λz, terminal half-life; Tmax, the time to reach peak concentration; VSS, steady-state volume of distribution; VZ, volume of distribution; λz, the first-order rate constant associated with the terminal phase.

To our knowledge, this is the first report of pharmacokinetics study of danofloxacin in pigeons. Pharmacokinetic parameters among the 3 groups (PO, IM, and IV) were not statistically significant (P > 0.05) except for AUC-POvsIV, MRT-POvsIM/IV, Tmax-POvsIM, and Cmax-POvsIM. In the PO group, the Tmax and Cmax were 4.5 ± 1.83 h and 0.61 ± 0.18 μg/mL, respectively, which were significantly different (P < 0.05) when compared with those in the IM group (Tmax of 0.53 ± 0.18 h and Cmax of 1.62 ± 0.24 μg/mL, respectively). In addition, the bioavailability for PO and IM routes was calculated as 68.08 ± 24.82% and 87.82 ± 25.36%, respectively, with no significant difference observed. The results suggest that danofloxacin was absorbed more rapidly and to a greater extent after intramuscular injection, in comparison to oral administration.

We also analyzed the pharmacokinetic parameters of danofloxacin in male and female pigeons under the 3 administration routes. The results showed that in both the PO and IV groups, there were no gender effects on any of the pharmacokinetic parameters. However, in the IM group, the Cmax values in females were significantly higher than those in males. The reasons for this gender difference in IM Cmax remain unclear. It is possible that variations in body composition between the sexes, such as differences in fat distribution and muscle mass, may influence the absorption and distribution of danofloxacin.

The Cmax (0.61 μg/mL) observed in pigeons after PO dosing was consistent with that reported in Gushi chicken (0.53 μg/mL, Chen et al., 2023b) and Lingnan yellow broiler chicken (0.51 μg/mL, Zeng et al., 2011). However, it is lower than the PO Cmax observed in geese (0.96 μg/mL, Sartini et al., 2021) and Muscovy ducks (0.81 μg/mL, Goudah and Mouneir, 2009), despite the same oral dose of 5 mg/kg being administered in all these studies. The Tmax in pigeons was also much later than in the other species mentioned (4 h for Gushi chickens, 2.33 h for Lingnan yellow broiler chickens, 1.7 h for geese, and 1.21 h for Muscovy ducks). After IM administration in pigeons, danofloxacin was rapidly absorbed into the bloodstream, reaching a peak concentration of 1.62 ± 0.24 μg/mL at 0.53 h. A similar early Tmax (0.5 h) was observed in partridges (Orhan et al., 2018) and geese (Corum et al., 2022). Statistical results showed significant differences in Cmax and Tmax between the IM and PO groups (P < 0.05). These results demonstrate that danofloxacin is absorbed more rapidly and completely after intramuscular injection compared to oral administration. The observed differences in peak time and peak concentration can be attributed to variations in poultry species and routes of administration. Different species may exhibit unique pharmacokinetic profiles due to differences in their physiology, metabolism, and absorption mechanisms.

Danofloxacin is incompletely absorbed in pigeons after oral administration, with a bioavailability of only 68.08 ± 24.82%. In contrast, the absorption after intramuscular administration was more complete, with a bioavailability of 87.82 ± 25.36%. These bioavailability values are lower than those previously reported for Muscovy ducks (89.26% ± 9.65% for PO and 103.21% ± 15.26% for IM, Goudah and Mouneir, 2009). However, the bioavailability in the PO group was higher than that in geese (57.68%, Corum et al., 2022) and partridges (47.62% ± 3.93%, Orhan et al., 2018). The IM bioavailability in pigeons was comparable to that in geese (87.99%, Corum et al., 2022) and partridges (86.33% ± 6.62%, Orhan et al., 2018). These findings suggest that IM administration of danofloxacin is more effective than PO administration in pigeons, consistent with observations in other poultry species such as geese (Corum et al., 2022), partridges (Orhan et al., 2018), and Muscovy ducks (Goudah and Mouneir, 2009).

In the present study, the t1/2λz of danofloxacin after PO, IM, and IV administration were 7.82 ± 3.3, 7.66 ± 2.84, and 6.41 ± 2.15 h, respectively. The t1/2λz values in the PO and IM groups were greater than those in the IV group, with no significant difference (P > 0.05). Similar results were observed in partridge (Orhan et al., 2018) at varying doses and the same 3 routes, with t1/2λz values of 9.44 ± 1.39, 10.16 ± 0.82, and 8.18 ± 0.22 h for PO, IM, and IV, respectively. Conversely, the other researchers found the opposite results (IM, PO < IV) in Muscovy ducks (Goudah and Mouneir, 2009), indicating that the dose and species influence the elimination process of danofloxacin, while the route of administration plays a lesser role in the process.

The study observed that after intravenous administration, danofloxacin exhibited wide distribution in pigeons, with VZ and VSS of 6.11±2.01 L/kg and 4.65±1.62 L/kg, respectively. Similar studies in nonlaying hens (Chen et al., 2023a), geese (Corum et al., 2022) and broiler chickens of the Lohmann breed (Knoll et al., 1999) reported VZ and VSS values ranging from 2.73 to 13.7 L/kg and 2.71 to 10.2 L/kg, respectively. These findings suggest that danofloxacin exhibits extensive tissue distribution across various poultry species following intravenous administration, likely due to its favorable bio-permeable membrane penetration and significant lipid solubility.

Danofloxacin, as a concentration-dependent antimicrobial drug (Zhang et al., 2017), exhibits antimicrobial activity closely related to AUC/MIC or Cmax/MIC ratios. A study in turkeys (Haritova et al., 2006) found that E. coli could be effectively eradicated with an AUC/MIC in plasma of >6.73 h. In this experiment, the AUC/MIC50 ratios for the PO, IM, and IV routes were 10.48, 13.52, and 15.4 h, respectively. The results showed that administering danofloxacin at 5 mg/kg BW was effective in eradicating E. coli with a MIC50 of 0.5 μg/mL, consistent with the findings of a previous study in broilers (Chen et al., 2024).

DISCLOSURES

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Fan Yang reports financial support was provided by the Foundation for the University Young Key Teacher Program of Henan Province. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

ACKNOWLEDGMENTS

This work was supported by funding from the Foundation for the University Young Key Teacher Program of Henan Province (no.2021GGJS044 ).

Ethical approval: All applicable international, national and institutional guidelines for the care and use of animals were followed. And the animal experimentation protocol adhered to the guidelines and approvals set forth by the Institutional Animal Care and Use Committee (IACUC) of Henan University of Science and Technology (approved # 20240063).
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