Antibiotic resistance profile of pathogenic enterobacteria strains isolated from some poultry farms in the Forécariah prefecture in the Republic of Guinea

 Corresponding author: Abdoulaye Makanéra Copyright © 2025 Author(s) retain the copyright of this article. This article is published under the terms of the Creative Commons Attribution License 4.0. Antibiotic resistance profile of pathogenic enterobacteria strains isolated from some poultry farms in the Forécariah prefecture in the Republic of Guinea Abdoulaye Djibril Diallo 1, Abdoulaye Makanéra 2, 3, *, Boubacar Sidy Sily Bah 1, Souleymane Diallo 1, Ramatoulaye Baldé 4, Mamadou Ciré Diallo 4, Ibrahima Sory Sané 4, Mamoudou Keita 4 and OuoOuo Balamou 4 1 Applied Research Laboratory in Natural Sciences (LARASCINA), Department of Biology, University of Kindia (UK), PO Box 212, Republic of Guinea. 2 Faculty of Health Sciences and Technology, Department of Medicine, Chair of Basic Sciences, Gamal Abdel Nasser University of Conakry, PO Box 1147, Republic of Guinea. 3 Biomedical Laboratory of the China-Guinea Friendship Hospital, Kipé, Cité des Médecins, Commune Ratoma 30, PO Box 710, Conakry, Republic of Guinea. 4 Institute of Applied Biology Research of Guinea (IRBAG), PO Box 146, Commune/Kindia, Republic of Guinea. GSC Advanced Research and Reviews, 2025, 24(03), 201-209 Publication history: Received on 08 August 2025; revised on 15 September 2025; accepted on 18 September 2025 Article DOI: https://doi.org/10.30574/gscarr.2025.24.3.0279 Abstract Introduction: Escherichia coli and Salmonella spp. are among the Enterobacteria responsible for human and animal diseases causing considerable economic losses in the poultry sector. The uncontrolled use of antibiotics in poultry farming often leads to the selection of antibiotic-resistant bacterial germs and a decrease in productivity. Objectives: This study, conducted from July to September 2024, aimed to determine the prevalence and antibiotic resistance of pathogenic Enterobacteriaceae strains isolated from poultry farms in Forécariah prefecture. Material and Methods: A total of 119 samples were collected from 5 breeding sites. Enterobacteriaceae strains were isolated using standard microbiology methods and confirmed by the Api 20 E gallery. Antibiotic resistance was determined using the agar diffusion method. Results: Enterobacteriaceae contamination was detected in 75.79% of fresh droppings samples and in 79.16% of cloacal swabs. The results of antibiotic resistance showed that: 100% of the pathogenic Enterobacteriaceae tested were resistant to at least one antibiotic: Escherichia coli strains were resistant to 92.86% to Gentamicin, 77.27% to Ampicillin and 42.86% to Azithromycin. Similarly, Salmonella spp. were 100% resistant to Gentamicin, 75% to Ampicillin and Nitrofurantoin. Furthermore, this study highlighted the presence of five genera of Enterobacteriaceae in the Forécariah prefecture. Although the most pathogenic ones are underestimated, it is necessary to strengthen biosecurity measures to stem the spread of these pathogens. Keywords: Resistance; Antibiotics; Pathogenic Enterobacteriaceae; Poultry farms; Forécariah 1. Introduction Poultry farming is the animal production sector that has experienced the most remarkable growth in recent decades. Production costs and product prices have contributed to making poultry the preferred meat for producers and consumers worldwide, particularly in developing countries [1]. GSC Advanced Research and Reviews, 2025, 24(03), 201-209 202 However, this sector faces challenges that are hampering its development. These include the hygienic quality of the water used to water exotic chickens, unfair competition from imported poultry meat, and pathological problems [2,3]. These pathologies, often of bacterial, viral, and parasitic origin, remain ever-present. Among the bacterial species that contaminate meat, some are known to be extremely pathogenic, and their presence makes the food unsafe, such as Salmonella, and those that are tolerated at very specific thresholds, such as Escherichia coli [1]. The presence of these germs in poultry products, including meat, eggs, and their derivatives, has often made them unsafe for human consumption [4,5]. This leads to gastrointestinal illnesses in humans and animals worldwide. In Europe, it is estimated that 25,000 deaths are due to infection with multidrug-resistant bacteria (MDR) each year. This cost is €1.5 billion per year [6]. Colibacillosis and salmonellosis are zoonotic diseases caused by Salmonella and Escherichia coli, which currently represent one of the most significant causes of economic losses in the poultry sector and a major concern for the food industry [7]. To counter the spread of these pathogens, poultry farmers resort to the overuse or inappropriate use of antibiotics as a cure or preventative measure to increase their production profitability and meet consumer demand. This inappropriate use of antibiotics can lead to the selection of resistant pathogenic bacteria [8]. In low-income countries, the cost of these antibiotics most often falls on patients, as there are few or no effective health insurance or social security systems [9]. This practice contributes to the emergence and spread of antibiotic-resistant or multi-resistant bacteria, leading to serious risks to human health. In West Africa, bacterial diseases of avian origin, particularly colibacillosis and salmonellosis, are frequently diagnosed in many countries such as Côte d'Ivoire, Senegal, and Mali [10-12]. In the Republic of Guinea, very little reliable statistical data are available on the prevalence and antibiotic resistance of these strains in poultry farms, particularly in the Forécariah prefecture. It is therefore clear that a better understanding of this issue could allow the implementation of a dynamic approach to the preservation of animal and human health in the Forécariah prefecture. The objective of this study was to determine the prevalence and resistance of pathogenic Enterobacteriaceae strains isolated from poultry farms in the Forécariah prefecture. 2. Material and methods 2.1. Presentation of the Study Area Forécariah is a prefecture within the administrative region of Kindia and plays an important role due to its geographical location (straddling the capital, Conakry, and the Republic of Sierra Leone). Forécariah Prefecture is located 99 km from Conakry between 9° 26′ 05″ N latitude and 13° 05′ 07″ W longitude. It is bordered by Coyah Prefecture to the north, the Republic of Sierra Leone to the south, Kindia Prefecture to the east, and the Atlantic Ocean to the west. It covers an area of approximately 4,187 km² with a population of approximately 259,573 inhabitants in 2016, or 62 inhabitants/km² [13]. It is crossed by the river of the same name which is a tributary of the Mellacorée and plays an important role in the life of the prefecture, particularly for agriculture, livestock farming and fishing. The climate in this area is sub-Guinean, with temperatures ranging from 21°C to 37°C and alternating seasons (rainy and dry). This seasonal variation favors the development of agriculture and livestock farming. Agriculture is dominated by the production of rice, peanuts, cassava, and pineapples, most of which are managed by groups/cooperatives that play an important role in the local economy. GSC Advanced Research and Reviews, 2025, 24(03), 201-209 203 Livestock farming, particularly poultry farming, is characterized by a strong presence of farms in the peri-urban area, which were significantly impacted by the avian flu epidemic in 2022. Despite certain challenging constraints, these two sectors are major providers of employment and income for approximately 70% of the working population [14]. The Institute of Applied Biology Research of Guinea (IRBAG), which served as our study framework, is located 6km northwest of the urban commune of Kindia. It consists of a management, a doctoral school and six scientific departments (Virology, Epidemiological Clinic, Medical Zoology, Venereology, Food Hygiene, Environment and Bacteriology). 2.2. Sampling This cross-sectional study was conducted from July to September 2024. The aim was to collect and analyze samples from the visited poultry farms in the laboratory. The study was conducted between July and September 2024 on a sample of five (05) laying hen farms located in the peri-urban areas of Forécariah. The selection of these farms was based on the owners' consent to cooperate during the study. Two visits were conducted to each farm: the first to identify the site and raise awareness, and the second to collect samples. The biological materials consisted of fresh droppings and cloacal swabs. 2.3. Transport The samples were transported in a cooler containing ice packs (dry ice) at 4°C and transported to the laboratory for analysis or storage within 4 hours, in accordance with ISO 15189 [15]. 2.4. Methods A total of 119 samples, including 95 fresh droppings and 24 cloacal swabs, were collected from five (05) private poultry farms between July and September 2024, with the following distribution by farm (Table 1). Table 1 Distribution of samples according to poultry farms Sampling sites Poultry Farm Codes Types of samples Fresh droppings (Y) Cloacal swabs (Z) Forecariah Center F1 20 7 F2 17 0 Maferinyah F3 22 7 Alassoyah F4 21 10 F5 15 0 Total 5 95 24 Legend: Y: Number of fresh droppings collected; Z: Number of cloacal swabs collected As shown in Table I, in farms F1 to F5, the droppings and swabs collected were as follows, respectively: • 37 and 7 for the two farms in Forécariah Centre; • 22 and 7 for the Maferinyah farm alone; • 36 and 10 for the two farms in Alassoyah. During the sampling, approximately 20g of fresh droppings were collected from one-third of the total surface area of the building and then placed in a sterile tube containing approximately 5ml of sterile distilled water. Cloacal swabs were also taken from laying hens showing suspicious clinical signs (diarrhea, anorexia, oral discharge, etc.) and which were not in the laying phase. All of these samples were placed in a cooler equipped with dry ice to maintain the temperature around 4°C and then transported within a period not exceeding 4 hours. Upon arrival, the samples were then refrigerated and processed the following day. Each batch of samples collected from the same farm was accompanied by a tracking sheet including the operator's name, the sampling date, the age and number of birds per flock, and any signs of disease. GSC Advanced Research and Reviews, 2025, 24(03), 201-209 204 2.4.1. Bacteriological Analysis Samples of organic products collected from the Forécariah poultry farms underwent bacteriological analysis. This analysis was carried out at the Medical Bacteriology Laboratory of the Guinean Institute for Applied Biology Research (IRBAG). Isolation and Characterization The isolation of Enterobacteriaceae was carried out according to the Enterobacteriaceae research protocol applied at the IRBAG bacteriology laboratory, inspired by the French standard NF U 47-101 (2007), which includes 3 steps: • Step 1: Pre-enrichment (for all Enterobacteriaceae): After cauterizing the surface, 1g of droppings was immersed in 9ml of buffered peptone water (BPPW) and homogenized using a V-32 Vortex Mixer for 1 minute, then each swab was dipped in buffered peptone water. All homogenates were left for revitalization at room temperature for 30 minutes and then incubated at 37°C for 18 to 20 hours. • Step 2: Enrichment (for Salmonella only) The next day, after revival, 1 ml of each type from the pre-enrichment is transferred for enrichment into 20 ml of Rappaport-Vassiliadis (RVs) broth and then incubated at 37°C for 18 to 24 hours. • Step 3: Isolation The next day, after homogenization, 0.1 ml of each suspension was inoculated onto a Hecktoen agar plate for Salmonella and a MacConkey agar plate for other Enterobacteriaceae, then incubated at 37°C for 18 to 24 hours. Biochemical Identification The biochemical identification of Enterobacteriaceae was carried out in two media: o -Kligler-Hajna agar Kligler medium was used to identify the Enterobacteriaceae present in the analyzed sample by rapidly demonstrating the fermentation of lactose and glucose (with or without gas production) as well as the production of hydrogen sulfide. Using a loop, one to two colonies characteristic of Salmonella spp. and/or Escherichia coli were collected from previously inoculated Petri dishes and subcultured into Kligler-Hajna slant tubes, incubated at 37°C for 18 to 24 hours. Typical cultures of Escherichia coli and/or Salmonella spp. corresponded to an alkaline slant (red) and an acidic pellet (yellow), with gas and hydrogen sulfide formation (blackening of the agar). API 20 E identification gallery After inoculation and incubation according to the manufacturer's recommendations, the reactions resulted in spontaneous color changes, revealed by the addition or absence of reagents. Reading was performed using APIWEB identification software (bio-Mérieux, France). For all these identification steps, incubation was performed at 37°C for 18 to 24 hours. Antibiograms The antibiogram was performed using the Mueller-Hinton agar diffusion method of antibiotic disks (bio-Mérieux). The results were interpreted according to the rules and recommendations of the Antibiogram Committee of the French Society of Microbiology (CA-SFM) [16]. Mueller-Hinton agar plates are flooded with bacterial suspensions scraped from GSC Advanced Research and Reviews, 2025, 24(03), 201-209 205 the slope of Kligler tubes, diluting the inoculum 1/1000, to obtain the equivalent of 106 CFU/ml. The reading was taken after 18 to 20 hours of incubation at 37°C. Inhibition zone diameters were measured, and the results were interpreted according to the criteria of the French Society of Microbiology's Antibiogram Committee. The following antibiotics were tested: Ampicillin (AMP10), Gentamicin (GN10), Trimethoprim/Sulfamethoxazole (SXT25), Ciprofloxacin (CIP5), Nitrofurantoin (F300), and Azithromycin (AZM30). 3. Results 3.1. Prevalence of Enterobacteriaceae contamination in Poultry Farms in Forécariah Table 2 Prevalence of Enterobacteriaceae contamination in droppings Isolated germs Number of cases Percentage (%) Escherichia coli 32 44.44 Citrobacter spp. 11 15.28 Proteus spp. 11 15.28 Serratia spp. 8 11.11 Enterobacter spp 5 6.94 Klebsiella spp 3 4.17 Salmonella spp. 2 2.78 Total 72 100 The microbiological study involved 95 droppings collected from five (05) semi-modern poultry farms in the Forécariah prefecture. Microbiological analysis of these droppings at the Bacteriology Laboratory of the Guinean Institute for Applied Biology Research (IRBAG) resulted in the isolation of 72 strains of Enterobacteriaceae. This represents 75.79% (72/95) of all Gram-negative bacteria isolated during the study period (Table 2). The majority of isolated germs were Escherichia coli (32 strains), followed by Citrobacter spp. and Proteus spp. (11 strains each), then Serratia spp. (8 strains), Enterobacter spp. (5 strains), Klebsiella spp. (3 strains), and Salmonella spp. (2 strains). Table 3 Prevalence of Enterobacteriaceae contamination in cloacal swabs Isolated germs Nomber of cases Percentage (%) Escherichia coli 9 47.37 Proteus spp. 4 21.05 Klebsiella spp. 3 15.79 Salmonella spp. 2 10.53 Enterobacter spp. 1 5.26 Total 19 100 A total of 24 cloacal swabs (Table 3) were collected during the surveys in three (03) poultry farms. Bacteriological analysis of these swabs allowed the isolation and identification of 19 strains of Enterobacteriaceae with a contamination prevalence of 79.16% (=19/24) for all Gram-negative bacteria. The proportion of isolated germs was as follows: Escherichia coli (47.37%), Proteus spp. (21.05%), Klebsiella spp. (15.79%), Salmonella spp. (10.53%), and Enterobacter spp. (5.26%). GSC Advanced Research and Reviews, 2025, 24(03), 201-209 206 3.2. Antibiotic Resistance Profile of Pathogenic Enterobacteriaceae Strains Due to their pathogenicity, particularly in poultry farms, two species were selected for testing against the six antibiotics mentioned above. These are Escherichia coli, which has been considered an opportunistic pathogen, and Salmonella spp., which remains the most pathogenic species in this family for poultry. Table 4 Frequency of Antibiotic Resistance in Escherichia coli Strains Poultry Farms Antibiotics (µg) AMP10 n (%) GN10 n (%) CIP5 n (%) F300 n (%) AZM30 n (%) SXT25 n (%) F1 (n=14) 14 (100) 13 (92.86) 3 (21.43) 1 (7.14) 5 (35.71) 14 (100) F2 (n=10) 8(80.00) 10 (100) 3 (70.00) 00 4 (40.00) 10 (100) F3 (n=4) 2 (50.00) 3 (75.00) 00 00 2 (50.00) 4 (100) F4 (n= 6) 3 (50.00) 3 (50.00) 1 (16.66) 1 (16.66) 1 (16.66) 6 (100) F5 (n=10) 7 (70.00) 8 (80.00) 4 (40.00) 00 6 (60.00) 10 (100) Total (n=44) 34 (77.27) 37 (84.10) 11 (25.00) 2 (4.76) 18 (42.86) 44 (100) Legend: AMP10: Ampicillin; GN10: Gentamicin; CIP5: Ciprofloxacin; F300: Nitrofurantoin; AZM30: Azithromycin; SXT25: Trimethoprim/Sulfamethoxazole. The results of the antibiograms of the present study carried out in Forécariah (Table 4) revealed that the majority of Escherichia coli strains were resistant to the following three antibiotics: Trimethoprim/Sulfamethoxazole (100% = 44/44), Gentamicin (84.10% = 37/44), and Ampicillin (77.27% = 34/44). In contrast, the resistance rate was average for Azithromycin (42.86%). However, the resistance rate was rather low to Ciprofloxacin (25% = 11/44) and Nitrofurantoin (4.76% = 2/44). Thus, of all the antibiotics tested on these Escherichia coli strains, Nitrofurantoin was the most active, followed by Ciprofloxacin. In other words, the sensitivity rate of Escherichia coli strains was 95.24%, and that of Ciprofloxacin was 75%. This indicates its preferred position among these two antibiotics in the treatment of severe infections in poultry farms in Forécariah. Table 5 Frequency of antibiotic resistance of Salmonella spp. strains Poultry farms Antibiotics (µg) AMP10 CN10 CIP5 F300 AZM30 SXT30 F4 (n= 2) 2 (100) 2 (100) 1 (50) 1 (50) 1 (50) 2 (100) F5 (n= 2) 1 (50) 2 (100) 0 0 0 2 (100) Total (n=4) 3 (75) 4(100) 1 (25) 1 (75) 1 (25) 4 (100) Legend: AMP10: Ampicillin; GN10: Gentamicin; CIP5: Ciprofloxacin; F300: Nitrofurantoin; AZM30: Azithromycin; SXT25: Trimethoprim/Sulfamethoxazole. In Table 5, Salmonella spp. strains isolated during this study showed varying resistance to the four antibiotics tested. Indeed, all Salmonella spp. strains (100%) were resistant to the combination of trimethoprim/sulfamethoxazole and gentamicin, while 75% of these strains were resistant to both ampicillin and nitrofurantoin (F300, 75%). In contrast, these strains of Salmonella spp., had a relatively low frequency of resistance (25%) to both Ciprofloxacin and Azithromycin. In other words, the sensitivity of these strains was 75% to both Ciprofloxacin and Azithromycin, suggesting that among the antibiotics tested, only these two antibiotics could be used in the treatment of infections caused by these strains of Salmonella spp. 4. Discussion The objective of this study was to assess the antibiotic resistance of pathogenic Enterobacteriaceae strains isolated from several poultry farms in the Forécariah prefecture. GSC Advanced Research and Reviews, 2025, 24(03), 201-209 207 The results of this study showed that the prevalence of Enterobacteriaceae contamination in Forécariah poultry farms varied depending on the nature and sampling areas. The isolation rates of Enterobacteriaceae were 75.79% (72/95) in droppings and 79.16% (=19/24) in cloacal swabs, for an overall rate of 76.47% (91/119) for avian samples. This contamination rate is higher than that obtained by Boutaiba in 2023 , which was 54.31% in western Algeria [7]. The results of our study also show that Escherichia coli is the most frequently isolated species among Enterobacteriaceae in poultry farms. Its prevalence is 44% in droppings and 47.37% in swabs. These rates are lower than those reported by Banameur in 2011 [17], which were 48.33% in the farms of Mostaganen, Mascara, Taret, Relizane, Chlef, and Tissemsilt (Algeria). The predominance of the Escherichia coli species in these types of samples may be due to its direct involvement in various infections and indirectly to colibacillary superinfections, as it is rarely a primary infection agent; it is rather an opportunistic bacterium [7,18]. On the other hand, Salmonella is the most important ubiquitous zoonotic pathogen in the Enterobacteriaceae family. It is present throughout the food chain, from farm to plate. Their direct involvement in foodborne illnesses, especially in poultry products, is often reported. In this study, the isolation rates in droppings and cloacal swabs were 2.78% and 10.53%, respectively. These rates are lower than those reported in many studies from other countries. Indeed, in 2013, Alloui et al. (2013) reported a rate of 50% in Algeria , while Bonny et al. (2011) reported a rate of 61.87% in Côte d'Ivoire [19,20]. In Cameroon, Piebeng et al. (2014) reported a rate of 78.46% of non-typhoidal Salmonella in a total of 65 birds (Gendarme Weavers) that had been captured and examined for microorganisms [21]. In Morocco, in the Meknes region, Abdellah and Fouzia reported a 24% incidence of Salmonella in chicken farming in 2016 [22]. Moreover, our results are higher than those reported in eastern Algeria by Elgroud in 2009 in the broiler and egg-laying sectors, with a frequency of positive Salmonella isolations of 1.66% and 0.68%, respectively. Antibiotic susceptibility testing of bacteria during this study revealed a very high rate of resistance of Escherichia coli strains to the Trimethoprim/Sulfamethoxazole combination. Indeed, all Escherichia coli strains (100%) were resistant to this antibiotic combination. They also had a high rate of resistance to Gentamicin (92.86%) and Ampicillin (77.27%), thus suggesting a high rate of multidrug resistance in these Escherichia coli strains. These results corroborate those mentioned in 2011 by Benameur [17] who showed a very high rate of Escherichia coli isolates (100% resistant to at least one antibiotic) as well as the multi-resistance of the isolates analyzed (96.51% of isolates multi-resistant to at least 2 different antibiotics and 92.20% to at least 3 antibiotics). Boutaiba Benkhlaouz M found during his work in 2023, results which showed that 90.34% of Escherichia coli strains were resistant to nalidixic acid and 86.89% of strains were resistant to tetracycline, while for ampicillin it was around 82.75%. An alarming rate of antibiotic resistance of Escherichia coli to a single antibiotic was revealed (100%), as well as for multiresistance (97.24% for at least 2 antibiotics and 95.86% for at least 3 antibiotics) [7]. On the other hand, Boutaiba BM in [7] revealed in his results that the resistance rate of Escherichia coli isolates to the Trimethoprim/Sulfamethoxazole combination was 56.25% and that of Ciprofloxacin was 81.25%. These data suggest that bacterial resistance to antibiotics depends on several factors, including the adaptive capacity of these bacteria. Analysis of the antibiotic resistance profile of Salmonella spp. strains showed 100% resistance to at least one antibiotic. The highest resistance rates were found for the combination of Trimethoprim/Sulfamethoxazole (100%), Gentamicin (100%), and Ampicillin (75%). These results are similar to those of Abba et al. in 2017, who reported in a similar study in Chad that the isolated Salmonella spp. strains showed complete resistance (100%) to Ampicillin, Erythromycin, and Imipenem. These authors also observed a 34.15% frequency of multidrug resistance in the bacterial strains studied. Many authors have found different resistance profiles for Salmonella spp. strains. For example, Sidibé et al., reported a frequency of resistance of Salmonella strains of 21.2% to Gentamicin, while Mzungu I et al. (2016) reported 100% resistance of Salmonella strains to Ampicillin[12,25]. finally, Lydia B. and Atika B (2022) reported a resistance rate of 50% of Salmonella strains to the combination Trimethoprim/Sulfamethoxazole [26]. GSC Advanced Research and Reviews, 2025, 24(03), 201-209 208 These different data show that the choice of antibiotics to be tested could vary depending on the authors; this difference could be explained by the level of antibiotic use which varies from one country to another. Our observation reveals that in poultry farms in Forécariah, the use of antibiotics is done in a haphazard manner (nonspecific treatment), which would favor the development and spread of multi-resistant bacteria. This same finding has been observed in other countries such as Chad and Cameroon [24,27]. Multidrug-resistant strains (resistant to three or more antibiotics) in the Forécariah prefecture have an overall prevalence of 58.33%. This rate is lower than that reported in Mali (69.96%) in the three peri-urban sites of Bamako [12]. 5. Conclusion During this study, five genera of Enterobacteriaceae were identified from 119 samples (95 droppings and 24 cloacal swabs) collected from five semi-modern poultry farms. It therefore seems essential to take appropriate measures to reduce contamination in laying hen farms and to appropriately use, in the event of contamination, the antibiotics that proved most active during this study. Looking ahead, we plan to expand the number of antibiotics tested on isolated organisms and conduct serological and molecular studies to determine the genetic underpinnings of these resistances and their modes of propagation in different bacterial populations in poultry farms in Guinea. Compliance with ethical standards Acknowledgments Thanks are extended to the Ministry of Higher Education, Scientific Research and Innovation of the Republic of Guinea for its funding support, as well as to the authorities at all levels that made this work possible. Disclosure of conflict of interest The authors declare no conflicts of interest. References [1] FAO. Poultry Sector Senegal. National Livestock Reviews of the FAO Animal Production and Health Division, 2014. No. 7. Rome, 70p. 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