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Multiple antimicrobial resistance indices of Staphylococcus aureus from the nares of goats and slaughterhouse attendants in Kampala city, Uganda– a cross sectional study

BMC Microbiology volume 25, Article number: 162 (2025) Cite this article

Abstract

The emergence of antimicrobial resistance (AMR) is a global menace to both public and animal health sectors with devastating effects in developing countries. Indiscriminate use of antibiotics in human health and livestock management contributes to development and rapid spread of AMR. Staphylococcus aureus is a major opportunistic zoonotic pathogen that colonises the skin and nostrils of human beings and animals and continues to develop antimicrobial resistance against different agents. The study aimed to determine multiple antibiotic resistance indices of S. aureus isolates from healthy domestic goats and slaughterhouse attendants in Kampala, Uganda.

Demographic characteristics of consenting slaughterhouse attendants and goat keepers were recorded through a questionnaire. Antibiotics use among slaughterhouse workers and domestic goats and skin infections in the past twelve months were recorded. Nasal swabs were collected from healthy domestic goats at household level (n = 378) and slaughterhouse attendants (n = 131). Isolates were obtained on mannitol salt agar (MSA) upon incubation at 35°C for 24 h. The Kirby-Bauer disc diffusion method was used to determine antimicrobial susceptibility to penicillin, gentamycin, erythromycin, tetracycline, ciprofloxacin, clindamycin, trimethoprim-sulfamethoxazole, linezolid, amoxicillin, ceftriaxone and cefoxitin. In this study, the participating slaughterhouse workers were predominantly male (79%) while does (90%) were the majority of the goats sampled. S. aureus carriage was 32% and 43% among slaughterhouse workers and goats, respectively. Methicillin resistant S. aureus carriage was 12% and 11% among slaughterhouse attendants and goats, respectively. There was a high level of exposure to antibiotics among S. aureus carriers (62%) and goats (41%) in the past one year, including use of critically important antimicrobials in human medicine for livestock disease management. Amoxicillin (17%) and ciprofloxacin (12%) were the most used antibiotics among the S. aureus carriers. Oxytetracycline (33%) and Penicillin-streptomycin combination (21%) were the most used antimicrobials in goat keeping. Close to a quarter of the human participants reported having suffered probable staphylococcal related infections like pustules in the previous months. With the exception of gentamycin and linezolid, all the S. aureus isolates from human nasal swabs were resistant to at least one of the antibiotics used. S. aureus isolates from goats’ nasal swabs were resistant to at least one of the antibiotics studied. The multiple antibiotic resistance (MAR) index of 41% of S. aureus isolates from slaughterhouse attendants was greater than 0.2 (mean = 0.2 ± 0.2, range 0.1 to 0.7). The MAR index of 22% of S. aureus isolates from goats was greater than 0.2 (mean = 0.2 ± 0.1, range = 0 to 0.7). The most frequent multidrug resistance (MDR) pattern was FOX, CIP, E, TE, SXT, CRO, and CD among S. aureus isolates from slaughterhouse attendants. The most frequent MDR patterns for the isolates from goats were E, TE, CRO, CD and TE, CRO, CD. Healthy domestic goats and slaughterhouse workers are carriers of multidrug resistant S. aureus strains in Kampala city.

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Introduction

The emergence of antimicrobial resistance (AMR) is a global menace to both public and animal health sectors, with devastating effects in low and middle income countries (LMICs) [1, 2]. Indiscriminate use of antibiotics in human health and livestock management is a key factor in the rapid development and spread of AMR [2, 3]. Improper use of antibiotics is rampant in livestock and human beings in LMICs [4]. Goats are Uganda’s second most important livestock after cattle considered the ‘poor man’s cow’ that is a basis of livelihood [5, 6]. There are about 17.4 million goats reared by about 3.3 million households [7]. In Uganda, goats provide meat, milk and skin and are also used to fulfil spiritual rituals [8]. In low and middle income countries (LMICs), goats are regarded as potential insurance against emergencies and settlement of dowry by households [9]. In Kampala, Uganda, family labour is used to keep goats on tiny plots of land. This is considered a worthwhile business with good returns on investment for smallholder farmers [7, 10].

Estimates of the national livestock census indicated 64,000 goats in Kampala mainly kept at family level in overcrowded settlements [7]. Overcrowding amidst livestock production increases the risk of contracting antimicrobial resistant pathogens including Staphylococcus aureus among humans and their animals [11]. Goat keeping is practiced through semi-intensive and tethering management systems in Kampala, Uganda [8]. Tethering is mostly at communal grazing sites where goats graze freely with cattle and sheep [8], and some grazing sites are in proximity to the abattoirs. Grazing mobility and trade-related-mobility (e.g., between farms, between farms and market, market and market, or markets and slaughterhouse, or farms and slaughterhouse) result in mixing of herds thus increased disease transmission [8, 12]. Animals are mostly herded or transported by vehicles, motorcycles, canoes, and bicycles from farm to farm or slaughterhouse or market. These mechanisms increase the risk of disease transmission at resting points, grazing sites and watering points within Kampala [13]. Animal movements between administrative sub-counties and districts require animal movement permits in Uganda [14]. However, the movement permits are not required during local movements in search for communal grazing land or watering points in Kampala.

S. aureus carriage among goats at abattoirs and slaughterhouse workers has been widely studied. The risk of contracting resistant zoonotic pathogens from livestock is high for workers at abattoirs, including S. aureus infections that result in bacteraemia, pustules and abscesses [15,16,17]. Slaughterhouse workers trade in livestock including goats, and their household rear goats in Kampala. Slaughterhouse workers can transmit livestock associated resistant pathogens to family, then communities and livestock. The affected animals share grazing sites and watering points with goats, sheep and cattle, and herd mixing increases disease transmission [12].

Staphylococcus aureus is an opportunistic pathogen that colonises the skin and nostrils of both humans and animals and its monitoring is crucial in the looming post antibiotic era [17, 18]. Goats are potential reservoirs for resistant staphylococcal transmission to slaughterhouse attendants, farmers and veterinarians [15, 16]. Slaughterhouse workers and farmers can also transmit S. aureus to livestock. It is probable that slaughterhouse workers continuously pick antibiotic resistant S. aureus from their workplace [17, 19, 20]. It could also be that goats in the community are reservoirs of resistant S. aureus strains that concentrate at the abattoirs at the time of slaughter.

S. aureus cripples the financial gains from goat keeping by causing antibiotic resistant infections [21]. In human populations, staphylococcal toxins lead to food poisoning, toxic shock and scalded skin syndromes [22]. S. aureus infection causes impetigo, septicaemia, orbital cellulitis, postoperative endophthalmitis, boils, staphylococcal pneumonia, breast abscesses, and erysipelas [22]. The antibiotics utilised to treat these infections comprise gentamicin, ceftriaxone, cloxacillin, erythromycin, vancomycin, chloramphenicol, ciprofloxacin and amoxicillin. However, antimicrobial resistance emerged, resulting in increased treatment costs, extended hospital stays and death [4]. According to a 2019 report, antimicrobial resistance (AMR) claimed over 7000 lives in Uganda within one year [23]. Staphylococcus aureus is the most prevalent Gram-positive organism reported in Uganda, with increasing antimicrobial resistance over the years [24]. According to a 2023 report on Uganda, S. aureus was associated with over 4000 deaths [24]. Colonisation with multi-drug resistant S. aureus has been previously reported in goats with paucity of data in Uganda, both at community level and the abattoirs [25, 26].

Uganda lacks both surveillance systems for AMR and biosecurity measures in animal production required to alleviate AMR [3]. There is indiscriminate use of antibiotics in the management of both human and livestock diseases in Uganda. This behaviour is propelled by poverty and access to antibiotics over-the-counter in the country [27]. There are a number of studies conducted to address S. aureus in Uganda. They focused on clinical isolates at regional referral hospitals and isolates from animal products, and they did not provide information about carriage of S. aureus by abattoir workers or goats. Using antimicrobial resistance patterns, we determined the multiple antibiotic resistance indices of S. aureus isolates from healthy domestic goats and slaughterhouse attendants in Kampala.

Materials and methods

Study site and period

The data for this cross-sectional study were collected between May 2023 and May 2024 from healthy domestic goats and slaughterhouse workers at sites A, B and C in Kampala, the capital city of Uganda in East Africa. Slaughterhouse sites A, B and C were in Kampala Central, Rubaga and Kawempe administrative divisions, respectively. The slaughterhouses receive goats from all city divisions of Kawempe, Nakawa, Central, Rubaga and Makindye, and from the rest of the country. The slaughterhouses are surrounded by overcrowded slums that also keep livestock. Movements in search for communal grazing land and watering points within the city do not require animal movement permits. Grazing mobility and trade-related-mobility result in mixing of herds. Households of slaughterhouse workers in Kampala are goat keepers, too.

Study design

A cross-sectional study was conducted. Participating households were selected by systematic sampling, with a random starting point selected for each one of the administrative parishes or villages in the five divisions of Kampala, the Capital city. The sample size of 384 households was estimated by using Danial’s sample size determination formula [28]. Every 10th household was selected to participate by providing an animal for sampling, except where the selected household had no goats and an adjacent one was selected. Kawempe, Nakawa, Central, Rubaga and Makindye city divisions had 18, 20, 10, 21 and 15 selected parishes, respectively. Purposive sampling was used to select slaughterhouse attendants and specifically to select households of consenting slaughterhouse workers who also kept goats. Purposive sampling was used to recruit the slaughterhouse sites.

Data collection instruments

Demographic characteristics of consenting slaughterhouse attendants were recorded through a developed questionnaire. The questionnaire was pretested in a different district and internal consistency was calculated using the Kuder and Richardson Formula 20 test [29] (ρ = 0.76). The characteristics recorded were sex, age, level of education and nature of work. The respondents were asked for use of antibiotics in the past three to twelve months, antibiotics used, and whether they had suffered any skin infections in the past 12 months.

Animal factors (e.g. body condition, sex) and the duration the goat had spent on the farm or household were recorded. The use of antibiotics on the herd or other livestock and frequency of use in the past seven to twelve months were recorded.

Nasal swab collection and transportation

Nasal swabs were collected from goats and slaughterhouse workers. The samples were obtained by gently inserting a sterile swab into one nostril until resistance was met. The swab was rotated 3–5 times against the wall of the nostril, allowed to sit for a few seconds, and then removed [30]. The procedure was repeated with the same swab used for the other nostril, which was kept in physiological saline (0.9% w/v) and transported on ice within 2 to 4 h. Goats’ nasal swabs that yielded S. aureus isolates were matched with household data from the questionnaire.

Detection of S.aureus

On arrival at Makerere University, College of Veterinary Medicine Microbiology Laboratory, the swabs were enriched with peptone water at 35–36°C for six hours. The swabs were transferred to inoculate mannitol salt agar (MSA) plates, which were subsequently incubated at 35–36°C for 24 h [31,32,33]. Yellow colonies were selected and Gram stained. The gram-positive staphylococci, catalase - and tube coagulase-positive isolates were presumed to be S.aureus strains. The tube coagulase test was conducted for 18–24 h with rabbit plasma (PRO-LAB diagnostics) via freshly prepared bacterial cultures.

Antimicrobial susceptibility testing and methicillin resistance detection

To determine antimicrobial susceptibility, 3–5 colonies of S. aureus isolates were collected from nutrient agar and suspended in brain heart infusion broth (0.5 ml). The suspension was then standardised to the turbidity of a 0.5 McFarland solution. Antimicrobial susceptibility testing was carried out via Kirby-Bauer disc diffusion method on Mueller - Hinton agar [34,35,36] according to the Clinical and Laboratory Standards Institute (CLSI) guidelines [37]. Aseptically, a cotton swab was immersed into a 0.5 McFarland adjusted suspension to inoculate Mueller - Hinton agar plates by streaking [36]. Antibiotic discs were aseptically dispensed on the surface of inoculated agar plates. The inoculated plates were incubated at 35–36°C for 24 h. The antibiotics discs included penicillin (10 U), gentamycin (10 µg), erythromycin (15 µg), tetracycline (30 µg), ciprofloxacin (5 µg), clindamycin (2 µg), trimethoprim-sulfamethoxazole (25 µg), linezolid (30 µg), amoxicillin (25 µg), and ceftriaxone (30 µg). Cefoxitin (30 µg) discs were used to establish methicillin resistance. The diameters of the zones of inhibition were measured and interpreted in accordance with Clinical and Laboratory Standards Institute guidelines [35, 38] and the European Committee on Antimicrobial Susceptibility Testing guidelines (Table 1). Staphylococcus aureus isolates that were cefoxitin resistant (< 22 mm) were presumed to be methicillin resistant strains. Quality control was achieved with methicillin susceptible Staphylococcus aureus-American Type Culture Collection (ATCC) 25,923 [39, 40] and methicillin resistant Staphylococcus aureus-ATCC 43,300.

Table 1 Zone diameter breakpoints for antibiotics according to international guidelines
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Data analysis

Data were entered in Microsoft Excel and percentages were generated. Multiple antimicrobial resistance indices (MARI) were determined.

Determination of multiple antibiotic resistance index (MARI)

Multiple antibiotic resistance indices were determined for each of the S. aureus isolates by dividing the number of resisted antibiotics (p) by the total number of antibiotics used (q) [43, 44]. MAR index values > 0.2 indicated a source with frequent exposure to antibiotics. MAR index ≤ 0.2 was attributed to a source with infrequent antimicrobial exposure [45].

Determination of multidrug resistance patterns of the isolates

In this study, multidrug resistance was described as non-susceptibility to three or more of the following antimicrobial agents selected from the respective antimicrobial categories: gentamicin an aminoglycoside, cefoxitin a cephamycin, ciprofloxacin a fluoroquinolone, Trimethoprim– sulphamethoxazole a folate pathway inhibition, clindamycin a lincosamide, erythromycin a macrolide, linezolid an oxazolidone, or tetracycline [46, 47]. MRSA predicts non-susceptibility to beta-lactam antibiotics and cephamycins, therefore, MRSA isolates were considered MDR [48].

Results

Demographic information of the slaughterhouse attendants and S. aureus carriage

One hundred thirty-one consenting slaughterhouse attendants (male = 79%, female = 21%) provided nasal swab samples for identification of S. aureus. The overall nasal carriage of S. aureus among abattoir workers was 32% (n = 42/131) at the three slaughterhouses. The disaggregated S. aureus carriage by slaughterhouse and sex of the participants is indicated (Table 2). The S. aureus carriage rates for site A, B and C were 32% (n = 19/59), 39% (n = 16/41) and 23% (n = 7/31), respectively.

Table 2 Demographic characteristics of the slaughterhouse workers, n = 131
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Demographic information of the goats in the study and S. aureus carriage

Three hundred seventy-eight households in five divisions of Kampala provided 378 goats free of apparent disease for nasal swab sampling. The household response rate was 98% (n = 378/386). One hundred sixty-three S. aureus isolates were obtained from 17 bucks and 146 does from the respective households. The body condition scores were 1.5, 2, 2.5, 3 and 3.5 for 4, 31, 67, 51 and 10 goats, respectively. The households had kept the goats for at least 6 months. The goats’ nasal carriage rate of S. aureus was 43% (n = 163/378).

Antimicrobials use among slaughterhouse attendants

62% (n = 26/42) of S. aureus carriers reported use of antibiotics in the past three to twelve months. At site A, thirteen male (n = 13/19, 68%) and two female (n = 2/19, 11%) participants had used antimicrobials in the past 3–12 months. One female (n = 1/16, 6%) and eight male (n = 8/16, 50%) participants at site B had used the antibiotics in the stated period. At site C, one female (n = 1/7, 14%) and two male (n = 2/7, 29%) participants had used antibiotics in the past 3–12 months’ period. The antibiotics used by the participants at each site are indicated (Table 3) with amoxicillin (n = 7/42, 17%) and ciprofloxacin (n = 5/42, 12%) as the most frequently recorded antibiotics.

Table 3 Antibiotics used by slaughterhouse attendants at the three slaughterhouses
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Close to a quarter (n = 10/42) of the S. aureus carriers had suffered pustules, skin abscesses or boils in the past twelve months. The ten participants (24%, n = 10/42) who experienced abscesses or boils also reported use of at least a commonly used class of antibiotics in the previous months.

Antimicrobials use among goats in the past seven to twelve months

Sixty-seven goats (41%, n = 67/163) had received antibiotics in the past seven to twelve months’ period. The antibiotics reported were amoxicillin (human formulation, 3%, n = 2/67), ampicillin (1.5%, n = 1/67), ampicillin-cloxacillin combination (Ampiclox, human antibiotics, 1.5%, n = 1/67), gentamycin and doxycycline (1.5%, n = 1/67), oxytetracycline (31%, n = 21/67), penicillin and streptomycin combination (Penstrep, 19%, n = 13/67), sodium sulphonamides (1.5%, n = 1/67), tetracycline (6%, n = 4/67), Trimethoprim - Sulfadiazine combination (3%, n = 2/67), Tylosin (5%, n = 3/67), and unknown antibiotics administered (n = 2, 3%, n = 2/67) in suspected bacterial infections. Twelve respondents (18%, n = 12/67) were unaware of the antibiotics the veterinarians or para-veterinarians had administered. Four households (6%, n = 4/67) did not state the antibiotics used. The most reported antibiotics with the corresponding diseases or conditions managed in goats are indicated (Table 4) with oxytetracycline (33%, n = 21/63) and penicillin-streptomycin combination (21%, n = 13/63) as most frequently used.

Table 4 Diseases and conditions in goats managed with antibiotics as reported by the participants n = 63
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Forty-two goats (26%, n = 42/163) had received antibiotics once in the past seven to twelve months, while 12%, (n = 19/163) and 3% (n = 4/163) were given antibiotics twice and thrice in the same period, respectively. Of the households that had administered antibiotics to goats, 36% (n = 24/67) had also given antibiotics to other animals under their care. The other antimicrobials that had been used on other livestock in these households were metronidazole (1.5%, n = 1/65), neomycin (1.5%, n = 1/65), oxytetracycline (17%, n = 11/65), penicillin-streptomycin combination (Penstrep, 11%, 7/65), streptomycin (2%, n = 1/65) Tylosin (3%, n = 2/65), amoxicillin (a human antibiotic, 6%, n = 4/65), chloramphenicol (1.5%, n = 1/65), Trimethoprim-sulfamethoxazole (Septrin, 1.5%, 1/65) and ampicillin (1.5%, 1/65).

Ninety-seven households had not administered antibiotics to goats but had used them on other animals under their care in the past seven to twelve months. 27% (n = 26/97) of the households with untreated goats had used antimicrobial agents on other livestock under their care in the same period. The other antimicrobials administered to the other livestock in that period were enrofloxacin (2%, n = 2/97), gentamycin– doxycycline combined (1%, n = 1/97), metronidazole (1%, n = 1/97), oxytetracycline (19%, n = 18/97), penicillin-streptomycin (Penstrep, 2%, n = 2/97), Tetracycline (1%, n = 1/97) and Tylosin (4%, n = 4/97), amoxicillin a human antibiotic (2%, n = 2/97), chloramphenicol (2%, n = 2/97), Ciprofloxacin (human formulation, n = 1, 1%, n = 1/97), Trimethoprim-sulfamethoxazole (Septrin, 1%, n = 1/97) and combined multivitamins with Colistin sulphate, Oxytetracycline, Erythromycin thiocyanate and streptomycin sulfate (n = 1, 1%, n = 1/97).

Antibiotic resistance in S. aureus isolates from human nasal swabs S. aureus isolates were resistant to amoxicillin (12%, n = 5/42), ciprofloxacin (19%, n = 8/42), ceftriaxone (2.4%, n = 1/42), clindamycin (19%, n = 8/42), erythromycin (33%, n = 14/42), cefoxitin (12%, n = 5/42), penicillin–G (98%, n = 41/42), co-trimoxazole (43%, n = 18/42) and tetracycline (29%, n = 12/42). Gentamycin and linezolid resistance was not observed. We detected intermediate susceptibility to ciprofloxacin, gentamycin, ceftriaxone, clindamycin, erythromycin and tetracycline (Fig. 1; Table 5). Cefoxitin resistance was used as a marker of methicillin resistance in S. aureus. 12% of the isolates (n = 5/42) from human nasal swabs were phenotypically methicillin - resistant S. aureus (MRSA).

Fig. 1
figure 1

Antimicrobial resistance patterns of S. aureus isolates from human nasal swabs

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Table 5 Antimicrobial resistance patterns and rates of resistance
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One participant (2%, n = 1/42) with a co-trimoxazole - resistant isolate had also taken the antibiotic in the past three to twelve months’ period. Similarly, two participants (5%, n = 2/42) had used ciprofloxacin and presented with resistant strains. There were no strains reported with resistance to erythromycin among participants who had also used the antibiotics in the past three - twelve months’ period.

Antibiotic resistance among S. aureus isolates from goats’ nasal swabs S. aureus isolates were resistant to amoxicillin (0.6%, n = 1/163), ciprofloxacin (2.5%, n = 4/163), gentamycin (0.6%, n = 1/163), ceftriaxone (5.5%, n = 9/163), clindamycin (3%, n = 5/163), erythromycin (16%, n = 26/163), cefoxitin (11%, n = 18/163), linezolid (3%, n = 5/163), penicillin–G (80%, n = 131/163), co-trimoxazole (15%, n = 25/163) and tetracycline (39%, n = 63/163). We detected intermediate susceptibility to amoxicillin, ciprofloxacin, gentamycin, ceftriaxone, clindamycin, erythromycin, cotrimoxazole and tetracycline. Cefoxitin resistance was used as a marker of methicillin resistance in S. aureus. 11% (n = 18/163) of the isolates from goats’ nostrils were methicillin - resistant S. aureus (Fig. 2; Table 5).

Fig. 2
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Antimicrobial resistance patterns of S. aureus isolates from goats’ nostrils

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Multiple antibiotics resistance index (MARI) of S. aureus isolates from human nasal swabs

Approximately 41% (n = 17/42) of S. aureus isolates from nasal swabs of slaughterhouse attendants had MARI > 0.2 (Table 6). The mean MARI of S. aureus isolates from human nasal swabs was 0.2 ± 0.2. The highest MARI was 0.7 identified from site A while the lowest index was 0.1 from the different sites A, B and C, respectively (Table 7). One slaughterhouse attendant at site A provided a nasal swab sample (MARI = 0.3) and also accepted to provide another from a buck at the household.

Table 6 Distribution of S. aureus isolates with MARI value > 0.2 among human beings n = 17
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Table 7 MAR indices of S. aureus isolates from human beings’ Nares n = 42
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Multiple antibiotic resistance index (MARI) for S. aureus isolates from goats

MAR indices of 23% (n = 38/163) of the S. aureus isolates were > 0.2 while 77% (n = 125/163) had MARI ≤ 0.2. The mean MAR index was 0.2 ± 0.1. The highest MAR index was 0.7, and the lowest was zero, indicating isolates that were susceptible to all antibiotics used (Table 8). MAR indices of 21% (n = 34/163) of the isolates from does and 3% (n = 4/163) of isolates from bucks were greater than 0.2. MARI of 20% (n = 32/163) of the isolates from goats that had received antimicrobial treatment in the past seven to twelve months were greater than 0.2. 4% (n = 6/163) of the S. aureus isolates had not received antibiotics in the past seven to twelve months and had MARI > 0.2.

Table 8 MAR indices of S. aureus isolates from goats’ nasal swabs n = 163
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A goat with MAR index of 0.4 had received antibiotics more than three times in the past twelve months’ period. 2% (n = 3/131) of the slaughterhouse attendants accepted to provide goat nasal swab samples at their respective households, and were S. aureus carriers, too. MAR indices of two S. aureus isolates from goats in households of slaughterhouse workers were > 0.2 while other isolates had MARI = 0.2. 1% (n = 2/163) of the S. aureus isolates with MARI > 0.2 were from goats that had been treated with oxytetracycline against respiratory illnesses and injuries in the past seven to twelve months, respectively. One of the two isolates with MARI > 0.2 was obtained from a buck in a household that had treated the other livestock with streptomycin in the past seven to twelve months. However, the oxytetracycline and streptomycin used were not recommended by veterinarians.

Multidrug resistance (MDR) among S. aureus isolates from human nasal swabs

Multidrug resistance was noted in 38% (n = 16/42) of the S. aureus isolates from slaughterhouse attendants (Table 9). S. aureus isolates that resisted three or more antimicrobial categories were regarded multidrug-resistant strains [47]. All MRSA isolates were MDR where resistance to cefoxitin was applied to predict non-susceptibility to all categories of beta-lactam antimicrobials [47]. Thirteen antibiotics resistance patterns were observed against the ten antimicrobials tested. Resistance to FOX, CIP, E, TE, SXT, CRO, CD was the most frequent MDR pattern (n = 4/16, 25%) among S. aureus isolates from slaughterhouse attendants. Another frequently observed MDR pattern was CIP, SXT, CD (3/16, 19%) (Table 9).

Table 9 Multidrug resistance patterns of S. aureus isolates from slaughterhouse attendants n = 16
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Twenty one percent (n = 9/42) of the abattoir workers presented with multidrug-resistant S. aureus strains and had used antibiotics in the past three to twelve months (Table 9). 7% (n = 3/42) of the human participants had suffered from pustules, abscesses or boils in the past three to twelve months and presented with multidrug resistant strains (Table 9).

Seventeen percent (n = 63/378) of the respondents mentioned abscesses, brucellosis, diarrhoea, eye infections, fever, footrot, infection, wound management, nasal discharge, post-abortion care, prevention of disease, respiratory illnesses and mastitis as the situations under which they administered antimicrobials like amoxicillin, ampicillin, ampicillin-cloxacillin combination, gentamycin-doxycycline combination, oxytetracycline, penicillin-streptomycin combination, sodium sulphonamides, tetracycline and trimethoprim– sulfadiazine to the goats in their households in the past twelve months (Table 4).

Multidrug resistance (MDR) patterns among S. aureus isolates from goats

Multidrug resistance was noted in 29% (n = 47/163) of the S. aureus isolates from goats (Table 10). S. aureus isolates that resisted three or more antimicrobial categories were regarded MDR strains (Table 10). Thirty-one multidrug resistance patterns were observed for S. aureus against nine antibiotics tested. Resistance to E, TE, CRO, CD pattern and TE, CRO, CD pattern was most frequent (11%, n = 5/47) for the MDR S. aureus isolates from goats (Table 10).

Table 10 Multidrug resistance (MDR) patterns in S. aureusisolates from goats n = 47
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Discussion

Asymptomatic carriage of S. aureus among human beings is a risk factor for localised and invasive infections when the protective barriers are broken or during immunodeficiency [49, 50]. This study found high carriage of S. aureus among slaughterhouse workers and healthy domestic goats in Kampala, the capital city. Gender disparity was skewed towards male slaughterhouse participants (79%) consistent with a previous report [51] probably caused by cultural determinants of gender roles at the study sites in Kampala. Nasal carriage of S. aureus was 32% among slaughterhouse workers. The carriage rate in this study is consistent with a previous report of 29.7% among animal handlers in Nigeria [52] and the 36.7% among healthy livestock keepers in Kamuli and Isingiro, Uganda [53]. The high S. aureus carriage rate is associated with occupational exposure at slaughterhouses, and probably spreads through poor hand-to-nose behaviour and hygiene practices [54]. The nasal carriage of S. aureus among slaughterhouse workers in this study was higher than the 22.9% carriage among patients at Mbale Regional Referral Hospital in Uganda [55] and the 28.8% at Kampala International Teaching Hospital among healthcare providers [56]. The higher S. aureus carriage rate in this study is probably a result of the increased risk associated with occupational exposure among abattoir workers.

This study recorded an average goats’ body condition score of 2.5 indicative of healthy animals [57]. Nasal carriage of S. aureus among livestock is a reservoir for human infection [58]. In this study, nasal carriage of S. aureus was 43% among healthy domestic goats, consistent with a previous study in Chongqing [59]. A previous study recorded 25% carriage of S. aureus in goats, however, a small sample size of goats was used [60]. The 18% carriage of S. aureus from goats’ nasal swabs in a previous study in Abeokuta, Nigeria [61], was lower than the carriage in this study. However, the 82.7% in a previous study in Iraq was higher than the S. aureus carriage by healthy domestic goats in this study [62]. The variation in S. aureus carriage might be attributed to differences in farm management practices in the different regions. Poor farm management practices increase transmission and nasal colonisation of S. aureus in livestock [63]. The high nasal carriage of S. aureus by slaughterhouse workers and healthy domestic goats in Kampala are suggestive of poor personal or workplace hygiene practices and improper farm management practices, respectively.

Goat-to-human transmission of MRSA has been previously reported as a risk factor for colonisation in animal handlers [64] and further spread to family members [65]. This study found 12% MRSA carriage among slaughterhouse attendants, consistent with findings in Maiduguri, Nigeria (13.5%) [52]. The present results differ from another study in Italy that found MRSA carriage of only 7.3% for a similar occupation [20]. The previous reports of 39.2% [66] and 51% [67] MRSA carriage in animal handlers in Tanzania and India, respectively, were higher than the 12% in this study. The deviation in MRSA carriage might be attributed to differences in hygiene practices during animal handling and variation in restrictions on use of antibiotics [68].

Livestock associated MRSA (LA-MRSA) colonises and infects human beings [69]. The index case transmits LA-MRSA to livestock and family members [65] within households or farms. MRSA is clinically considered multidrug resistant, and its spread limits the therapeutic options available in the management of human and livestock infections. The current study revealed nasal carriage of MRSA of 11% in healthy domestic goats, lower than the 55% in a previous report in India [67]. A previous report in Sweden found zero carriage of MRSA by the goats [70]. The differences in nasal carriage of MRSA might be attributed to differences in antibiotics exposure in different settings [68, 71].

In this study, both S. aureus carriers (62%) and goats (41%) had exposure to antibiotics in the past one year. S. aureus carriers reported use of either amoxicillin, ampicillin - cloxacillin combination, azithromycin, ciprofloxacin, doxycycline, erythromycin or co-trimoxazole in the past three to twelve months. Frequent antibiotics use in this study is consistent with the findings of a previous study in urban, rural and peri-urban settings in Uganda [72]. In the current study, the goats had received either gentamycin-doxycycline combination, oxytetracycline, penicillin-streptomycin combination, sulphonamides, tetracycline, tylosin or other antibiotics administered by veterinarians or para-veterinarians within the past seven to twelve months. The antibiotics reported in this study were mostly over-the-counter drugs, consistent with a previous report in Uganda [73]. The current study recorded use of human antibiotics like co-trimoxazole, amoxicillin and ampicillin - cloxacillin combination and ciprofloxacin in livestock. A previous report of utilisation of human antibiotics in livestock in Uganda, Tanzania and India [74] was consistent with this study. One small holder farmer (1%) reported use of Colistin sulphate in goat keeping. Polymyxins like colistin are last resort antibiotics categorised under Highest Priority Critically Important Antimicrobials (HPCIA) recommended for critically ill patients in intensive care units [75]. Misuse and overuse of polymyxins compromises the management of antimicrobial resistance in critical care.

S. aureus carriers (25%) reported having suffered staphylococcal related infections like pustules, skin abscesses or boils in the past twelve months. The present study is in agreement with previous reports of staphylococcal infections in Uganda [24, 76]. 24% (24%) of the S. aureus carriers had used over-the-counter antibiotics in the same period, consistent with a previous report of unlimited access to most antibiotics in Uganda [27]. The infections and antibiotics misuse in the current study are similar to previous reports in Uganda, since the population characteristics in terms of sickness and antibiotics use are comparable. The level of infections among S. aureus carriers in this study are in agreement with the occupational hazards reported previously [77, 78] when sharp tools like knives and bare hands are used to remove goatskin. The high rate of antibiotics exposure might be contributing to the spread of antibiotic resistant S. aureus strains observed in this study.

This study observed antibiotic resistance against amoxicillin, cefoxitin, ceftriaxone, ciprofloxacin, clindamycin, penicillin-G, tetracycline and cotrimoxazole among S. aureus isolates from both slaughterhouse workers and healthy domestic goats. The resistance pattern among isolates from slaughterhouse workers is in agreement with previous reports in Busia, Kenya [19] and Ethiopia [79]. In the present study, cefoxitin, ciprofloxacin, cotrimoxazole and erythromycin resistance were lower than those of the previous report in Busia, Kenya [19]. Erythromycin resistance in S. aureus is determined by transposon551 [80]. This study found erythromycin resistance among S. aureus isolates from human beings and goats. The development of antibiotic resistance, in this study, could be a result of either horizontal gene transfer that occurs between animal and human strains [81] or the resistant S. aureus strains are from a common ancestry. Erythromycin is considered a critically important antimicrobial in human medicine [75]. Zoonotic transmission of erythromycin resistant S. aureus to humans compromises the use of macrolides [82]. The review by [2] found amoxicillin, ciprofloxacin and gentamycin resistance in S. aureus from livestock at 4.8, 6.5 and 5.2% that are higher than the resistance in this study, respectively. According to the review [2], tetracycline and penicillin resistance were lower than reported in the present study. In Uganda tetracycline, penicillin and amoxicillin (human formulation) among other antibiotics are frequently used through self-medication in livestock as indicated in this study, and this might be accelerating resistance against these antibiotics. In this study, gentamycin and linezolid resistance occurred among S. aureus isolates from goats and not the abattoir workers. Gentamycin resistance was absent or reported at very low percentages in previous reports in Uganda [19, 53]. Gentamycin is not dispensed over-the-counter [83] or used by unlicensed drug shop operators in Uganda [27]. Therefore, gentamycin resistance is expected to be low due to limited antibiotic exposure in the community. A previous report in Busia, Kenya found linezolid resistance among abattoir workers [19] in contrast to our findings that identified this resistance in five isolates from goats, one of which was MRSA. Linezolid is an oxazolidinone that inhibits protein synthesis in sensitive S. aureus and other bacteria. In case of zoonotic or human-to-human transmission of linezolid resistant strains, MRSA management becomes complicated [84]. Low levels of linezolid resistance have been previously reported in Uganda in clinical settings and communities, and this might be attributed to linezolid being one of the antibiotics that have just been introduced into the country [85]. Linezolid is a prescription antibiotic in Uganda, mostly in multidrug– resistant tuberculosis (MDRTB) [83] and therefore S. aureus in this population is less exposed to the antibiotic.

The present study found remarkable penicillin resistance in S. aureus from both human beings (98%) and goats (80%). Our findings are in agreement with previous reports among slaughterhouse attendants in Kenya [19] and Ethiopia [79], and among livestock keepers [53] and clinical samples in Uganda [86] and Romania [87]. Penicillin resistance might be attributed to maintenance of antibiotics selection pressure in humans and livestock and intrinsic resistance in the presence of β-lactamase or altered penicillin-binding proteins that is well documented from the time penicillin was introduced in the 1940s [88, 89]. Cefoxitin is resistant to β-lactamase hydrolysis that enables S. aureus to inactivate penicillin and cephalosporin– like antibiotics. Penicillin-binding protein (PBP2a), a restructured protein, confers methicillin resistance to S. aureus. This study found 12% cefoxitin resistance among isolates from both goats and abattoir workers, respectively. In the present study, cefoxitin resistance is in agreement with the 11% reported in South Africa [90] but higher than the 6% reported among goats in Korea [58] and the 2% reported in Uganda [91], although less than the 48.7% reported among HIV/AIDS outpatients in Uganda [92]. Our findings indicate increasing circulation of either community– associated or livestock– associated MRSA or both that might be attributed to the widespread use of antibiotics in livestock and humans as reported by the participants in this study. Healthy goats carrying antibiotic resistant S. aureus can transmit the strains to slaughterhouse workers and vice versa, and these spread further into families and communities.

Ceftriaxone is a therapeutic option recommended against methicillin susceptible S. aureus [83] in Uganda, and accordingly it is prescribed for surgical prophylaxis [93], staphylococcal bronchitis, severe cellulitis and septicaemia [83]. However, inappropriate prescription and missed doses or failure to complete the dose have been previously reported in Uganda [93, 94]. In this study, we found ceftriaxone resistance in isolates from healthy domestic goats (5.5%) and slaughterhouse workers (2.4%), and also three of the isolates from goats were resistant to cefoxitin too (MRSA). Zoonotic transmission of resistant strains to human populations would complicate disease management from such infections. The present study reported ceftriaxone resistance in agreement with the 1.7% at a Kampala International University hospital in Uganda [95]. This study reported ceftriaxone resistance in S. aureus, lower than the 63.9% previously reported among goats and sheep in Addis Ababa [96]. Ceftriaxone overuse is limited, since it is not available over-the-counter in Uganda. The general population is less exposed to ceftriaxone since it is intramuscularly or intravenously administered, thus requires a professional health worker. This might be contributing to the reduced incidence of ceftriaxone resistance, as reported here. However, the health workers should adhere to proper prescription requirements as recommended by the clinical guidelines [83, 93].

MAR index indicates the organism’s previous exposure to antimicrobial agents [45] where MARI ≥ 0.2 shows the organism originates from a source contaminated by two or more antibiotics [97, 98]. 41% of S. aureus from nasal swabs of slaughterhouse attendants had MARI > 0.2 (mean = 0.2 ± 0.2, range 0.1 to 0.7). 22% of S. aureus from goats had MAR indices greater than 0.2 (mean = 0.2 ± 0.1, range = 0 to 0.7). MAR indices were greater than 0.2 in goats that had received antimicrobial treatment in the previous months and those that had not been treated in the same period. Two goats (1%) from slaughterhouse attendants’ households had MARI = 0.3, and had been exposed to oxytetracycline in the past one year without a veterinarian’s recommendation. Other livestock at the household of the slaughterhouse attendant had received antibiotics treatment in the past months. S. aureus from goats and slaughterhouse workers in this study are directly or indirectly exposed to antimicrobial agents. One of the bucks owned by a slaughterhouse worker had MAR index > 0.2. In Kampala, Uganda, households hire bucks for breeding purposes. The bucks breed randomly at communal grazing sites. This can spread diseases that are resistant to antibiotics. Cross– transmission of antibiotic resistant S. aureus strains should be avoided, probably through improved personal hygiene practices and improved livestock management practices at household level or goat farms in Kampala. In the present study, the most frequent multidrug resistance (MDR) pattern was FOX, CIP, E, TE, SXT, CRO, CD among S. aureus isolates from nasal swabs of slaughterhouse attendants. The most frequent MDR patterns were E, TE, CRO, CD and TE, CRO, CD among S. aureus isolates from goats. This study suggested that both goats and slaughterhouse workers in Kampala might spread multiple antibiotic resistant S. aureus strains.

Conclusion and recommendation

This study found high S. aureus carriage rates and high multidrug resistance rates among isolates from nasal swabs of abattoir attendants and healthy domestic goats in Kampala. There is a need to strengthen the monitoring of antimicrobial resistance (AMR) in the slaughterhouse environment to mitigate the associated risk to the workers in the study setting. Context-specific interventions are needed to reduce AMR emergence and spread in the slaughterhouse environment and the community.

Data availability

The original data presented for this research are openly available in FigShare at DOI https://doiorg.publicaciones.saludcastillayleon.es/10.6084/m9.figshare.26767771.

References

  1. Lushniak BD. Surgeon general’s perspectives. Public Health Rep. 2014;129(4):314–6.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Herawati O, Bejo SK, Zakaria Z, Ramanoon SZ. The global profile of antibiotic resistance in bacteria isolated from goats and sheep: A systematic review. Vet World. 2023;16(5):977–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. OMS, Tracking AMR. Country Self Assessment Survey (TrACSS) 2023 Country Report Mexico Tracking AMR Country Self Assessment Survey (TrACSS) 2023 Country Report. 2023;1–10.

  4. Gautam A. Antimicrobial resistance: the next probable pandemic. J Nepal Med Assoc. 2022;60(246):225–8.

    Article  Google Scholar 

  5. James H, Namayanja D, The SLM, Manual. Volume 2 final. 2017;2(July 2018). Available from: https://www.researchgate.net/publication/326156581

  6. Iqbal A, Khan BB, Tariq M, Mirza MA. Goat-a Potential Dairy Animal: Present and Future Prospects. Pakistan J agricuture Sci. 2008;45(2):227–30. Available from: https://agris.fao.org/agris-search/search.do?recordID=PK2009000399

  7. UBOS. National Livestock Census 2021 Abridged Version Uganda Bureau of Statistics the Republic of Uganda. 2024;(March). Available from: www.ubos.org

  8. Kabirizi JML. Climate Smart Technologies and Management Practices for a Profitable Goat Enterprise in Uganda. 2022;(July):1–89.

  9. Girma M. Production system of Indigenous goat population reared in pastoral and agro-pastoral districts of South Omo, Ethiopia. Int J Agric Res Innov Technol. 2023;13(1):51–9.

    Article  Google Scholar 

  10. Mwebe R, Ejobi F, Laker CD. Assessment of the economic viability of goat management systems in Goma sub County and Mukono town Council in Mukono district, Uganda. Trop Anim Health Prod. 2011;43(4):825–31.

    Article  PubMed  Google Scholar 

  11. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008;451(7181):990–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ekwem D, Morrison TA, Reeve R, Enright J, Buza J, Shirima G et al. Livestock movement informs the risk of disease spread in traditional production systems in East Africa. Sci Rep. 2021;11(1):1–13. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41598-021-95706-z

  13. Gordon LG, Porphyre T, Muwonge A, Nantima N, Ademun R, Ochwo S et al. Identifying target areas for risk– based surveillance and control of transboundary animal diseases: a seasonal analysis of slaughter and live– trade cattle movements in Uganda. Sci Rep. 2023;1–16. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41598-023-44518-4

  14. Uganda R. of. Preliminary 1. 2. 1971.

  15. Park S. Staphylococcus aureus in Agriculture: Lessons in Evolution from a Multispecies Pathogen. 2021;(February):1–27.

  16. Piva S, Mariella J, Cricca M, Giacometti F, Brunetti B, Mondo E et al. Epidemiologic case investigation on the zoonotic transmission of Staphylococcus aureus infection from goat to veterinarians. 2021;(March):684–90.

  17. Rao RT, Madhavan V, Kumar P, Muniraj G, Sivakumar N, Kannan J. Epidemiology and zoonotic potential of Livestock-associated Staphylococcus aureus isolated at Tamil Nadu, India. BMC Microbiol. 2023;23(1):1–12. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12866-023-03024-3

  18. Eiff V. Nasal carriage as a Sourc E of Sta ph Yloc Occ Us aureus bac Ter Emia nasal carriage as a source of Staphylococcus aureus bacteremia. Engl J. 2001;344(1):11–6.

    Article  Google Scholar 

  19. Obanda BA, Gibbons CL, Fèvre EM, Bebora L, Gitao G, Ogara W, et al. Multi-Drug resistant Staphylococcus aureus carriage in abattoir workers in Busia, Kenya. Antibiotics. 2022;11(12):1–14.

    Article  Google Scholar 

  20. Mascaro V, Leonetti M, Nobile CGA, Barbadoro P, Ponzio E, Recanatini C, et al. Prevalence of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) among farm and slaughterhouse workers in Italy. J Occup Environ Med. 2018;60(8):E416–25.

    Article  PubMed  Google Scholar 

  21. Mohamed M, Received. 10 August 2023 І Accepted: 12 November 2023. 2023;30(November):108–14.

  22. Health MOF. U ganda C linical G uidelines. 2016.

  23. Institute for Health Metrics and Evaluation. The burden of antimicrobial resistance (AMR) in Portugal. Inst Heal Metrics Eval. 2022;1–4. Available from: https://www.healthdata.org/sites/default/files/2023-09/Germany.pdf

  24. Saudah NK, Migisha R, Okello PE, Simbwa B, Kabami Z, Agaba B et al. Increasing trends of antibiotic resistance, Uganda: an analysis of National antimicrobial resistance surveillance data, 2018–2021. 2023;8(1):1–13.

  25. Titouche Y, Akkou M, Campaña-Burguet A, González-Azcona C, Djaoui Y, Mechoub D, et al. Phenotypic and genotypic characterization of Staphylococcus aureus isolated from nasal samples of healthy dairy goats in Algeria. Pathogens. 2024;13(5):408.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. A CL AINA, C ABSS b, A JL-F AMZ, Torres C. Comparative review of the nasal carriage and genetic characteristics of Staphylococcus aureus in healthy livestock: insight into zoonotic and anthroponotic clones. Infect Genet Evol. 2023;109.

  27. Nabaweesi I, Olum R, Sekite AB, Suubi WT, Nakiwunga P, Machali A, et al. Antibiotic practices, perceptions and self-medication among patients at a National referral hospital in Uganda. Infect Drug Resist. 2021;14:2155–64.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Danial W, Biostatistics. A foundation for analysis in the health sciences. 7th ed. New York: Wiley; 1999.

    Google Scholar 

  29. Kuder GF, Richardson MW. The theory of the estimation of test reliability. Test. 1937;2(3):151–60.

  30. Hart B, Tu YP, Jennings R, Verma P, Padgett LR, Rains D et al. A comparison of health care worker-collected foam and polyester nasal swabs in convalescent COVID-19 patients. PLoS One. 2020;15(10 October):1–10. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1371/journal.pone.0241100

  31. Koch FE. Electivnährboden Für Staphylokokken Zentr Bakt Parasitenk. 1942;122–4.

  32. Chapman GH. STAPHYLOCOCCI ’. 1945;7–9.

  33. Shields P, Tsang AY. Mannitol Salt Agar Plates Protocols. Am Soc Microbiol. 2006;6(13):3–5. Available from: https://asm.org/ASM/media/Protocol-Images/Mannitol-Salt-Agar-Plates-Protocols.pdf?ext=.pdf

  34. Bauer AW, Perry DM, Kirby WMM. Single-Disk antibiotic-Sensitivity testing of Staphylococci: an analysis of technique and results. AMA Arch Intern Med. 1959;104(2):208–16.

    Article  CAS  PubMed  Google Scholar 

  35. Barry AL. Standardization of antimicrobial susceptibility testing. Clin Lab Med. 1989;9(2):203–19. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/S0272-2712(18)30624-3

  36. Bauer AW, Kirby WMM, Sherris JCTM. Susceptibility Testing by a Standardized Single Disk Method,. Am J Clin Pathol. 1966;45(4):493–6. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1093/ajcp/45.4_ts.493

  37. Weinstein MP, Lewis JS. The clinical and laboratory standards Institute subcommittee on antimicrobial susceptibility testing: background, organization, functions, and processes. 58, J Clin Microbiol. 2020.

  38. (US) NC for CLS. Performance standards for antimicrobial disk susceptibility tests: approved standards. Natl Comm Clin Lab Stand; 2006.

  39. ATCC. Staphylococcus aureus subsp. aureus Rosenbach 25923. Available from: https://www.atcc.org/products/25923

  40. Treangen TJ, Maybank RA, Enke S, Friss MB, Diviak LF, David DK, et al. Complete genome sequence of the quality control strain Staphylococcus Aureus subsp. Aureus ATCC 25923. Genome Announc. 2014;2(6):25923.

    Article  Google Scholar 

  41. EUCAST. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 14.0, 2024. Http://Www.Eucast.Org 2024;077. Available from: http://www.eucast.org

  42. Committee TE, Testing AS, Changes N, Pseudomonas E. European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_50_Breakpoint_Table_01.pdf. 2015;0–77. Available from: http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_5.0_Breakpoint_Table_01.pdf

  43. P.H K. Multiple antibiotic resistance indexing of Escherichia coli to identify High-Risk sources of fecal contamination of foods. Appl Enviromental Microbiol. 1983;165–70.

  44. Titilawo Y, Sibanda T, Obi L, Okoh A. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of faecal contamination of water. Environ Sci Pollut Res. 2015;22(14):10969–80.

    Article  CAS  Google Scholar 

  45. Thenmozhi S, Rajeswari P, Suresh Kumar T, Saipriyanga VK. Multi-drug resistant patterns of biofilm forming Aeromonas hydrophila from urine samples. Int J Pharm Sci Res. 2014;5(7):2908–18.

    Google Scholar 

  46. Liliana Serweci´nska. Antimicrobials and Antibiotic-Resistant Bacteria: Water. 2020;12:3313–30.

  47. Sweeney MT, Lubbers BV, Schwarz S, Watts JL. Applying definitions for multidrug resistance, extensive drug resistance and pandrug resistance to clinically significant livestock and companion animal bacterial pathogens. J Antimicrob Chemother. 2018;73(6):1460–3.

    Article  CAS  PubMed  Google Scholar 

  48. Magiorakos A, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG et al. bacteria: an international expert proposal for interim standard definitions for acquired resistance. 2011.

  49. Wertheim HFL, Melles DC, Vos MC, Van Leeuwen W, Van Belkum A, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751–62.

    Article  PubMed  Google Scholar 

  50. Park B, Liu GY. Staphylococcus aureus and hyper-ige syndrome. Int J Mol Sci. 2020;21(23):1–12.

    Article  CAS  Google Scholar 

  51. Nielsen KJ, Hansen CD, Bloksgaard L, Christensen AD, Jensen SQ, Kyed M. The impact of masculinity on safety oversights, safety priority and safety violations in two male-dominated occupations. Saf Sci. 2015;76:82–9. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ssci.2015.02.021

  52. Gulani IA, Geidam YA, Adamu LH, Lawal JR, Abadam F, Gulani IA, Geidam YA, Adamu LH, Lawal JR, Abadam FA. (2016). Prevalence and phenotypic detection of methicillin resistance Staphylococcus aureus between ruminants butchered for humanoid intake and animal handlers in Maiduguri, Nigeria. J Adv Vet Anim Res. 2016;3:152–9.

  53. Kungu JM, Tegule SS, Awke IA, Namayanja J, Namyalo E, Oposhia J et al. Antimicrobial susceptibility profiles of Staphylococcus aureus in cattle and humans in farming communities of Isingiro and Kamuli districts, Uganda. Sci Rep. 2024;14(1):1–9. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1038/s41598-024-52035-1

  54. Zarazaga M, Gómez P, Ceballos S, Torres C. Molecular Epidemiology of Staphylococcus aureus Lineages in the Animal-Human Interface. Staphylococcus Aureus. Elsevier Inc.; 2017. 189–214 p. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/B978-0-12-809671-0.00010-3

  55. Thembo, N., Masifa, G., Kamugisha, G., Nabitaka, R., Akais, B., Olupot, P. O.,…Ampaire L. Methicillin Resistant Staphylococcus Aureus Nasal Carriage And Associated Factors In A Rural Tertiary Hospital In Eastern Uganda: A Prospective Crosssectional Study. 2020;1–2.

  56. Abimana JB, Kato CD, Bazira J. Methicillin-Resistant Staphylococcus aureus Nasal Colonization among Healthcare Workers at Kampala International University Teaching Hospital, Southwestern Uganda. Can J Infect Dis Med Microbiol. 2019;2019.

  57. Villaquiran M, Gipson T, Merkel R, Goetsch AL, Sahlu T. Body condition scores in goat. Goat F Day. 2017;(3):1–7.

  58. Mechesso AF, Moon DC, Ryoo GS, Song HJ, Chung HY, Kim SU et al. Resistance profiling and molecular characterization of Staphylococcus aureus isolated from goats in Korea. Int J Food Microbiol. 2021;336(September 2020):108901. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ijfoodmicro.2020.108901

  59. Zhou Z, Zhang M, Li H, Yang H, Li X, Song X, et al. Prevalence and molecular characterization of Staphylococcus aureus isolated from goats in Chongqing, China. BMC Vet Res. 2017;13(1):1–8.

    Article  CAS  Google Scholar 

  60. Rahimi H, Saei HD, Ahmadi M. Nasal carriage of Staphylococcus aureus: frequency and antibiotic resistance in healthy ruminants. Jundishapur J Microbiol. 2015;8(10):8–13.

    Article  Google Scholar 

  61. Omoshaba EO, Ojo OE, Oyekunle MA, Sonibare AO, Adebayo AO. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from Raw milk and nasal swabs of small ruminants in Abeokuta, Nigeria. Trop Anim Health Prod. 2020;52(5):2599–608.

    Article  CAS  PubMed  Google Scholar 

  62. Abdulrahman VAR. Detection and molecular characterization of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus (MRSA) nasal carriage isolates from healthy domestic animal in Duhok Province. Egypt J Vet Sci. 2023;54(2):263–73.

    Google Scholar 

  63. Exel CE, de Geus Y, Spaninks M, Koop G, Benedictus L. Colonization of extramammary sites with Mastitis-Associated S. aureus strains in dairy goats. Pathogens. 2023;12(4):1–8.

    Article  Google Scholar 

  64. Loncaric I, Brunthaler R, Spergser J. Suspected goat-to-human transmission of methicillin-resistant Staphylococcus aureus sequence type 398. J Clin Microbiol. 2013;51(5):1625–6.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Graveland H, Wagenaar JA, Bergs K, Heesterbeek H, Heederik D. Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE. 2011;6(2):1–7.

    Article  Google Scholar 

  66. Mlimbila J, Kafuru KD, Kishinhi SS, Shabani S, Nelson W, Mamuya S. Nasal colonization of methicillin resistant Staphylococcus aureus among slaughterhouse workers in Dar Es Salaam, Tanzania. Int J Fam Community Med. 2022;6(2):81–5.

    Article  Google Scholar 

  67. Venkatvasan R, Antony PX, Mukhopadhyay HK, Jayalakshmi V, Vivek Srinivas VM, Thanislass J et al. Characterization of methicillin - Resistant Staphylococcus aureus from goats and their relationship to goat handlers using multi-locus sequence typing (MLST). Small Rumin Res. 2020;186(July 2019):106097. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.smallrumres.2020.106097

  68. Wooten DA, Winston LG. Risk factors for methicillin-resistant Staphylococcus aureus in patients with community-onset and hospital-onset pneumonia. Respir Med. 2013;107(8):1266–70. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.rmed.2013.05.006

  69. Benito D, Lozano C, Rezusta A, Ferrer I, Vasquez MA, Ceballos S et al. Characterization of tetracycline and methicillin resistant Staphylococcus aureus strains in a Spanish hospital: Is livestock-contact a risk factor in infections caused by MRSA CC398? Int J Med Microbiol. 2014;304(8):1226–32. Available from: https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.ijmm.2014.09.004

  70. Persson Y, Börjesson S, Myrenås M, Pedersen K. No detection of Methicillin-Resistant Staphylococcus aureus in dairy goats. Dairy. 2021;2(1):65–70.

    Article  Google Scholar 

  71. Wardyn SE, Forshey BM, Farina SA, Kates AE, Nair R, Quick MK, et al. Swine farming is a risk factor for infection with and high prevalence of carriage of multidrug-resistant Staphylococcus aureus. Clin Infect Dis. 2015;61(1):59–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Nayiga S, Kayendeke M, Nabirye C, Willis LD, Chandler CIR, Staedke SG. Use of antibiotics to treat humans and animals in Uganda: A cross-sectional survey of households and farmers in rural, urban and peri-urban settings. JAC-Antimicrobial Resist. 2020;2(4):1–11.

    Article  Google Scholar 

  73. Kibooga C, Nakiyemba C, Asiimwe R. Antibiotic use in Uganda’s livestock-keeping households: prevalence, patterns, and determinants. Pastoralism. 2024;14(July):1–15.

    Google Scholar 

  74. Myers J, Hennessey M, Arnold JC, McCubbin KD, Lembo T, Mateus A et al. Crossover-Use of human antibiotics in livestock in agricultural communities: A qualitative Cross-Country comparison between Uganda, Tanzania and India. Antibiotics. 2022;11(10).

  75. Group WHOA, Surveillance I, Resistance A. WHO| WHO list of Critically Important Antimicrobials (CIA). Available from: http://www.who.int/foodborne_disease/resistance/cia/en/#.UiMEZ7zmSDA.mendeley

  76. Pius T, Irege R, Makeri D, Tamale A. Among patients with skin and soft tissue infections: A Cross-Sectional study at a tertiary hospital in Bushenyi, Western, Uganda. Open Access Libr J. 2023;10(5):1–12.

    Google Scholar 

  77. Mosoeu LG, Rathebe PC. Occupational Hazards and Health Risks Among Abattoir Workers: A Narrative Review. 2024;27(May):187–92.

  78. Abdullahi A, Hassan A, Kadarman N, Junaidu YM, Adeyemo OK, Lua PL. Occupational hazards among the abattoir workers associated with noncompliance to the meat processing and waste disposal laws in Malaysia. Risk Manag Healthc Policy. 2016;9:157–63.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Abunna F, Abriham T, Gizaw F, Beyene T, Staphylococcus. Isolation, identification and antimicrobial resistance in dairy cattle farms, municipal abattoir and personnel in and around Asella, Ethiopia. J Vet Sci Technol. 2016;07(06).

  80. Khan SA, Novick RP. Terminal nucleotide sequences of Tn551, a transposon specifying erythromycin resistance in Staphylococcus aureus: homology with Tn3. Top Catal. 1980;4(2):148–54.

    CAS  Google Scholar 

  81. Khan SA, Nawaz MS, Khan AA, Cerniglia CE. Transfer of erythromycin resistance from poultry to human clinical strains of Staphylococcus aureus. J Clin Microbiol. 2000;38(5):1832–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Miklasińska-Majdanik M. Mechanisms of resistance to macrolide antibiotics among Staphylococcus aureus. Antibiotics. 2021;10(11).

  83. Naunton M, Guidelines MOH, Moller MSFN, Health D, Guideline MOF. U Ganda C Linical G Uidelines. J Pharm Pract Res. 2012;5(2):374–9.

    Google Scholar 

  84. Metlay JP, Waterer GW, Long AC, Anzueto A, Brozek J, Crothers K, et al. Diagnosis and treatment of adults with community-acquired pneumonia. Am J Respir Crit Care Med. 2019;200(7):E45–67.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Liguori K, Keenum I, Davis BC, Calarco J, Milligan E, Harwood VJ et al. Antibiotic Resistance in Uganda: Situation Analysis and Recommendations. Environmental Science and Technology. 2022;56:1–94. Available from: www.ugandanationalacademy.org

  86. Busingye JC, Bazira J, Musinguzi B, Ssemakadde T, Nalumaga P, Mukundane B et al. Archives of clinical and medical microbiology prevalence of nasal carriage of methicillin resistant Staphylococcus aureus among patients, Health Care Workers and Patients ’ Care Takers at Kabale Regional Referral Hospital, South Western Uganda. 2(4).

  87. Tălăpan D, Sandu AM, Rafila A. Antimicrobial resistance of Staphylococcus aureus isolated between 2017 and 2022 from infections at a tertiary care hospital in Romania. Antibiotics. 2023;12(6).

  88. Spink WW, Hall WH, Ferris V. Clinical significance of Staphylococci: with natural or acquired resistance to the sulfonamides and to penicillin. J Am Med Assoc. 1945;128(8):555–9.

    Article  Google Scholar 

  89. Santajit S, Indrawattana N. Mechanisms of Antimicrobial Resistance in ESKAPE Pathogens. Biomed Res Int. 2016;2016.

  90. Ocloo R, Nyasinga J, Munshi Z, Hamdy A, Marciniak T, Soundararajan M et al. Epidemiology and antimicrobial resistance of Staphylococci other than Staphylococcus aureus from domestic animals and livestock in Africa: a systematic review. Front Vet Sci. 2022;9.

  91. Ikwap K, Gertzell E, Hansson I, Dahlin L, Selling K, Magnusson U, et al. The presence of antibiotic-resistant Staphylococcus spp. And Escherichia coli in smallholder pig farms in Uganda. BMC Vet Res. 2021;17(1):1–8.

    Article  Google Scholar 

  92. Ssenyonga B, Mwebaze S, Atuhairwe C, MugishaTaremwa I. Perspective for Methicillin-resistant Staphylococcus aureus colonization, antibiotic susceptibility patterns and risk factors for colonization among people living with HIV at Nyenga hospital, Buikwe district, in central Uganda. Int J Infect Prev. 2020;1(1):1–8.

    Article  Google Scholar 

  93. Kutyabami P, Munanura EI, Kalidi R, Balikuna S, Ndagire M, Kaggwa B et al. Evaluation of the clinical use of ceftriaxone among in-patients in selected health facilities in Uganda. Antibiotics. 2021;10(7).

  94. Kiguba R, Karamagi C, Bird SM. Extensive antibiotic prescription rate among hospitalized patients in Uganda: but with frequent missed-dose days. J Antimicrob Chemother. 2016;71(6):1697–706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Tirwomwe M, Onchweri AN, Miruka CO, Nalwoga J, Maniga JN, Nyaribo M et al. Drug Resistant Staphylococcus aureus in Clinical Samples at Kampala International University-teaching Hospital. Am J Biomed Res. 2016;4(4):94–8. Available from: http://pubs.sciepub.com/ajbr/4/4/3

  96. Tefera M, Aleme H, Girma S, Ali A, Gugsa G, Abera F, et al. Antimicrobial susceptibility pattern of S. aureus isolated from sheep and goat carcasses. Open Microbiol J. 2019;13(1):16–20.

    Article  CAS  Google Scholar 

  97. Sandhu R, Dahiya S, Sayal P. Evaluation of multiple antibiotic resistance (MAR) index and Doxycycline susceptibility of acinetobacter species among inpatients. Indian J Microbiol Res. 2016;3(3):299.

    Article  Google Scholar 

  98. Chai MH, Sukiman MZ, Liew YW, Shapawi MS, Roslan FS, Hashim SN et al. Detection, molecular characterization, and antibiogram of multi-drug resistant and methicillin-resistant Staphylococcus aureus (MRSA) isolated from pets and pet owners in Malaysia. Iran J Vet Res. 2021;22(4):277–87. Available from: http://www.ncbi.nlm.nih.gov/pubmed/35126535http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC8806171

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Acknowledgements

Authors appreciate the participants for their involvement in the study.

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This research study received no external funding.

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Authors and Affiliations

  1. Faculty of Science, Kyambogo University, P.O. Box 1, Kyambogo, Uganda

    Kizito M. Muwonge, Hellen Ndagire & Charles Kakuhikire Twesigye

  2. Department of Biochemistry and Sports Science, Makerere University, P.O. Box 7062, Kampala, Uganda

    Julius Mulindwa

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  1. Kizito M. Muwonge
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Contributions

K.M.M conceptualised, designed and conducted laboratory analysis and drafted the initial manuscript. J.M and C.T.K supervised the research activities. H.N conducted the laboratory analysis. J.M and H.N revised the manuscript. The authors read and approved the final manuscript.

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Correspondence to Kizito M. Muwonge.

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The authors have declared no conflict of interest.

Ethical approval

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Ethics Committee of Uganda Christian University Research Ethics Committee (Ref: UCUREC − 2023 − 757, 20 -02-2024) and the Institutional Animal Care and Use Committee of the School of Veterinary Medicine and Animal Resources, Makerere University (Ref: Date of approval: SVAR_IACUC/83/2021, Renewed 08-01-2024).

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All the subjects provided informed consent for inclusion before they participated in the study.

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Muwonge, K.M., Ndagire, H., Mulindwa, J. et al. Multiple antimicrobial resistance indices of Staphylococcus aureus from the nares of goats and slaughterhouse attendants in Kampala city, Uganda– a cross sectional study. BMC Microbiol 25, 162 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12866-025-03891-y

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Keywords

BMC Microbiology

ISSN: 1471-2180

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