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Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches

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A special issue of Antibiotics (ISSN 2079-6382).

Deadline for manuscript submissions: 31 October 2024 | Viewed by 13485

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Dr. Amira A. Moawad

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Guest Editor

Friedrich-Loeffler-Institut, Institute of Bacterial Infections and Zoonoses, Jena, Germany
Interests: antimicrobial resistance; WGS; epidemiology; genetics; antimicrobial susceptibility testing; molecular biology; animal production; mass spectrometry; zoonotic diseases; foodborne pathogens; food hygiene and control

Dr. Hosny El-Adawy

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Guest Editor

Friedrich-Loeffler-Institute, Institute of Bacterial Infections and Zoonoses, Jena, Germany
Interests: microbiology; molecular biology; AMR; campylobacter; avian diseases; bacterial zoonotic infections; animal diseases diagnosis

Prof. Dr. Heinrich Neubauer

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Guest Editor

Friedrich-Loeffler-Institut, Institute of Bacterial Infections and Zoonoses, Jena, Germany
Interests: microbiology; antimicrobial resistance; WGS; epidemiology; zoonotic diseases; genetics; molecular biology; mass spectrometry; foodborne pathogens; food hygiene; bacterial zoonotic infections; animal diseases diagnosis

Special Issue Information

Dear Colleagues,

Mastitis is an inflammatory response of the mammary gland tissue caused by microbial infections or physical trauma. It is regarded as the most prevalent illness that causes financial loss in the dairy industry because of decreased yields, poor milk quality, culling of non-treatable animals, and human health issues. Bacterial pathogens are majorly incriminated in the etiology of mastitis; more than 135 different bacterial species are linked to bovine mastitis, but the most frequent pathogenic bacteria are 20 different species. Antimicrobial drugs are the main regimen used to treat bacterial-caused mastitis. Nevertheless, mastitis treatment is usually prolonged for more than expected due to the recurrence of the condition and the difficulty in bacterial eradication using a variety of antimicrobials. This has resulted in the emergence of multidrug-resistant bacteria globally. Estimation of the distribution of pathogens associated with clinical and subclinical mastitis and understating their antimicrobial resistance patterns has to be focused on. Combating the threat of antimicrobial resistance is a high priority as it is considered a serious human- and animal-threating problem. Additionally, alternative approaches to tackle the mastitis causative pathogens with the avoidance of the development of drug resistance are eagerly seeked.

Dr. Amira A. Moawad
Dr. Hosny El-Adawy
Prof. Dr. Heinrich Neubauer
Guest Editors

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Keywords

mastitis
etiology
multidrug resistance
alternative bovine mastitis treatment
WGS

Published Papers (7 papers)

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Research

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27 pages, 2582 KiB

Open AccessArticle

Prevalence and Antimicrobial Resistance of Escherichia coli O157:H7 and Salmonella, and the Prevalence of Staphylococcus aureus in Dairy Cattle and Camels under Pastoral Production System

by Diriba Hunduma, Kebede Amenu, Hiwot Desta, Delia Grace, Getahun E. Agga and Oudessa Kerro Dego

Antibiotics 2024, 13(1), 26; https://doi.org/10.3390/antibiotics13010026 - 27 Dec 2023

Viewed by 2075

Abstract

Escherichia coli O157:H7, Salmonella and Staphylococcus aureus are common foodborne pathogens. We determined the prevalence of E. coli O157:H7 and Salmonella in feces and milk and the prevalence of S. aureus in milk from dairy cattle and camels in the Borana pastoral community in the Southern Oromia Region of Ethiopia. Paired individual cow composite (pooled from all quarters in equal proportions) milk and fecal samples were collected from cows (n = 154) and camels (n = 158). Samples were cultured on bacterial isolation and identification media. E. coli O157:H7 and Salmonella isolates were further tested for susceptibility against nine antimicrobial drugs. Different risk factors associated with hygienic milking practices were recorded and analyzed for their influence on the prevalence of these bacteria in milk and feces. The prevalence of E. coli O157:H7 and Salmonella in feces were 3.9% and 8.4%, respectively, in cows, and 0.6% and 2.5%, respectively, in camels. E. coli O157:H7 and Salmonella were detected in the composite milk samples of 2.6% and 3.9% of the cows, respectively, and 0% and 1.3% of the camels, respectively. S. aureus was detected in composite milk samples of 33.4% of the cows and 41.7% of the camels. All E. coli O157:H7 (n = 11) and Salmonella (n = 25) isolates from both animal species and sample types were resistant to at least one antimicrobial drug. Multidrug resistance was observed in 70% (7/10) of the E. coli O157:H7 fecal and milk isolates from cows and 33.3% (2/6) of the Salmonella fecal and milk isolates from camels. The prevalence of these bacteria in feces and milk was not affected by risk factors associated with milking practices. Given the very close contact between herders and their animals and the limited availability of water for hand washing and udder cleaning, these bacteria are most likely present in all niches in the community. Improving community awareness of the need to boil milk before consumption is a realistic public health approach to reducing the risk of these bacteria. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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14 pages, 653 KiB

Open AccessArticle

Antimicrobial Resistance Profiles of Staphylococcus Isolated from Cows with Subclinical Mastitis: Do Strains from the Environment and from Humans Contribute to the Dissemination of Resistance among Bacteria on Dairy Farms in Colombia?

by Martha Fabiola Rodríguez, Arlen Patricia Gomez and Andres Ceballos-Garzon

Antibiotics 2023, 12(11), 1574; https://doi.org/10.3390/antibiotics12111574 - 28 Oct 2023

Viewed by 1466

Abstract

Staphylococcus is a very prevalent etiologic agent of bovine mastitis, and antibiotic resistance contributes to the successful colonization and dissemination of these bacteria in different environments and hosts on dairy farms. This study aimed to identify the antimicrobial resistance (AMR) genotypes and phenotypes of Staphylococcus spp. isolates from different sources on dairy farms and their relationship with the use of antibiotics. An antimicrobial susceptibility test was performed on 349 Staphylococcus strains (S. aureus, n = 152; non-aureus staphylococci (NAS), n = 197) isolated from quarter milk samples (QMSs) from cows with subclinical mastitis (176), the teats of cows (116), the milking parlor environment (32), and the nasal cavities of milk workers (25). Resistance and multidrug resistance percentages found for S. aureus and NAS were (S. aureus = 63.2%, NAS = 55.8%) and (S. aureus = 4.6%, NAS = 11.7%), respectively. S. aureus and NAS isolates showed resistance mainly to penicillin (10 IU) (54.1% and 32.4%) and ampicillin (10 mg) (50.3% and 27.0%) drugs. The prevalence of AMR Staphylococcus was higher in environmental samples (81.3%) compared to other sources (52.6–76.0%). In S. aureus isolates, the identification of the blaZ (83.9%), aacAaphD (48.6%), ermC (23.5%), tetK (12.9%), and mecA (12.1%) genes did not entirely agree with the AMR phenotype. We conclude that the use of β-lactam antibiotics influences the expression of AMR in Staphylococcus circulating on dairy farms and that S. aureus isolates from the environment and humans may be reservoirs of AMR for other bacteria on dairy farms. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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16 pages, 2498 KiB

Open AccessArticle

Dilution Reduces Sample Matrix Effects for Rapid, Direct, and Miniaturised Phenotypic Antibiotic Susceptibility Tests for Bovine Mastitis

by Matthew Michael Long, Sarah Helen Needs and Alexander Daniel Edwards

Antibiotics 2023, 12(9), 1363; https://doi.org/10.3390/antibiotics12091363 - 24 Aug 2023

Viewed by 1178

Abstract

The time-consuming nature of current methods for detecting antimicrobial resistance (AMR) to guide mastitis treatment and for surveillance, drives innovation towards faster, easier, and more portable technology. Rapid on-farm testing could guide antibiotic selection, reducing misuse that contributes to resistance. We identify challenges that arise when developing miniaturized antibiotic susceptibility tests (AST) for rapid on-farm use directly in milk. We experimentally studied three factors: sample matrix (specifically milk or spoiled milk); the commensal bacteria found in fresh bovine milk; and result time on the performance of miniaturised AST. Microfluidic “dip-and-test” devices made from microcapillary film (MCF) were able to monitor Gram-negative bacterial growth colourimetrically even in the presence of milk and yoghurt (used to simulate spoiled milk samples), as long as this sample matrix was diluted 1:5 or more in growth medium. Growth detection kinetics using resazurin was not changed by milk at final concentrations of 20% or lower, but a significant delay was seen with yoghurt above 10%. The minimum inhibitory concentration (MIC) for ciprofloxacin and gentamicin was increased in the presence of higher concentrations of milk and yoghurt. When diluted to 1% all observed MIC were within range, indicating dilution may be sufficient to avoid milk matrix interfering with microfluidic AST. We found a median commensal cell count of 6 × 10⁵ CFU/mL across 40 healthy milk samples and tested if these bacteria could alter microfluidic AST. We found that false susceptibility may be observed at early endpoint times if testing some pathogen and commensal mixtures. However, such errors are only expected to occur when a susceptible commensal organism is present at higher cell density relative to the resistant pathogen, and this can be avoided by reading at later endpoints, leading to a trade-off between accuracy and time-to-result. We conclude that with further optimisation, and additional studies of Gram-positive organisms, it should be possible to obtain rapid results for microfluidic AST, but a trade-off is needed between time-to-result, sample dilution, and accuracy. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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20 pages, 2406 KiB

Open AccessArticle

Rationally Designed Pyrimidine Compounds: Promising Novel Antibiotics for the Treatment of Staphylococcus aureus-Associated Bovine Mastitis

by Guillaume Millette, Evelyne Lacasse, Renaud Binette, Véronique Belley, Louis-Philippe Chaumont, Céline Ster, Francis Beaudry, Kumaraswamy Boyapelly, Pierre-Luc Boudreault and François Malouin

Antibiotics 2023, 12(8), 1344; https://doi.org/10.3390/antibiotics12081344 - 21 Aug 2023

Cited by 1 | Viewed by 1144

Abstract

Staphylococcus aureus is one of the major pathogens causing bovine mastitis, and antibiotic treatment is most often inefficient due to its virulence and antibiotic-resistance attributes. The development of new antibiotics for veterinary use should account for the One Health concept, in which humans, animals, and environmental wellbeing are all interconnected. S. aureus can infect cattle and humans alike and antibiotic resistance can impact both if the same classes of antibiotics are used. New effective antibiotic classes against S. aureus are thus needed in dairy farms. We previously described PC1 as a novel antibiotic, which binds the S. aureus guanine riboswitch and interrupts transcription of essential GMP synthesis genes. However, chemical instability of PC1 hindered its development, evaluation, and commercialization. Novel PC1 analogs with improved stability have now been rationally designed and synthesized, and their in vitro and in vivo activities have been evaluated. One of these novel compounds, PC206, remains stable in solution and demonstrates specific narrow-spectrum activity against S. aureus. It is active against biofilm-embedded S. aureus, its cytotoxicity profile is adequate, and in vivo tests in mice and cows show that it is effective and well tolerated. PC206 and structural analogs represent a promising new antibiotic class to treat S. aureus-induced bovine mastitis. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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12 pages, 1954 KiB

Open AccessArticle

Staphylococcus aureus-Cure-Associated Antigens Elicit Type 3 Immune Memory T Cells

by Kamila R. Santos, Fernando N. Souza, Eduardo M. Ramos-Sanchez, Camila F. Batista, Luiza C. Reis, Wesley L. Fotoran, Marcos B. Heinemann, Adriano F. Cunha, Mussya C. Rocha, Angélica R. Faria, Hélida M. Andrade, Mônica M. O. P. Cerqueira, Magnus Gidlund, Hiro Goto and Alice Maria M. P. Della Libera

Antibiotics 2022, 11(12), 1831; https://doi.org/10.3390/antibiotics11121831 - 16 Dec 2022

Viewed by 1497

Abstract

Background: Staphylococcus aureus is one of the most frequently major mastitis pathogens that cause clinical and subclinical mastitis worldwide. Current antimicrobial treatments are usually ineffective, and the commercially available vaccines lack proven effectiveness. The immunological response elicited by the recombinant S. aureus-cure-associated proteins phosphoglycerate kinase (PGK), enolase (ENO), and elongation factor-G (EF-G) in combination with the granulocyte-macrophage colony-stimulating factor (GM-CSF) DNA vaccination was studied in this work. Methods: Here, twenty-three C57BL/6 mice were divided into four groups and vaccinated with: G1: none (control); G2: GM-CSF DNA plasmid DNA vaccine; G3: the combination of EF-G+ENO+PGK; and G4: the combinations of EF-G+ENO+PGK proteins plus GM-CSF plasmid DNA vaccine. After 44 days, spleen cells were collected for immunophenotyping and lymphocyte proliferation evaluation by flow cytometry upon S. aureus stimulus. Results: Immunization with the three S. aureus recombinant proteins alone resulted in a higher percentage of IL-17A⁺ cells among CD8⁺ T central memory cells, as well as the highest intensity of IL-17A production by overall lymphocytes indicating that the contribution of the combined lymphocyte populations is crucial to sustaining a type 3 cell immunity environment. Conclusion: The immunization with three S. aureus-cure-associated recombinant proteins triggered type 3 immunity, which is a highly interesting path to pursue an effective bovine S. aureus mastitis vaccine. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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12 pages, 710 KiB

Open AccessArticle

Ecological Distribution of Virulent Multidrug-Resistant Staphylococcus aureus in Livestock, Environment, and Dairy Products

by Basma Badawy, Mahmoud Elafify, Alshimaa M. M. Farag, Samar M. Moustafa, Mohamed Z. Sayed-Ahmed, Amira A. Moawad, Abdelazeem M. Algammal, Hazem Ramadan and Mahmoud Eltholth

Antibiotics 2022, 11(11), 1651; https://doi.org/10.3390/antibiotics11111651 - 18 Nov 2022

Cited by 5 | Viewed by 2189

Abstract

Staphylococcus aureus is one of the most common causes of mastitis, leading to severe economic losses in the dairy industry. It is also zoonotic, with potential risks to public health. This study aimed to detect the occurrence of S. aureus-resistant strains isolated from cattle, buffalo, their environment, milk and dairy products; and to investigate the extent of animal, ecological, and food contamination by methicillin-resistant (MRSA) or enterotoxigenic S. aureus. Samples (n = 350) were collected from four animal (two cattle and two buffalo) farms, i.e., their environment. Thirty Karish cheese samples were collected from 10 markets in Mansoura, Egypt. S. aureus was detected in 17.9%, 17.6%, and 16.7% of samples collected from cattle, buffalo and Karish cheese, respectively. About 19% of isolated S. aureus strains carried the mecA gene. The distribution of the mecA gene was high in isolates from Karish cheese (60%), followed by samples collected from buffalo (16.2%) and cattle (16%). More than 34% of isolated S. aureus strains were enterotoxigenic, and the presence of enterotoxin genes was higher in isolates from Karish cheese (80%) than those from cattle (48%) and buffalo (18.9%). The most predominant enterotoxin gene among isolated S. aureus strains was the sea gene (26.9%), followed by sec (4.5%) and sed (3%) genes. Isolated strains were resistant to clindamycin (100%), kanamycin (97%), nalidixic acid (86.6%), cefotaxime (73.1%) sulphamethazole—trimethoprim (65.6%). Meanwhile, 95.5%, 94%, 86.6% and 77.7% of S. aureus strains were sensitive to ciprofloxacin, amikacin, imipenem and both cefoxitin and gentamycin, respectively. In conclusion, the presence of enterotoxigenic- and methicillin-resistant S. aureus strains in animals, their environment, and dairy products represents a public health concern, particularly in small-scale dairy farms in Egypt. To reduce the risk of infection of livestock and humans with resistant strains, strict regulations and guidelines for antimicrobial use in such a system are urgently required. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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Review

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21 pages, 1057 KiB

Open AccessReview

Bacteriophage Therapy to Control Bovine Mastitis: A Review

by Janet Y. Nale and Neil R. McEwan

Antibiotics 2023, 12(8), 1307; https://doi.org/10.3390/antibiotics12081307 - 10 Aug 2023

Cited by 1 | Viewed by 2648

Abstract

Bovine mastitis is a polymicrobial disease characterised by inflammation of the udders of dairy and beef cattle. The infection has huge implications to health and welfare of animals, impacting milk and beef production and costing up to EUR 32 billion annually to the dairy industry, globally. Bacterial communities associated with the disease include representative species from Staphylococcus, Streptococcus, Enterococcus, Actinomyces, Aerococcus, Escherichia, Klebsiella and Proteus. Conventional treatment relies on antibiotics, but antimicrobial resistance, declining antibiotic innovations and biofilm production negatively impact therapeutic efficacy. Bacteriophages (phages) are viruses which effectively target and lyse bacteria with extreme specificity and can be a valuable supplement or replacement to antibiotics for bovine mastitis. In this review, we provide an overview of the etiology of bovine mastitis, the advantages of phage therapy over chemical antibiotics for the strains and research work conducted in the area in various model systems to support phage deployment in the dairy industry. We emphasise work on phage isolation procedures from samples obtained from mastitic and non-mastitic sources, characterisation and efficacy testing of single and multiple phages as standalone treatments or adjuncts to probiotics in various in vitro, ex vivo and in vivo bovine mastitis infection models. Furthermore, we highlight the areas where improvements can be made with focus on phage cocktail optimisation, formulation, and genetic engineering to improve delivery, stability, efficacy, and safety in cattle. Phage therapy is becoming more attractive in clinical medicine and agriculture and thus, could mitigate the impending catastrophe of antimicrobial resistance in the dairy sector. Full article

(This article belongs to the Special Issue Mastitis: Causative Agents, Drug Resistance, and Treatment Approaches)

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