Diagnosing Intramammary Infection: Meta-Analysis and Mapping Review on Frequency and Udder Health Relevance of Microorganism Species Isolated from Bovine Milk Samples

SIMPLE SUMMARY: Innovations in veterinary medicine diagnostic methods can help to better identify the microorganisms causing bovine mastitis. Matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry is such an innovation. This tool can identify many different microorganisms cultured from bovine milk samples to species-level. However, not all these microorganisms are necessarily pathogenic to the cow udder. Using 93,353 milk samples from different countries, we aimed to determine the diversity and proportion of different microorganisms cultured from bovine milk of apparently healthy cow mammary glands and of clinical mastitis cases, and identified by MALDI-TOF. Moreover, we highlighted the current knowledge gaps on the effect of these microorganisms on udder health. We revealed a great diversity of microorganisms in both types of samples, but, for most species (206 of 294), little literature regarding their udder health relevance was available. However, some microorganisms with little or no scientific literature were frequently isolated from clinical mastitis samples; thus, suggesting that they may be relevant in terms of udder health. For other species, more research is needed to clarify their role. ABSTRACT: Matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry provides accurate species-level identification of many, microorganisms retrieved from bovine milk samples. However, not all those microorganisms are pathogenic. Our study aimed to: (1) determine the species-specific prevalence of microorganisms identified in bovine milk of apparently healthy lactating quarters vs. quarters with clinical mastitis (CM); and (2) map current information and knowledge gaps on udder health relevance of microorganisms retrieved from bovine milk samples. A mixed study design (meta-analysis and mapping review) was chosen. We gathered several large Canadian, US and Brazilian data sets of MALDI-TOF results for organisms cultured from quarter milk samples. For meta-analysis, two datasets (apparently healthy quarters vs. CM samples) were organized. A series of meta-analyses was conducted to determine microorganisms’ prevalence. Then, each species reported was searched through PubMed to investigate whether inflammation (increased somatic cell count (SCC) or signs of CM) was associated with microorganism’s recovery from milk. A total of 294 different species of microorganisms recovered from milk samples were identified. Among 50,429 quarter-milk samples from apparently healthy quarters, the 5 most frequent species were Staphylococcus chromogenes (6.7%, 95% CI 4.5–9.2%), Aerococcus viridans (1.6%, 95% CI 0.4–3.5%), Staphylococcus aureus (1.5%, 95% CI 0.5–2.8%), Staphylococcus haemolyticus (0.9%, 95% CI 0.4–1.5%), and Staphylococcus epidermidis (0.7%, 95% CI 0.2–1.6%). Among the 43,924 quarter-milk CM samples, the 5 most frequent species were Escherichia coli (11%, 95% CI 8.1–14.3%), Streptococcus uberis (8.5%, 95% CI 5.3–12.2%), Streptococcus dysgalactiae (7.8%, 95% CI 4.9–11.5%), Staphylococcus aureus (7.8%, 95% CI 4.4–11.9%), and Klebsiella pneumoniae (5.6%, 95% CI 3.4–8.2%). When conducting the PubMed literature search, there were 206 species identified by MALDI-TOF for which we were not able to find any information regarding their association with CM or SCC. Some of them, however, were frequently isolated in our multi-country dataset from the milk of quarters with CM (e.g., Citrobacter koseri, Enterococcus saccharolyticus, Streptococcus gallolyticus). Our study provides guidance to veterinarians for interpretation of milk bacteriology results obtained using MALDI-TOF and identifies knowledge gaps for future research.