Histidine decarboxylase-positive lactic acid bacteria strains and the formation of histamine in ripened cheeses

Abstract

The relationship between histidine decarboxylase‐positive (hdc+) lactic acid bacteria (LAB) counts and the amounts of biogenic amines, particularly histamine, in cheeses made with and without LAB starter were investigated. Sixty LAB strains were isolated from ripened cheeses made with raw milk inoculated with lactic starter and cheeses without starter. The strains were identified by carbohydrate fermentation test and the histidine decarboxylase gene was determined by PCR. Biogenic amine contents from the cheeses were determined by HPLC. LAB counts and their diversity were higher in the cheeses without starter. The cheeses contained low concentrations of the studied amines. The lowest concentrations were found for ethylamine and putrescine followed by cadaverine, tyramine, phenyletilamine, and histamine, especially in the cheeses with starter. There was a direct relationship between the percentage of hdc+ LAB strains and histamine and between this percentage and the sum of tyramine, phenylethylamine and ethylamine concentrations. Practical applications It is a well‐known fact that the content of biogenic amines in cheeses should be controlled because these compounds can cause toxicity and undesirable flavor. The results of the present study show that LAB starter cultures do not completely prevent the formation of biogenic amines in cheeses manufactured with raw milk. Although the LAB starter helps to reduce the total amount of biogenic amines, histamine concentration is not clearly linked to the use of starter. In order to ensure the safety of cheeses, it is necessary to use high‐quality milk, follow hygienic practices and take advantage of the selective pressure of the physicochemical and technological parameters that occur during cheese making.

Histamine accumulation in dairy products: Microbial causes, techniques for the detection of histamine‐producing microbiota, and potential solutions

“…30a (ATCC 33222) (Le Jeune et al., 1995 ), Lentilactobacillus buchneri, Levilactobacillus brevis, Lacticaseibacillus casei, Lactiplantibacillus plantarum , and Lactobacillus delbrueckii subsp. lactis (del Valle et al., 2018)…”

“…30a (ATCC 33222), Lentilactobacillus buchneri StA2 and Lentilactobacillus hilgardii BIFI‐87 (Marcobal et al., 2005) , Lentilactobacillus buchneri B301 (Ladero et al., 2015) , Lentilactobacillus buchneri StA2, Lentilactobacillus buchneri NZHD1, Lentilactobacillus buchneri NZHD2, Lentilactobacillus buchneri NZHD3, Lentilactobacillus buchneri NZHD4, Lentilactobacillus buchneri NZHD5 and Lentilactobacillus buchneri CIVO29 (Le Jeune et al., 1995 ), Lentilactobacillus buchneri, Levilactobacillus brevis, Lacticaseibacillus casei, Lactiplantibacillus plantarum , and Lactobacillus delbrueckii subsp. lactis (del Valle et al., 2018), Lentilactobacillus parabuchneri KUH1, Lentilactobacillus parabuchneri KUH2, Lentilactobacillus parabuchneri KUH8, and Lacticaseibacillus paracasei KUH3 (Møller, Ucok, & Rattray, 2020)…”

“…helveticus originated from a starter culture used for cheese production. Other species, such as L. brevis , L. casei , and L. plantarum , were found to contain the hdc gene in cheeses prepared with raw milk, and some of those species had not been added as starter cultures (del Valle et al., 2018). The Lb.…”

“…The hdc gene was also amplified in a Leuconostoc sp. strain isolated from raw goat milk cheese (del Valle et al., 2018). Potential histamine formation by E. faecium or E. casseliflavus in cheese has also been reported, but the contribution of enterococci to the level of histamine in cheese is probably irrelevant (Roig‐Sangüés et al., 2002; Tham, Karp, & Danielsson‐Tham, 1990).…”

“…Some authors adapted the pair of primers HDC3 and HDC4 to detect gram‐positive HPB in cheese or home‐made yogurt, which had been initially applied to smoked salmon by Burdychova and Komprda (2007) and Coton and Coton (2005). (Berthoud et al., 2017; Gezginc, Akyol, Kuley, & Ozogul, 2013; O'Sullivan et al., 2015) Primers CL1, CL2, JV16HC, and JV17HC, initially published by Le Jeune, Lonvaud‐Funel, ten Brink, Hofstra, and van der Vossen (1995), were used by other authors to highlight LAB containing the hdc gene in ripened or artisan cheeses (del Valle, Ginovart, Gordún, & Carbó, 2018; Ladero et al., 2015; Møller et al., 2020). Primers HIS2‐F and HIS2‐R, initially described by de Las Rivas et al.…”