A survey of the main technology, biochemical and microbiological
features influencing the concentration of biogenic amines of twenty
Apulian and Sicilian (Southern Italy) cheeses
Rosa Guarcello
a
, Annamaria Diviccaro
b
, Marcella Barbera
a
, Elena Giancippoli
b
,
Luca Settanni
a
, Fabio Minervini
b, *
, Giancarlo Moschetti
a
, Marco Gobbetti
b
a
Department of Agricultural and Forest Science, University of Palermo, Viale delle Scienze 4, 90128 Palermo, Italy
b
Department of Scienze del Suolo, della Pianta e degli Alimenti, University of Bari Aldo Moro, via Amendola 165/a, 70126 Bari, Italy
article info
Article history:
Received 11 September 2014
Received in revised form
27 November 2014
Accepted 28 November 2014
Available online 5 December 2014
abstract
Twenty Apulian and Sicilian cheeses were analysed for their concentrations of eight biogenic amines
(BAs), free amino acids, pH, water activity, and subjected to microbiological characterisation. In addition,
lactic acid bacteria isolated from cheeses were assayed for their capacity to generate BAs. Principal
component analysis was performed to find the effect of different parameters on the distribution of the
cheeses. Although short-ripened (30 d) cheeses did not show significant BA concentrations, the only BA
showing high positive correlation with time of ripening was histamine. Concentration of histidine and,
especially, percentage of histidine-decarboxylase bacteria presumably affected histamine concentration.
High pH values were negatively correlated to the concentration of tyramine, putrescine, and cadaverine.
Fifty percent of the cheeses contained at least one BA at potentially toxic concentrations. Unambiguous
and ever-valid relations among parameters and BAs are difficult to determine, because BAs are the result
of combined and varied factors.
© 2014 Elsevier Ltd. All rights reserved.
1. Introduction
Biogenic amines (BAs) are low-molecular nitrogenous organic
bases that are formed in foodstuffs by microbial decarboxylation of
the precursor amino acids. Tyrosine, histidine, lysine, tryptophan,
and phenylalanine are, respectively, precursor amino acids for
tyramine, histamine, cadaverine, tryptamine, and 2-
phenylethylamine. Ornithine and arginine may be the precursors
for putrescine, spermidine and spermine. Although small amounts
of BAs are biosynthesised in plant and animal cells, having different
biological activities (Pinho et al., 2004), these compounds are
potentially toxic to human health. The effects on nervous and
vascular systems are particularly severe in sensitive people or when
the amine oxidases, naturally involved in the detoxification, are
inhibited (Shalaby, 1996; Silla Santos, 1996). The toxicity limit of
BAs in foods is estimated to be 100 mg kg
1
, even though it is stated
that the safe sum of histamine, tyramine, putrescine and
cadaverine should not exceed 900 mg kg
1
(Shalaby, 1996;
Valsamaki, Michaelidou, & Polychroniadou, 2000).
Cheeses are among the foods most commonly associated with
the presence of BAs (Innocente & D'Agostin, 2002; Moret,
Bortolomeazzi, Feruglio, & Lerker, 1992; Stratton, Hutkins, &
Taylor, 1991). Indeed, the main biochemical process that takes
place during cheese ripening, proteolysis, leads to the accumulation
of free amino acids (FAAs), some of which are precursors of BAs. The
BA concentration of many typical and/or traditional Italian cheeses
was analysed (Innocente, Biasutti, Padovese, & Moret, 2007;
Ladero, Fern andez, &
Alvarez, 2009; Martuscelli et al., 2005;
Schirone et al., 2013; Spizzirri et al., 2013). Overall, the concentra-
tion and type of BAs in cheeses is extremely variable, depending on:
(i) type of milk (cows'/sheep's/goats' milk); (ii) thermal treatment
of cheese milk; (iii) section of the cheese (edge/core); (iv) ripening
conditions; (v) post-ripening processing; (vi) type of packaging;
(vii) storage time and temperature; and (viii) microbiota respon-
sible for cheese-making (Loizzo et al., 2013). Generally, the con-
centration of BAs was lower in short-ripened than in long-ripened
cheeses (Bunkov a et al., 2010; Fern andez, Linares, Del Rio, Ladero, &
Alvarez, 2007), where the level of proteolysis and catabolism of
* Corresponding author. Tel.: þ39 080 5442950.
E-mail address: fabio.minervini@uniba.it (F. Minervini).
Contents lists available at ScienceDirect
International Dairy Journal
journal homepage: www.elsevier.com/locate/idairyj
http://dx.doi.org/10.1016/j.idairyj.2014.11.007
0958-6946/© 2014 Elsevier Ltd. All rights reserved.
International Dairy Journal 43 (2015) 61e69