Sustainable triazine-derived quaternary ammonium salts as antimicrobial agents

Article abstract of DOI:10.1039/d1ra03455c

The first examples of highly efficient antimicrobial triazine-derived bis imidazolium quaternary ammonium salts (TQAS) are reported. TQAS have been prepared with an easy, atom efficient, economically sustainable strategy and tested as antimicrobial agents

Full text of DOI:10.1039/d1ra03455c

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Sustainable triazine-derived quaternary ammonium
salts as antimicrobial agents†
Cite this: RSC Adv., 2021, 11, 28092
ac
Andrea Morandini,a Emanuele Spadati,a Benedetta Leonetti,b Roberto Sole,
d
a
ad
*
Vanessa Gatto,
Flavio Rizzolio
and Valentina Beghetto
Received 4th May 2021
Accepted 15th August 2021
The first examples of highly efficient antimicrobial triazine-derived bis imidazolium quaternary ammonium
salts (TQAS) are reported. TQAS have been prepared with an easy, atom efficient, economically sustainable
strategy and tested as antimicrobial agents, reaching MIC values below 10 mg Lꢀ1. Distinctively, TQAS have
low MIC and low cytotoxicity.
DOI: 10.1039/d1ra03455c
rsc.li/rsc-advances
Infectious diseases remain one of the most important health role in determining the antimicrobial action of QAS, requiring
problems in the world affecting millions of people.1 The new an hydrophobic segment compatible with the bilayer of the
COVID-19 pandemic further increased the pressure for the membrane and a positively charged quaternary nitrogen atom
development of new efficient antibacterial agents to prevent the alike to the polar head of phospholipid acids.9,12 Thus, at least
spread of pathogens from the environment to human beings. one of the organic substituents present on the nitrogen atom
Surface disinfection emerges as a winning strategy towards the should be an alkyl chain and in fact, the activity of QAS may be
mitigation of multi-drug resistance (MDR) phenomena, pre- tuned by changing the length of this alkyl chain.13,14 Addition-
venting the spread of pathogens. A wide variety of physical2 and ally, the antimicrobial activity of QAS depends on the number of
chemical3 treatments have been developed to combat the positive charges present, so that these compounds are divided
spreading of bacterial infections.
into Mono, Bis (gemini) and tris-QAS (Fig. 1).6a,c,8,9,14
Antibiotics have been massively employed to face global
Bis-QAS are in general more efficient than mono QAS, while
health emergencies,4 but abuse of antibiotics has generated no signicant improvement is oen observed when tris-QAS are
multi drug resistant bacteria, hampering the efficiency of employed. Additionally, bis-QAS induce lower bacterial resis-
infection treatments.5 Thus the development of alternative tance phenomena compared to most commercially available
antimicrobials is fundamental for human survival. Additionally, mono-QAS.6c–15 Generally, QAS are synthesized by reaction of
because of the COVID-19 pandemic, the use of surface disin- a tertiary amine with an alkyl, aryl, or heterocyclic halide at
fectants has emerged as a fundamental best practice for solvent reux temperature. This standard procedure, despite its
prevention.
simplicity, in most cases, requires the use of toxic alkyl-
Quaternary ammonium salts (QAS) are a well-known class of bromides as reagents.
efficient antimicrobial agents with a broad spectrum of activity
With all this in mind, herein we reported the synthesis of
and long-lasting efficiency due to their persistence on treated new triazine based bis-QAS and their efficacy as antimicrobial
surfaces.1a,4b,6 They are commonly present in domestic cleaning agents against several Gram-positive and Gram-negative bacte-
products,6g food preservatives,7 health care products,6d,8 rial species. To the best of our knowledge, this is the rst
biomedical materials9 and surfactants,10 and are expected to example of the use of triazine quaternary ammonium salts as
reach a turnover of $8 billion by 2021.11
QAS generally contain four alkyl, aryl, or heterocyclic organic
groups bonded to a nitrogen atom. According to the literature,
the organic groups present on the nitrogen atom play a pivotal
a
`
Universita Ca’ Foscari di Venezia, Via Torino 155, Venezia Mestre, 30172, Italy.
E-mail: beghetto@unive.it
bBrenta S.r.l. – Nine Trees Group., Viale Milano, 26, 36075 Montecchio Maggiore
Vicenza, Italy
c
`
Consorzio Interuniversitario per le Reattivita Chimiche e Catalisi (CIRCC), Via C.
Ulpiani 27, 70126 Bari, Italy
dCrossing S.r.l., Viale della Repubblica 193/b, Treviso, 31100, Italy
† Electronic supplementary information (ESI) available. See DOI:
10.1039/d1ra03455c
Fig. 1 General QAS classification.
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application as activators in dehydro-condensation reactions for
the production of amides or esters (Fig. 2).17 Nevertheless,
DMTMM is a very reactive compound, with low stability in
solution decomposing within 48 h, to generate 2,4-dimethoxy-6-
hydroxy-1,3,5-triazine (DMTOH) and N-methyl morpholinium
chloride. Thus, this class of quaternary ammonium salts are
inadequate to be used as antimicrobials and have never been
tested for the scope.
It is no less true that according to the literature the stability
and reactivity of 4-(4,6-dimethoxy-1,3,5-triazin-2-yl)-4-tert-amine
chloride, prepared by reaction of 2-chloro-4,6-dialcoxy-1,3,5-
triazine and a tert-amine, may be tuned by changing the tert-
amine.18 When the tert-amine is N-methylimidazole, the corre-
Fig. 2 DMTMM, DMTOH, DMT-Imi, DEAT, DIAT.
sponding
3-(4,6-dimethoxy-1,3,5-triazin-2-yl)-1-methyl-1H-
imidazol-3-ium chloride (DMT-Imi, Fig. 2) is highly stable and is
unable to promote condensation reactions.18a
With a radically different approach, this drawback became
a positive feature with the aim to prepare stable triazine based
quaternary ammonium salts to be used as antimicrobials.
According to the general rule that antimicrobials should have
a long alkyl chain within their structure and that bis-QAS are
more efficient and give lower bacterial resistance phenomena,
3,30-(6-(alkylamino)-1,3,5-triazine-2,4-diyl)bis(1-methyl-1H-
imidazol-3-ium) quaternary ammonium salts were synthesized
and tested as antimicrobials. Thus, two different synthetic
approaches were devised for the synthesis of bis-TQAS (VI–X), as
reported in Scheme 1.
The synthesis of bis-TQAS was tested by two different
synthetic strategies employing the same reagents but in
a different addition sequence (Scheme 1). In the rst case, 2,4,6-
trichloro-1,3,5-triazine (CC) was reacted, at room temperature,
with methyl imidazole, in 1/2 molar ratio (Scheme 1a), but no
3,30-(6-chloro-1,3,5-triazine-2,4-diyl)bis(1-methyl-1H-imidazol-
3-ium) chloride (XI) was formed. Further experiments were
carried out in different reaction conditions but without success.
A second synthetic strategy was veried, foreseeing rst the
synthesis of 4,6-dichloro-N-alkyl-1,3,5-triazin-2-amine (I–V) by
reaction of CC with an alkyl amine, followed by the reaction of
compounds I–V with N-methylimidazole (Scheme 1b).
Commercially available alkyl amines of variable length (C10–
C18) were used to introduce into nal bis-TQAS a long hydro-
phobic carbon chain required to interact with the bilayer of the
membrane (Schema 1b).6e,19 With this synthetic strategy ve
different 2,4-dichloro-6-alkylamino-1,3,5-triazines (I–V) were
synthesized in yields between 50–70%, within 1.5 h (Scheme
Scheme 1 Alternative synthetic strategies for bis-TQAS.
antimicrobials. The use of a triazine core allowed us to imple-
ment an innovative synthetic approach avoiding the use of alkyl
halides and reducing solvent consumption based on a simple,
easy to tune, atom efficient methodology.
Triazines are very reactive compounds, widely employed for
the synthesis of a plethora of ne chemicals, dyes, herbicides,
polymers.16 Since 1998, when Kunishima and Kaminsky devel-
oped the synthesis of the rst triazine derived quaternary
ammonium salt, 4-(4,6-dimethoxy-1,3,5-triazin-2-yl)-4-methyl-
morpholinium chloride (DMTMM), triazines have found a key
Table 1 Minimal inhibitory concentration, IC50, critical micelle concentration and Log P(n-octanol/water) of TQAS
MIC [mg Lꢀ1
]
Compound
Log P
CMC [mM]
S. a.
E. f.
E. c.
P. a.
IC50 [mg Lꢀ1
]
VI
ꢀ0.77
0.02
0.81
1.60
2.40
—
250
7.80
3.90
125
250
125
62.5
62.5
62.5
62.5
250
500
500
250
>500
>500
13.3
7.6
2.4
6.7
5.1
VII
VIII
IX
20.5
9.3
2.2
1.1
62.5
62.5
250
>500
X
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alkylamino-1,3,5-triazines (I–V) were synthesized and further
employed for the preparation of bis-TQAS.
The antimicrobial activity of all compounds was tested
against Gram-positive Staphylococcus aureus (ATCC 25923),
Enterococcus faecalis (CECT 795) and Gram-negative Escherichia
coli (ATCC 25922), Pseudomonas aeruginosa (CECT 111) strains.
Minimum inhibitory concentration (MIC) was taken as lowest
concentration completely inhibiting microbial growth and all
experiments were carried out in biological and technical tripli-
cate. Minimal inhibitory concentration, IC50, critical micelle
concentration and Log P(n-octanol/water) of bis-TQAS are re-
ported in Table 1.
The activity of bis-TQAS towards S. aureus showed a para-
bolic trend for compound VI, IX and X, respectively with 10, 16,
and 18 carbon atoms in the alkyl chain, while lowest MICs were
measured with compounds VII and VIII (C12, C14). These data
are well in line and even superior to most efficient antimicrobial
Fig. 3 MIC values of different bis-TQAS against S. aureus, E. faecalis, E.
coli and P. aeruginosa.
bis-QAS recently reported in the literature, giving MIC values
between 8 and 80 mg Lꢀ1
.
20
MIC against Gram-negative E. coli strains showed a similar
trend to S. aureus, reaching best MIC (62 mg Lꢀ1) with bis-TQAS
containing C12, C14 alkyl chains. Except for compound VI, all
bis-TQAS were equally efficient towards E. faecalis with a MIC of
62 mg Lꢀ1 (Fig. 3 and 4). Moreover, VIII was moderately active
also against P. aeruginosa (250 mg Lꢀ1). In fact, this Gram-
negative strain is rather resistant to QAS and in most cases
MIC values achieved are within the range of 40 to 1410 mg Lꢀ1
,
while only in few cases MIC values below 10 mg Lꢀ1 have been
achieved, albeit with more complex structures and synthesis.20
Cytotoxicity of bis-TQAS was tested against eukaryotic
broblasts MRC-5 as half maximal inhibitory concentration
IC50 values. IC50 for compounds VII, IX and X were comparable
and respectively of 7.6, 6.7 and 5.1 mg Lꢀ1, while VIII, showed
slightly higher cytotoxicity (2.4 mg Lꢀ1), but signicantly lower
than commercially available QAS such as for example benzal-
konium chloride (0.1 mg mLꢀ1),20b indicating a very low cyto-
toxicity of bis-TQAS tested. Compound VI (C10), possessing
a modest antimicrobial activity, showed even lower IC50
(13.3 mg Lꢀ1). Interestingly, MIC and IC50 are generally corre-
lated to the alkyl chain length19b while no signicant variations
were observed with bis-TQAS. Further studies are ongoing to
investigate this behaviour, nevertheless it should be considered
that correlation of biological effect and specic chain length
may depend on several physicochemical parameters such as
hydrophobicity, adsorption, solubility, and transport in the
medium so that deviations from general structure–activity
dependence have been reported for several QAS.6c,21
To gain dipper insight into bis-TQAS activity, Log P and
critical micelle concentration (CMC) of different bis-TQAS were
calculated to determine possible correlations between hydro-
phobicity of the compounds and their antimicrobial activity. In
fact, according to the literature21,22 the antimicrobial activity of
QAS should depend not only on the length of the alkyl chain but
also on CMC and hydrophobicity/lipophilicity.
MIC versus LogP showed a minimum for compounds VII and
VIII (Fig. 5), conrming that, as for QAS, too long or too short
alkyl chains adversely affect the antimicrobial activity of bis-
Fig.
4 Antimicrobial performance of compound VIII at various
concentrations against S. aureus (orange) and E. coli (blue).
ꢁ
1b). Addition of the primary amine was carried out at 0 C to
prevent the formation of di or tri-substituted products (Scheme
1, ESI†). The synthesis of bis-TQAS was carried out at room
temperature, by simple addition of two equivalents of N-meth-
ylimidazole to compounds I–V, to give the desired bis-TQAS (VI–
X) (Scheme 1b). No purication steps were required and all bis-
TQAS were recovered from the reaction mixture, within few
minutes, by simple ltration in high yields ($90%).
Additionally, 2-chloro-4,6-dialkylamino-1,3,5-triazines could
be prepared for the synthesis of corresponding mono-TQAS.
Nevertheless, as reported in the literature, the presence of two
alkylamino electron-donating groups strongly reduce the reac-
tivity of the corresponding triazine, so much that, 2-chloro-4,6-
(diethylamino)-1,3,5-triazine
(DEAT)
and
2-chloro-4,6-
(diisopropylamino)-1,3,5-triazine (DIAT) are unable to react
with a tertiary amine to give the corresponding triazine
quaternary ammonium salt.18b Thus, only 2,4-dichloro-6-
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Conclusions
In conclusion, in this study, a family of stable bis-TQAS were
synthesized starting from 2,4-dichloro-6-alkylamine-1,3,5-
triazine, in the presence of methyl imidazole with an easy and
sustainable methodology. The process was readily scaled up to
over 500 g scale. The compounds have been obtained in very
high yields (over 90%) in short reaction times (1.5 hours),
without the use of alkyl halides. A set of different bis-TQAS was
prepared bearing C10–C18 alkyl chains to study the correlation
between the length of the alkyl chain and their antimicrobial
activity against Gram-positive and Gram-negative bacterial
strains.
The bacterial inhibition effects were found to be remarkable
when bis-TQAS VII (C12) and VIII (C14) are in the range between
3.9 to 7.8 mg Lꢀ1 for S. aureus, and 62 mg Lꢀ1 for both E. coli and
E. faecalis. A further benet of these compounds is their low
cytotoxicity compared to many commercially available QAS.
This article therefore opens an innovative perspective to
produce a new class of antimicrobial QAS having low toxicity.
Fig. 5 Bis-TQAS dependence of Log P (water/n-octanol) and CMC
versus MIC, against S. aureus and E. coli.
Conflicts of interest
There are no conicts to declare.
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