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Biogenic Amines in Fish Roles in Intoxication Spoilage and Nitrosamine Formationa Review

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Abstruse

Putrescine and cadaverine are among the most common biogenic amines (BA) in foods, only it is advisable that their aggregating exist avoided. Present cognition near their toxicity is, however, limited; further research is needed if qualitative and quantitative take chances assessments for foods are to be conducted. The present work describes a existent-fourth dimension analysis of the cytotoxicity of putrescine and cadaverine on abdominal cell cultures. Both BA were cytotoxic at concentrations found in BA-rich foods, although the cytotoxicity threshold for cadaverine was twice that of putrescine. Their mode of cytotoxic action was similar, with both BA causing cell necrosis; they did not induce apoptosis. The present results may assist in establishing legal limits for both putrescine and cadaverine in food.

Introduction

Biogenic amines (BA) are naturally occurring nitrogenous compounds synthesised by plants, animals and microorganisms, mainly through the decarboxylation of amino acids. BA can accumulate at loftier concentrations in foods, largely due to the metabolic action of microorganisms with amino acid decarboxylase activenessone,2,3,4. Foods likely to contain high BA concentrations are fish, fish products and fermented foodstuffs (meat, dairy, some vegetables, beers and wines)5,6,vii,8. Although BA have of import biological functions in humans and are endogenously synthesised, the ingestion of food with high concentrations of BA can provoke serious toxicological reactionssix,8,nine,ten,eleven,12.

According to their chemical structure and number of amine groups, the BA putrescine and cadaverine are aliphatic diamines. The European Food Rubber Authorization (EFSA) has declared them amid the most common BA institute in foods12. Putrescine tin can accumulate at high concentrations in dairy fermented products such equally cheese (upwards to 1560 mg/kg), fermented sausages (up to 1550 mg/kg), fish sauces (up to 1220 mg/kg), fermented vegetables (upwards to 549 mg/kg), and fish and fish products (up to 337 mg/kg)12. Cadaverine tin can accumulate at high concentrations in cheese (upwardly to 3170 mg/kg), fish and fish products (up to 1690 mg/kg), fermented sausages (up to 1250 mg/kg) and fish sauces (upwards to 1150 mg/kg)12. Certainly, they are among the almost arable BA constitute in cheeses, forth with tyramine and histamine8,11,13 (considered by the EFSA as the about toxic of all BA12).

The information nearly the toxicity of putrescine and cadaverine is deficient, no human dose-response data are bachelor and only one creature report has been published in which a non-observed adverse effect level (NOAEL) of 2000 ppm (180 mg/kg body weight/twenty-four hour period) was established in Wistar ratsxiv. Although the pharmacological activities of putrescine and cadaverine seem less potent than those of histamine and tyramine12, the consumption of these vasoactive BA has been related to acute un-good for you effects such as increased cardiac output, lockjaw and paresis of the extremities, dilatation of the vascular system, hypotension, and bradycardia (possibly leading to heart failure and cerebral haemorrhage)half dozen,xv. In addition, both take indirect toxic effects via their potentiating the toxicity of other BA, such equally histamine. This occurs via the competitive inhibition of the detoxifying enzymes (diamine oxidase and histamine N-methyltransferase) involved in the oxidative catabolism of histamine16,17,eighteen,nineteen. The potentiation of histamine's toxic effect may also be explained by putrescine and cadaverine facilitating the passage of histamine across the small-scale intestine, thus increasing its rate of absorption into the blood streamtwenty,21. In addition, putrescine and cadaverine can react with nitrites and produce nitrosamines (putrescine yields nitrosopyrrolidine and cadaverine nitrosopiperidine)22, compounds known to be carcinogenichalf-dozen,ten,15. Putrescine (which physiological concentration in the colonic lumen is commonly in the milimolar range23) has besides been indicated direct involved in the oncogenic process24,25,26. An clan has also been reported between loftier intakes of dietary putrescine, along with the polyamines spermidine and spermine, and the take a chance of developing colorectal adenocarcinoma26,27.

Given these dangers, the legislation regarding the limits for BA in food needs revisiting. Indeed, in the European union it has only been established a maximum legal limit for histamine28. Similarly, in the U.s.a., the U.s. Food and Drug Assistants29 has only established legal limits for histamine in fish and fish products. No legislation has been established anywhere else, nor for any other BA. In fact, in a scientific opinion document regarding the risk-based command of BA formation in fermented products12, the EFSA panel on Biological Hazards (BIOHAZ) highlighted that a lack of noesis prevented whatever reliable quantitative or qualitative hazard assessment of putrescine and cadaverine in foods, concluding that farther inquiry on BA toxicity was needed.

Our group has recently developed an in vitro model for assessing the cytotoxicity of BA, either individually or in combination, in human intestinal jail cell cultures using real-time cell analysis (RTCA)30,31. With this model, tyramine and histamine were plant to exist cytotoxic towards intestinal cell cultures at concentrations hands reached in inherently BA-rich foods. In addition, it was revealed that while tyramine mainly causes cell necrosis, histamine induces apoptosis31. The model was also used to examine synergistic cytotoxicity betwixt tyramine and histaminethirty. The aim of the present work was to examine, using the aforementioned model, the in vitro cytotoxicity of putrescine and cadaverine. The concentration of BA required to achieve half of the strongest cytotoxic event observed in RTCA (IC50), the NOAEL, and the lowest observed adverse upshot level (LOAEL), were calculated for both BA. The mode of activity of each was also determined.

Results

Dynamic responses of putrescine and cadaverine-treated HT29 cells

As adamant by RTCA, a dose-dependent reduction in the normalized cell alphabetize was recorded for the HT29 cells exposed to putrescine (Fig. 1A) and cadaverine (Fig. 1B).

Figure 1
figure 1

Real-time cell analysis of the effects of putrescine and cadaverine on HT29 cells. Cells were exposed to the indicated concentrations of putrescine (A), cadaverine (B) or command medium (0 mM). Vertical arrows testify the point of administration of putrescine or cadaverine. The information represent to a representative experiment of the triplicates achieved. Vertical bars represent standard deviations.

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The dose-response curves constructed after 24 h of putrescine (Fig. 2A) or cadaverine (Fig. 2B) exposure fitted a sigmoid curve with an R2 of 0.988 and 0.982 respectively. The Loma slope value for cadaverine (−2.085) was lower than that for putrescine (−one.49), indicating that for the same increase in concentration, a greater cytotoxic effect was seen with cadaverine than with putrescine.

Figure 2
figure 2

Dose-response curves for putrescine and cadaverine in HT29 abdominal cells. Cell cultures were exposed to a range of putrescine (A) or cadaverine (B) concentrations for 24 h. The curves were made by plotting the normalized cell index at 24 h of treatment obtained using RTCA, against the log10 value of the corresponding BA concentration. The information represent the means ± standard deviations of at least three independent experiments. An asterisk indicates the first significant divergence with respect to the smallest dose of BA assayed (0.63 mM for both putrescine and cadaverine); it therefore corresponds to the LOAEL  (*p < 0.05). Numerical values for the IC50, NOAEL, LOAEL, Hill gradient and R2 are besides indicated.

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To determine the cytotoxicity of putrescine and cadaverine towards HT29 intestinal cells, the ICfifty values for each BA were adamant at 8 h, 12 h, 18 h and 24 h (Table 1). The concentrations of putrescine and cadaverine required to crusade half of the strongest cytotoxic effect observed in RTCA were progressively reduced with increasing incubation fourth dimension. The IC50 values indicate that putrescine and cadaverine were similarly cytotoxic (IC50 for putrescine later on 24 h of handling 39.76 ± 4.83 mM, compared to forty.72 ± 1.98 mM for cadaverine). The NOAEL and LOAEL values for putrescine were 5 mM and 10 mM respectively, while for cadaverine they were 2.5 mM and 5 mM respectively (Fig. 2). The cytotoxicity threshold for cadaverine would therefore appear to be twice that of putrescine for HT29 cell cultures nether the present experimental conditions.

Table 1 IC50 values (mean ± standard deviation) for putrescine and cadaverine determined after exposure of HT29 abdominal cells to these BA for different lengths of time.

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Microscopic examination of putrescine- and cadaverine-treated cell cultures

Effigy 3 shows the cytotoxic effects of different concentrations of putrescine and cadaverine on the HT29 cells. Concentrations for either BA below 20 mM had no consequence on the morphology of the cells, or the number of cells. Nonetheless, concentrations approximately higher up 20 mM acquired an apparent progressive reduction in jail cell numbers and a gradual modification of cell morphology, confirming the dose-dependent cytotoxicity of both BA.

Figure 3
figure 3

Toxicity towards HT29 cells of putrescine and cadaverine. HT29 cells were grown in apartment-bottomed microplates for 20 h, then exposed to increasing amounts of (A) putrescine (five, 20, twoscore, sixty and 100 mM) or (B) cadaverine (v, 20, 40, seventy and 90 mM) for 24 h. Cells were observed using an inverted optical microscope (magnification 40x).

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Style of activity of putrescine and cadaverine

Neither putrescine nor cadaverine induced the formation of intracellular Dna fragments (a typical feature of apoptotic cells) in the cell cultures, either at their ICfifty concentrations (0.97 ± 0.58% and 0.35 ± 0.43% DNA fragmentation for putrescine and cadaverine respectively) or at college concentrations (3.6 ± i.16% and 3.6 ± ane.27% DNA fragmentation for 80 mM putrescine and 70 mM cadaverine respectively) (no further information shown). Assays were therefore performed to measure the release of the cytosolic enzyme lactate dehydrogenase (LDH) into the medium to determine whether necrosis occurred. Figure 4A and B testify the percentage cytolysis of the jail cell cultures exposed to increasing concentrations of putrescine and cadaverine respectively. Those exposed to putrescine concentrations beneath 80 mM, or cadaverine concentrations below 70 mM, showed negligible LDH activity. Above these concentrations, however, a dose-dependent increase in LDH activity was observed for both BA. Some 50.vi% cytolysis was recorded in cultures exposed to the highest putrescine concentration tested (160 mM), and about 77.3% in cultures exposed to the highest cadaverine concentration tested (150 mM). Together, these results propose putrescine and cadaverine have a necrotic rather than an apoptotic mode of cytotoxic action on these intestinal cells in civilization.

Figure 4
figure 4

Determination of the cytolytic consequence of putrescine (A) and cadaverine (B) on HT29 intestinal cells. RTCA jail cell civilisation supernatants were collected after 24 h of incubation with the respective concentration of putrescine or cadaverine. BA-induced necrosis was monitored as the release of cytosolic lactate dehydrogenase (LDH) into the culture medium. The data correspond the percentage of cells lysed by handling with different concentrations of putrescine or cadaverine. Data represent the means of at least three contained experiments; vertical bars stand for standard deviations.

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Word

The nowadays results indicate putrescine and cadaverine to have a dose-dependent cytotoxic consequence towards HT29 intestinal cells in culture. The cytotoxicity threshold for cadaverine was higher than that of putrescine; although their IC50 values were comparable, the NOAEL and LOAEL values for cadaverine were lower than those recorded for putrescine. To our cognition, this is the starting time study of the ICfifty, NOAEL and LOAEL values for putrescine and cadaverine for in vitro cultures of an intestinal cell line. Recently, the values for these toxicological variables were RTCA-assessed for tyramine and histamine31. The comparing of the ICl, NOAEL and LOAEL values for putrescine and cadaverine with those recorded for tyramine and histamine31 indicates the former pair of BA to be less cytotoxic than the latter. Indeed, after 24 h of treatment, putrescine and cadaverine were approximately x-times less cytotoxic to abdominal cells in culture than recorded for tyramine (IC50 putrescine 39.76 ± four.83 and twoscore.72 ± 1.98 mM for cadaverine, compared to iii.2 ± 0.04 mM for tyramine31) and approximately ane.5 times less cytotoxic than histamine (ICfifty histamine 26.0 ± 1.two mM31). These data confirm and quantify the lesser toxicity assigned to these BA compared to histamine and tyramine, the almost toxic of all dietary BA12.

Although the cytotoxic mode of activity of putrescine and cadaverine was necrotic, as previously established for tyramine31, the per centum cytolysis caused by similar concentrations was much higher in tyramine-treated cells31. This further supports the bottom cytotoxicity of putrescine and cadaverine compared to tyramine. Further, while histamine caused the apoptosis of cell cultures31, negligible apoptotic DNA fragmentation was seen with putrescine and cadaverine. The necrotic effect of putrescine towards the HT29 intestinal prison cell cultures might be explained by its polycationic nature at physiological pH; this might allow it to interact with phospholipids (of anionic nature) and destabilize prison cell membranes32,33. A like caption might exist proposed for the necrotic effect of cadaverine.

Our grouping recently reported the in vitro model used in this work to be helpful for estimating the chance of toxicity later on the consumption of tyramine and histamine individually31 and in combination30. The nowadays work too shows information technology to allow estimations for the risk of toxicity after the consumption of putrescine and cadaverine. The literature contains no human dose-response data for nutrient-borne putrescine or cadaverine, and only one fauna study has been performed12,14. Consequently, no legal limit has been established for putrescine in whatever food, fifty-fifty though this BA may accumulate at very loftier concentrations in cheese (up to 1560 mg/kg), fermented sausages (up to 1550 mg/kg), and fish sauces (upwards to 1220 mg/kg)12 - levels much college than the lowest concentration of putrescine plant to be cytotoxic in this work (LOAEL = x mM, equivalent to 881.l mg/kg). These concentrations might therefore be considered hazardous to human health.

Similarly, no legal limit has been established for cadaverine in any nutrient either12, even though it too may accrue at very high concentrations in cheese (up to 3170 mg/kg), fish and fish products (up to 1690 mg/kg), fermented sausages (upwards to 1250 mg/kg) and fish sauces (up to 1150 mg/kg). In these foods, the cadaverine concentration reached tin be much college than the lowest concentration found to be cytotoxic in the present work (LOAEL = 5 mM, equivalent to 510.89 mg/kg). These concentrations might therefore too be considered hazardous for human health.

The loftier sensitivity of the in vitro model used in this study allowed to accurately estimate the NOAEL values for putrescine (5 mM, equivalent to 440.75 mg/kg) and cadaverine (ii.5 mM, equivalent to 255.45 mg/kg), which were more than four and 7 times lower respectively than that obtained in oral toxicity studies performed in rats fed with diets containing putrescine or cadaverine, in which the NOAEL values for both BA were set at 2000 mg/kgfourteen.

Given the possible potentiating effect of putrescine and cadaverine on the toxicity of other BA such every bit histamine and tyramine16,19, the threshold limits assigned for them should perchance be even lower. Neither should it be forgotten that the toxicity of putrescine and cadaverine might be increased in certain consumers as a result of a reduced capacity to detoxify them (via a genetically or acquired impairment of amino oxidase activities). Children, elderly patients with gastrointestinal affliction, and individuals taking monoamine and diamine oxidase inhibitors might as well be at greater take a chance6,x,12.

The present results, plus those obtained in previous studies on tyramine and histamine30,31, advise that tyramine is the nearly cytotoxic of these BA, followed by histamine, cadaverine, and finally putrescine.

Conclusions

The results of this work show putrescine and cadaverine to be cytotoxic towards HT29 intestinal cell cultures at concentrations that can be hands reached in BA-rich foods. The IC50 value of putrescine was 39.76 ± 4.83 mM, while that of cadaverine was xl.72 ± 1.98 mM. The cytotoxicity threshold for cadaverine was twice that of putrescine; the LOAEL value for cadaverine was 5 mM while that for putrescine was 10 mM. These BA appear to exert their cytotoxic effects via the induction of necrosis rather than apoptosis. The nowadays results may be useful to safety regime in establishing legal limits for these BA in foods. This would help to foreclose consumers suffering adverse health furnishings.

Methods

Jail cell line and growth weather condition

The intestinal cell line HT29 (ECACC 91072201), derived from a man colorectal adenocarcinoma was used to provide an in vitro model of the abdominal epithelium. The cells were routinely cultured in McCoy'south 5a medium as described in Linares et al.31.

Real-time prison cell analysis

An xCelligence Real-Time Cell Analyzer (ACEA Bioscience Inc., San Diego, CA, United states of america) was used as previously described31 to detect changes in the HT29 cells following their treatment with unlike concentrations of putrescine (ane,4-diaminobutane dihydrochloride) (Sigma-Aldrich, Madrid, Spain) or cadaverine (1,5-diaminopentane dihydrochloride) (Sigma-Aldrich).

In brusk, HT29 cells were seeded at a density of two × 104 cells/well in 16-well Due east-Plates (ACEA Biosciences Inc.) containing 100 µl of medium per well, and then incubated and monitored in a Heracell-240 Incubator (Thermo Electron LDD GmbH, Langenselbold, Federal republic of germany) at 37 °C under a 5% CO2 temper31. Stock solutions of putrescine and cadaverine were dissolved in water and adjusted to pH vi.9. Approximately 20 h later seeding, the cells were treated with one of fifteen concentrations of putrescine (0 to 160 mM) or cadaverine (0 to 150 mM). The final volume of civilisation media supplemented with BA was 200 µl per well. The jail cell index was monitored for 24 h; this was normalized to the fourth dimension point just previously the addition of the BA and fix to one. For each status, measurements were washed in triplicate.

Dose-response curves for putrescine and cadaverine were made past plotting the normalized cell alphabetize at 24 h of treatment (obtained using RTCA software 1.2.1; ACEA Biosciences Inc.) against the log10 value of the corresponding BA concentration (0.63, 1.25, 2.50, five, 10, 12.5, 15, 17, 20, 30, 40, sixty, 80, 100, 120 and 160 mM for putrescine and 0.63, 1.25, 2.fifty, 5, ten, fifteen, twenty, 25, 30, twoscore, 50, lx, 70, 80, 90, 100 and 150 mM for cadaverine). Non-linear regression trend lines were fitted to sigmoid dose-response (variable slope) curves using SigmaPlot thirteen.0 software (Systat Software Inc., San Jose, CA, United states). This software was likewise used to determine the coefficient of decision (R2), which indicates the goodness of the adjustment of the experimental information to the bend, as well every bit the Hill slope value, which shows the steepness of the curve.

The IC50 values for putrescine and cadaverine were calculated at different arbitrary time points (8 h, 12 h, 18 h and 24 h) of BA exposure every bit described in Linares et al.31.

Live prison cell microscopy

Cells were seeded at a density of 2 × 104 cells/well and incubated in flat-bottomed 96-well microplates nether the same conditions to those used in the RTCA studies. Later on 24 h of incubation, the cells were treated with concentrations of putrescine (5, 20, 40, lx and 100 mM) and cadaverine (5, 20, 40, 70, 90 mM). At 24 h post-treatment, live cells were observed using an inverted LumaScope-600 Series optical microscope (Etaluma, Carlsbad, CA, USA) with a 40x objective.

Prison cell apoptosis

The Cellular Dna Fragmentation ELISA Kit (Roche Practical Science, Federal republic of germany) was used to measure apoptosis-associated DNA fragments in the cytoplasm. DNA-fragmentation in BA-treated samples was determined as described in Linares et al.31 with some modifications [proliferating cells were exposed for 24 h to BA doses similar to the ICl (35.48 mM for putrescine and 41.03 mM for cadaverine), and above the ICfifty (80 mM for putrescine and 70 mM for cadaverine)]. Positive and negative controls were performed as described in Linares et al.31. Dna fragmentation in the BA-treated samples was indicated every bit a percentage of the value for the positive controls.

Prison cell lysis assay

The presence of LDH activeness in RTCA prison cell civilization supernatants collected after 24 h of incubation with the respective dose of putrescine or cadaverine, was tested equally an indicator of prison cell lysis, using the Cytoscan Cytotoxicity Assay Kit (Chiliad Biosciences, St. Louis, MO, United states of america) post-obit the manufacturer's instructions. Negative (no lysis reagent) and positive (with lysis reagent) controls were performed simultaneously. The percentage of cells lysed was determined as follows: 100 × [(492 nm absorbance of BA-treated samples − absorbance of negative control)/(absorbance of positive control − absorbance of negative control)].

Data and statistical assay

The results of the different experiments were indicated as the hateful ± standard deviation of three independent replicates. Statistical handling involved ANOVA followed by Fisher's least significant deviation exam, performed using SigmaPlot software. Significance was set at p < 0.05 (indicated in figures with an asterisk).

The NOAEL value was identified as the highest concentration of BA that acquired no detectable agin effect on the target cells; the LOAEL value was divers as the lowest concentration of BA that produced a detectable adverse issue31.

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Acknowledgements

This piece of work was funded by the Spanish Ministry of Economy and Competitiveness (AGL2016-78708-R and AGL2015-64901-R). The authors thank Adrian Burton for linguistic help.

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Affiliations

  1. Dairy Enquiry Institute, IPLA-CSIC, Paseo Rio Linares s/n, 33300, Villaviciosa, Spain

    Beatriz del Rio, Begoña Redruello, Daniel 1000. Linares, Victor Ladero, Patricia Ruas-Madiedo, Maria Fernandez, Chiliad. Cruz Martin & Miguel A. Alvarez

Contributions

B.d.R. performed the experiments, participated in data interpretation and drafted the manuscript. B.R. and D.M.L. collaborated in the realization of some of the experiments and participated in data interpretation. P.R.M. carried out the maintenance of HT29 cell cultures. 5.L., Chiliad.F. and M.C.G. participated in data interpretation. Thou.A.A. provided the general concept, participated in study design, data interpretation, supervised the work and revised the manuscript. All authors contributed to the discussion of the research and approved the concluding manuscript.

Corresponding author

Correspondence to Beatriz del Rio.

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del Rio, B., Redruello, B., Linares, D.Yard. et al. The biogenic amines putrescine and cadaverine evidence in vitro cytotoxicity at concentrations that can be found in foods. Sci Rep 9, 120 (2019). https://doi.org/10.1038/s41598-018-36239-due west

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  • DOI : https://doi.org/x.1038/s41598-018-36239-w

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