Determination of Phenolic Compounds

in Three Edible Ripening Stages of Yellow

Guava (Psidium cattleianum Sabine) after
Acidic Hydrolysis by LC-MS/MS

Mayara Schulz, Siluana Katia Tischer

Seraglio, Fabiana Della Betta, Priscila
Nehring, Andressa Camargo Valese,
Heitor Daguer, et al.
Plant Foods for Human Nutrition

ISSN 0921-9668

Plant Foods Hum Nutr

DOI 10.1007/s11130-019-00792-0

1 23
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 Author's personal copy
Plant Foods for Human Nutrition
https://doi.org/10.1007/s11130-019-00792-0

ORIGINAL PAPER

Determination of Phenolic Compounds in Three Edible Ripening

Stages of Yellow Guava (Psidium cattleianum Sabine) after Acidic
Hydrolysis by LC-MS/MS
Mayara Schulz 1 & Siluana Katia Tischer Seraglio 1 & Fabiana Della Betta 1 & Priscila Nehring 1 &
Andressa Camargo Valese 2 & Heitor Daguer 2 & Luciano Valdemiro Gonzaga 1 & Ana Carolina Oliveira Costa 1 &
Roseane Fett 1

# Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract
Yellow guava (Psidium cattleianum Sabine) has received considerable attention in the last years because of their high content in
bioactive compounds with potential application in food and pharmaceutical industries. In this regard, this study aimed to
investigate the phenolic compounds of three edible ripening stages of yellow guava fruits after acidic hydrolysis by liquid
chromatography-tandem mass spectrometry (LC-MS/MS) and their antioxidant capacity. Among the 23 phenolics quantified,
catechin, isoquercitrin, quercetin, gallic acid, and syringic acid showed significant concentrations in all the evaluated stages, with
values ranging from 479.59 ± 12.52 to 12,795.50 ± 320.95 μg 100 g−1 of dry matter. In general, higher concentrations of phenolic
acids were found in the latter ripening stages, while flavonoids were in the earlier ripening stages. These findings suggest that the
ripening process promotes changes in the phenolic composition of yellow guava. However, considering the sum of phenolic
compounds and the antioxidant capacity, all ripening stages investigated can be suggested as a supply of bioactive compounds for
consumers.

Keywords Araçá . Fruits . Maturation . Bioactive compounds . Antioxidant

Introduction known as araçá-amarelo, yellow strawberry guava, and yellow

Brazil is considered one of the main genetic centers of diver-
sity of fruit species in the world. However, most of these
species remain unexplored and their potential unknown [1].
Yellow guava (Psidium cattleianum Sabine, Myrtaceae), also
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s11130-019-00792-0) contains supplementary
material, which is available to authorized users.
* Mayara Schulz
schulzmay@gmail.com
* Roseane Fett
roseane.fett@gmail.com
1
Department of Food Science and Technology, Federal University of
Santa Catarina, Florianópolis, SC 88034-001, Brazil
2
Livestock, and Food Supply, Brazilian Ministry of Agriculture, São
José, SC 88102-600, Brazil
cattley guava, is a fruit with shiny yellowish peel and a fleshy
and whitish pulp with many small seeds [2, 3]. This fruit is native
from sub-tropical Brazil and it has promising potential [4].
Studies carried out with this fruit found high antioxidant
capacity, antidiabetic, anticarcinogenic, antimicrobial, anti-in-
flammatory, and antiaging effects [3–5]. Furthermore, the
presence of carotenoids such as trans-β-cryptoxanthin, all-
trans-β-carotene, and all-trans-lutein [2], as well as free phe-
nolic compounds, especially catechin, epicatechin,
isoquercitrin, ellagic acid, quercetin, epicatechin gallate,
taxifolin hexoside, vanillic acid hexoside, and gallic acid were
reported [2, 4–6].
Phenolic compounds are known as the main responsibles
for the antioxidant properties of fruits, due to their high oxida-
tion and reduction potential assigned to their chemical struc-
tures [7]. These compounds are found in the free form or
bound to sugars (glycosides) or other compounds, influencing
its bioactive potential [7]. In this way, analytical procedures,
such as the hydrolysis method, can significantly affect contents
 Author's personal copy
and types of phenolic compounds. These compounds can be
hydrolyzed using an acid or an alkali to release hydrolysable
phenolics [8], which no information in literature could be
found for yellow guava.
Additionally, the phenolic compounds profile and concen-
tration may vary depending on the type of plant, genetic fac-
tors, environmental conditions, and ripening process [9].
During ripening, phenolic compounds undergo a series of
processes of biosynthesis and degradation, leading to changes
in its composition [10].
Therefore, the phenolic composition and antioxidant ca-
pacity of yellow guava (Psidium cattleianum Sabine) fruit
were investigated to provide information regarding changes
in the bioactive potential of this fruit at different edible ripen-
ing stages.
Materials and Methods
Reagents and Solutions
Ascorbic acid, anhydrous sodium sulfate, citric acid, and
hydrochloric acid were acquired from Vetec (Duque de
Caxias, RJ, Brazil). Methanol and acetonitrile were obtained
from Merck (Darmstadt, Germany). Ethyl acetate, formic
acid, 2,2-diphenyl-1-picrylhydrazil (DPPH), ascorbic acid,
2,4,6-tris(2-pyridil)-s-triazine (TPTZ), ferric chloride, and
ultra-pure standard of apigenin, isorhamnetin, pinobanksin,
ferulic acid, sinapic acid, p-aminobenzoic acid, p-coumaric
acid, 4-methylumbelliferone, vanillic acid, rutin, naringin,
(+)-catechin, sinapaldehyde, caffeic acid, chlorogenic acid,
coniferaldehyde, syringaldehyde, chrysin, hesperidin,
syringic acid, kaempferol, naringenin, (−)-epigallocatechin
gallate, (−)-epicatechin, pinocembrin, galangin, salicylic ac-
id, quercetin, gallic acid, benzoic acid, 3,4-dihydroxybenzoic
acid, isoquercitrin, and luteolin were purchased from Sigma-
Aldrich (St. Louis, MO, USA). All reagents used in this
study were of analytical grade and ultra-pure water was ob-
tained from a Milli-Q system (Millipore, Bedford, MA,
USA).
Samples
Fruits of yellow guava (Psidium cattleianum Sabine) were
harvested in Pinhalzinho, Santa Catarina State, Brazil (latitude
26o 85′02”S, longitude 52o 98′17”W, altitude 515 m), in
January 2015. Fruits with intact exocarp were manually col-
lected from three randomly selected plants and were divided
into three edible ripening stages namely less mature, mature,
and fully mature. These ripening stages were defined accord-
ing to the skin colour (Fig. 1) and total soluble solids/total
titratable acidity ratio (Supplementary material 1). Samples
were packed in polyethylene bags under nitrogen atmosphere,
Plant Foods Hum Nutr
hermetically sealed, and stored at −18 ± 2 °C until analysis.
Samples were thawed at 4 ± 2 °C, seeds and peduncles were
removed and discarded, edible portions were grinded and ho-
mogenized in a domestic food processor.
Phenolic Compounds Characterization by LC-MS/MS
The extraction of the phenolic compounds were performed
according to the acidic hydrolysis method described by
Seraglio et al. [11], using the following procedure: 1.0 ±
0.1 g of the sample was mixed with ascorbic acid (final con-
centration 2.22 mg mL−1) and manually stirred for 1 min. An
aliquot of HCl (5 mL, 6 mol L−1) was added to the mixture and
incubated at 85 ± 2 °C in an oven (Greenhouse Labor SP-400/
1, São Paulo, SP, Brazil) for a period of 30 min. After cooling,
the extract was sequentially extracted for three times with
5 mL of ethyl acetate for 1 min and centrifugated (5 min/
1338 x g) (Fanem, model 280R, São Paulo, Brazil). The su-
pernatants were combined, dried with anhydrous sodium sul-
fate (3 g) and evaporated under low pressure (Fisatom 802,
São Paulo, SP, Brazil). The extract was reconstituted in 1 mL
of methanol, diluted 1:9 (v/v) with the mobile phase for LC-
MS/MS analysis. Subsequent dilutions were performed when
necessary.
The determination of 33 individual phenolic compounds
was carried out by method of Seraglio et al. [11] using an
Agilent 1290 series liquid chromatographic system (Agilent
Technologies, Waldbronn, Germany) coupled to the hybrid
quadrupole linear ion trap mass spectrometer QTRAP®
5500 from Sciex (Framingham, MA, USA) with an
electrospray ionization source (ESI). The acquisition data
was performed in multiple reaction monitoring (MRM) in
the positive and negative modes simultaneously and the best
ionization mode was chosen for each phenolic compound.
Mass spectrometry parameters for MRM transitions mode,
detection and quantification limits, and calibration curves for
the phenolic compounds are shown in Supplementary material
2. The results were expressed in μg 100 g−1 of dry matter
(DM).
Antioxidant Capacity
For the determination of antioxidant capacity, the extrac-
tion procedure was performed according to Seraglio et al.
[11]. The DPPH assay was done according to the method
of Kim et al. [12]. The antioxidant capacity was calculated
as inhibition percentage and expressed as mg acid ascorbic
equivalent g−1 of DM. The FRAP assay was determined
according to the method described by Arnous et al. [13]
and the results expressed as μmol ascorbic acid equivalent
g−1 of DM.
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Plant Foods Hum Nutr
Fig. 1 Total ion chromatogram of less mature (a), mature (b), and fully
mature (c) Psidium cattleianum (yellow guava) (1 – gallic acid; 2 – p-
aminobenzoic acid; 3–3,4-dihydroxybenzoic acid; 4 – chlorogenic acid; 5
– (+)-catechin; 6 – caffeic acid; 7 – (−)-epicatechin; 8 – syringic acid; 9 -
(−)-epigallocatechin gallate; 10 – p-coumaric acid; 11 – isoquercitrin; 12
Statistical Analysis
Mean values (± standard deviation) of the studied variables
were presented. Data were submitted to variance analysis
(ANOVA) and the mean values compared by the Tukey’s test
at p < 0.05 using the Statistica 13.0 software (Statsoft Inc.,
Tulsa, OK, USA).
Results and Discussion
Thirty-three phenolic compounds, including coumarins, fla-
vonoids, lignin-derived aldehydes, and phenolic acids, were
investigated in yellow guava fruits in three edible ripening
stages after acidic hydrolysis and their contents are shown in
Table 1. Of all the investigated phenolics compounds, 23 were
identified and quantified in at least one ripening stage, and 15
were found in the three ripening stages (Fig. 1). Eight phenolic
compounds (4-methylumbelliferone, chrysin, galangin,
hesperidin, pinocembrin, rutin, naringin, and vanillic acid)
were not detected and two compounds (apigenin and p-
aminobenzoic acid) were detected but were under the limits
of quantification (LOQ).
Catechin was the main phenolic found in the three stages of
yellow guava, ranging from 10,880.74 ± 532.15 to 12,795.50
± 320.95 μg 100 g−1 DM. Isoquercitrin, quercetin, gallic acid,
and syringic acid were also found in high levels, ranging from
479.59 ± 12.52 to 3158.31 ± 28.34 μg 100 g−1 DM. In a pre-
vious study, Betta et al. [5] assessed the content of free phe-
nolic compounds in two edible stages of yellow guava and
found that catequin, isoquercitrin, and gallic acid were present
– syringaldehyde; 13 – sinapic acid; 14 – ferulic acid; 15 – sinapaldehyde;
16 – coniferaldehyde; 17 – benzoic acid; 18 – salicylic acid; 19 – luteolin;
20 – quercetin; 21 – apigenin; 22 – naringenin; 23 – pinobanksin; 24 –
kaempferol; 25 – isorhamnetin)
in higher concentrations in mature samples. When the free
phenolics were assessed, nine compounds were quantified,
while in this study after the acidic hydrolysis 23 phenolics
were quantified in at least one stage. Similarly, Colak et al.
[14] found a higher number of phenolics in bog bilberry ana-
lyzed after acidic hydrolysis over the analysis of free phenolic
compounds. This increase in the number of phenolic com-
pounds may be related to the acidic hydrolysis applied. This
procedure becomes an interesting process as it allows the re-
lease of phenolic compounds bound to other components of
the food matrix, which would not be determined otherwise
[15]. However, this process also results in the hydrolysis of
glycosylated phenolic compounds, which are less bioavailable
than their aglycone form [16]. It is interest to note that among
the glycosylated phenolic compounds evaluated, only
isoquercitrin was quantified after the acid hydrolysis. This fact
could be associated to an incomplete hydrolysis of this com-
pound. The presence of isoquercitrin in jambolan, jabuticaba
and guabiju fruits after acid hydrolysis was also reported by
Seraglio et al. [11]. Also, the study of Betta et al. [5] evaluated
free phenolic compounds in yellow guava and observed
isoquercitrin concentration much higher than those found in
the present study, suggesting that this compound was partially
hydrolyzed after acid hydrolysis.
Other studies in the scientific literature corroborate our
findings. Arnous et al. [13] also found epicatechin, gallic acid,
isoquercitrin, catechin, and quercetin as the main compounds
of Psidium cattleianum juices. Epicatechin and gallic acid
were the most abundant phenolics found by Teixeira et al.
[17] in different genotypes of yellow guava. The presence of
isoquercitrin as one of the major phenolic compounds in
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Plant Foods Hum Nutr

Table 1 Content of phenolic

compounds (μg 100 g−1 of dry Yellow guava
matter) after acid hydrolysis and
antioxidant capacity by DPPH Less mature Mature Fully mature
(mg ascorbic acid equivalent g−1
of dry matter) and FRAP methods Flavonoids
(μmol ascorbic acid equivalent Apigenin <LOQ <LOQ <LOQ
g−1 of dry matter) in yellow guava
(+)-Catechin 11,424.20 ± 561.23a 10,880.74 ± 532.15a 12,795.50 ± 320.95a
(Psidium cattleianum Sabine)
fruits in three edible ripening (−)-Epigallocatechin gallate 32.99 ± 0.51 ND ND
stages (+)-Epicatechin ND ND 22.34 ± 0.97
Isoquercitrin 3158.31 ± 28.34a 2622.13 ± 449.93a 1194.60 ± 1.76b
Isorhamnetin 29.46 ± 2.32b 179.91 ± 18.23a 34.33 ± 1.97b
Kaempferol 32.85 ± 3.42b 228.97 ± 10.57a 32.70 ± 1.94b
Luteolin 127.55 ± 7.41 ND ND
Naringenin 24.93 ± 4.42a 26.16 ± 0.88a 28.00 ± 0.56a
Quercetin 1833.67 ± 240.90a 1118.72 ± 17.64b 1038.77 ± 73.11b
Pinobanksin 29.14 ± 1.98a 30.90 ± 0.06a 34.33 ± 0.92a
Lignin-derived aldehydes
Coniferaldehyde 23.07 ± 0.45b 32.10 ± 1.51a 19.86 ± 0.51b
Sinapaldehyde 17.02 ± 1.66a 22.27 ± 0.74a 18.34 ± 1.96a
Syringaldehyde 55.42 ± 2.31b 80.22 ± 0.87a 46.79 ± 1.19c
Phenolic acids
p-Aminobenzoic acid <LOQ <LOQ <LOQ
Benzoic acid <LOQ <LOQ 293.53 ± 27.41
Caffeic acid <LOQ <LOQ 54.28 ± 2.03
Chlorogenic acid 18.13 ± 0.49a 11.87 ± 2.15b 8.74 ± 0.17b
p-Coumaric acid 53.69 ± 6.13a 90.31 ± 14.85a 63.00 ± 5.55a
3,4-Dihydroxybenzoic acid 64.06 ± 1.94b 88.81 ± 3.91a 75.60 ± 4.31ab
Ferulic acid <LOQ 124.56 ± 0.33a 79.28 ± 4.61b
Gallic acid 532.61 ± 19.76c 781.93 ± 66.75b 1542.01 ± 75.63a
Salicylic acid <LOQ 29.46 ± 0.79a 30.42 ± 0.92a
Sinapic acid <LOQ 20.84 ± 1.35b 24.74 ± 0.04a
Syringic acid 585.83 ± 9.04a 598.29 ± 7.09a 479.59 ± 12.52b
Sum of phenolic compounds 18,042.93 ± 781.10a 16,968.19 ± 852.82a 17,916.77 ± 114.60a
Antioxidant capacity
DPPH 19.69 ± 0.65a 20.01 ± 0.84a 18.46 ± 0.32a
FRAP 34.23 ± 0.80a 35.73 ± 1.05a 33.57 ± 0.79a

Results expressed as mean ± standard deviation; a-c Mean values in the same row followed by different letters
indicate significant difference (p < 0.05) by Tukey test; ND – not detected; LOQ – limit of quantification; DPPH –
2,2-diphenyl-1-picrylhydrazyl radical; FRAP – ferric reducing antioxidant power

yellow and red guava cultivars was also reported by
Biegelmeyer et al. [18]. The presence of catequin,
isoquercitrin, and gallic acid were also the main compounds
found in other underexploited fruits cultivated in Brazil, such
as jabuticaba, jambolão, guabiju [11], taperabá, caju, acerola,
açaí-do-amazonas [19].
As shown in Table 1, the different ripening stages influ-
enced the profile and concentration of most phenolic com-
pounds in yellow guava fruits. Lower amounts of phenolic
compounds were observed for the different stages. The con-
centration of isoquercitrin and syringic acid was similar for the
two first stages, but lower for the fully mature stage. For
quercetin and chlorogenic acid, the highest content was found
in the less mature stage, lower for the two follow stages. In
addition, epigallocatechin gallate and luteolin were quantified
only in the less mature stage. The absence of these phenolic
compounds in the mature and fully mature stages may be
associated to the formation of new phenolic compounds. In
the case of luteolin, compounds such as flavone chrysoeriol,
luteolin-7-O-D-glucuronide and luteolin-7-O-D-glucoside
may be formed, while epigallocatechin gallate may have been
hydrolyzed to gallic acid, for example [20, 21].
On the other hand, the content of epicatechin and gallic,
benzoic, sinapic, and caffeic acids increased. Gallic acid and
 Author's personal copy
Plant Foods Hum Nutr
ellagic acid and their derivatives are reported as the main
phenolic compounds in yellow guava fruits [2, 6, 22]. The
increase of epicatechin during ripening was also reported by
Karaaslan et al. [23] for sour cherry. In fact, this increase may
be related to the hydrolysis of complex tannins, in which a
catechin or epicatechin unit has a glycosidic bound to a
gallotannin or an ellagitannin unit, and through hydrolysis,
complex tannins yield catechin or epicatechin and gallic or
ellagic acid [24].
For some phenolic compounds, higher contents were ob-
served in the mature stage. The highest content of
isorhamnetin, kaempferol, coniferaldehyde, syringaldehyde
and ferulic acid was found in this stage. For 3,4-
dihydroxybenzoic and salicylic acids, an increase was ob-
served in the mature stage compared with the less mature stage,
but did not differed to the fully mature stage (p > 0.05). For
catechin, naringenin, pinobanksin, sinapaldehyde and p-
coumaric acid, their contents were similar for all samples.
In general, it was observed that the phenolic compounds
might undergo complex changes (biosynthesis and degrada-
tion), which can influence their profile and concentration in
the fruits at different stages of maturation. In most cases, great-
er variations are generally dependent on the type of phenolic
and its metabolic pathway [10].
From the sum of the phenolic compounds quantified in the
yellow guava (Table 1), it can be observed that regardless of
the edible stage, this fruit presents relevant concentrations of
these compounds, varying from 16,968.19 to 18,042,93 μg
100 g−1 DM during ripening. Such values are higher than
those found for other fruits as blackberry [25] and acerola
[26], which are recognized sources of phenolics.
As for the sum of the phenolic compounds, the antioxidant
capacity did not differ statistically between the samples
(Table 1), reinforcing the bioactive potential of yellow guava
in the three edible ripening stages.
Conclusion
Individual phenolic compounds of yellow guava fruit were
investigated to provide information regarding quality bioac-
tive of this fruit at different edible ripening stages. After acidic
hydrolysis, 23 phenolic compounds were quantified and sig-
nificant concentrations of catechin, isoquercitrin, quercetin,
gallic acid, and syringic acid were found in the three stages
evaluated. In general, the highest concentrations of phenolic
acids were found in the fruits of the stages mature and fully
mature, while for flavonoids the highest values were generally
observed in the stages less mature and mature. However, con-
sidering the sum of phenolic compounds and the antioxidant
capacity, all ripening stages investigated can be suggested as a
supply of bioactive compounds and contribute with benefit to
human health.
Acknowledgments This study was financed in part by the Coordenação
de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) –
Finance Code 001. Authors also wish to thank the Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq) and the Cabanha
Seraglio.
Compliance with Ethical Standards
Conflict of Interest The authors declare that they have no conflict of
interest.
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