Received: 17 February 2020 Revised: 23 May 2020 Accepted: 11 June 2020

DOI: 10.1111/1541-4337.12600

COMPREH ENSIVE REVIEWS IN FOOD SCIENCE AND FOOD SAFETY

Fish Quality Index Method: Principles, weaknesses,

validation, and alternatives—A review

Yago A. A. Bernardo1,2 Denes K. A. Rosario2,3 Isabella F. Delgado1

Carlos A. Conte-Junior1,2,3,4

1Post Graduate Program in Sanitary

Surveillance, National Institute of Health Abstract
Quality Control, Oswaldo Cruz Fish is a high nutritional value matrix of which production and consumption
Foundation, Rio de Janeiro, Brazil
have been increasing in the last years. Advancements in the efficient evaluation
2Center for Food Analysis, Technological
Development Support Laboratory
of freshness are essential to optimize the quality assessment, to improve con-
(LADETEC), Avenida Horácio Macedo, sumer safety, and to reduce raw material losses. Therefore, it is necessary to use
Polo de Química, Ilha do Fundão, Cidade rapid, nondestructive, and objective methodologies to evaluate the quality of this
Universitária, Rio de Janeiro, Brazil
3 Post Graduate Program in Food Science,
matrix. Quality Index Method (QIM) is a tool applied to indicate fish freshness
Institute of Chemistry, Federal University through a sensory evaluation performed by a group of assessors. However, the
of Rio de Janeiro, Av. Athos da Silveira use of QIM as an official method for quality assessment is limited by the pro-
Ramos, 149, Cidade Universitária, Rio de
tocol, sampling size, specificities of the species, storage conditions, and asses-
Janeiro, Brazil
4Post Graduate Program in Veterinary
sor’s experience, which make this method subjective. Also, QIM may present
Hygiene, Faculty of Veterinary Medicine, divergences regarding the development of microorganisms and chemical analy-
Fluminense Federal University, Vital sis. In this way, novel quality evaluation methods such as electronic noses, elec-
Brazil Filho, Niterói, Rio de Janeiro,
Brazil tronic tongues, machine vision system, and colorimetric sensors have been pro-
posed, and novel technologies such as proteomics and mitochondrial analysis
Correspondence
have been developed. In this review, the weaknesses of QIM were exposed, and
Carlos Adam Conte Junior, Avenida Athos
da Silveira Ramos, n◦ 149, Bloco A, Sala novel methodologies for quality evaluation were presented. The consolidation of
545. Cidade Universitária, Zip code: 21.941- these novel methodologies and their use as methods of quality assessment are an
909, Rio de Janeiro - RJ, Brazil.
alternative to sensory methods, and their understanding enables a more effective
Email: conte@iq.ufrj.br
fish quality control.
Funding information
Coordenação de Aperfeiçoamento KEYWORDS
de Pessoal de Nível Superior—Brazil Freshness State, Health Surveillance, Quality Index Method, Seafood, Sensory Analysis
(CAPES); Fundação de Amparo à Pesquisa
do Estado do Rio de Janeiro—Brazil
(FAPERJ), Grant/Award Numbers: E-
26/200.195/2020, E-26/203.049/2017, E-
26/010.000148/2020; Conselho Nacional
de Desenvolvimento Científico e Tec-
nológico, Grant/Award Numbers:
311422/2016-0, 140947/2019-1

1 INTRODUCTION to these attractive characteristics and other factors such as

reduced trade losses, improvement of utilization and dis-
Fish is a product composed of proteins with high bio- tribution, and population growth, it is estimated that per
logical value and is rich in vitamins A and D, minerals, capita fish consumption in Latin America will increase
and unsaturated fatty acids (Rodrigues et al., 2017). Due by 18% and that fishery will increase by up to 24.2% by

Compr Rev Food Sci Food Saf. 2020;19:2657–2676. wileyonlinelibrary.com/journal/crf3 © 2020 Institute of Food Technologists
R 2657
2658
2030 (FAO, 2018). However, fish is a highly perishable
matrix due to high levels of free amino acids and other
nonnitrogenous substances utilized as a source of nutri-
ents for microbial growth (Monteiro et al., 2018). Its pro-
tein composition has a large proportion of essential amino
acids, which although beneficial to consumer health,
present rapid deterioration. After the dissolution of rigor
mortis and the establishment of the process of autolysis,
endogenous proteases are some of the first enzymes to act,
promoting protein hydrolysis and leading to quality losses
(Delbarre-Ladrat, Chéret, Taylor, & Verrez-Bagnis, 2006).
Henceforth, the rapid and efficient control of the quality
of these products becomes a challenge for public health
authorities.
In order to evaluate the freshness and quality of fish,
some protocols have emerged for the detection and quan-
tifying changes in their sensory characteristics, such as
(i) the European Union Scheme (EC, 1996), (ii) the Torry
Scheme (Shewan, Macintosh, Tucker, & Ehrenberg, 1953),
and (iii) the Quality Index Method (QIM) (Bremner, 1985).
The European Union scheme classifies fish according to
its degree of freshness and observation of complemen-
tary characteristics, through specific parameter lists (EC,
1996). The Torry scheme evaluates the freshness of cooked
fish by assigning decreasing scores that range from 10 to
0 (Shewan et al., 1953) according to the sensorial evalu-
ation (Alasalvar, Taylor, Oksuz, Shahidi, & Alexis, 2002).
Nonetheless, the most commonly employed method to
evaluate freshness is the QIM.
According to Olafsdóttir et al. (1997), scores assigned by
QIM are accurate and impartial. However, it depends on
a few highly trained assessors as it is a sensory method.
Qualitative methods, such as QIM, are subject to sam-
pling size, storage conditions, and species specificity, lead-
ing to gaps in the protocol. Moreover, the bacteriological
validation showed controversial results (Baixas-Nogueras,
Bover-Cid, Veciana-Nogues, Nunes, & Vidal-Carou, 2003;
Sant’Ana, Soares, & Vaz-Pires, 2011), which limits its use as
an official method for fish quality assessment. Although
recent studies have shown QIM to be a useful device
(Ahmadi Shalhe, Khodanazary, & Hosseini, 2018; Ghani
Kuvei, Khodanazary, & Zamani, 2019; Khodanazary, 2019),
novel methods have been reported showing high perfor-
mance and being precision tools (Hassoun & Karoui, 2015;
Wu, Pu, & Sun, 2019). Notwithstanding, there is a lack
regarding the correlation between the use of these novel
methods and the sensory evaluation of fish. In addition,
important reviews have been published in the last decade
summarizing QIM schemes developed between 2000 and
2013 (Bernardi, Mársico, & Freitas, 2013) and between 2013
and 2017 (Ndraha, 2017). However, none of them depicted
the limitations by using QIM as a sensory method to estab-
lish fish quality. In this review, the principles, develop-
ment, and the main weaknesses of QIM are pointed, as
QIM—A COMPREHENSIVE REVIEW. . .
well as the statistical, chemical, and bacteriological vali-
dation of the sensory evaluation. Furthermore, the use of
this methodology as a tool of quality judgment is discussed,
and the use of novel tools for quality assessment were pro-
posed.
2 QIM
After harvesting, fish undergoes a complex process of
microbial and enzymatic activities, resulting in protein
degradation and lipid oxidation (Huidobro, Pastor, &
Tejada, 2000). This process leads to changes in sensory
and nutritional characteristics, as well as consumer rejec-
tion, making fish inappropriate for commercialization and
consumption (Ahmadi Shalhe et al., 2018). QIM is con-
sidered a practical and fast approach to assess the fresh-
ness and quality of fish (Sveinsdottir, Martinsdottir, Hyldig,
Jorgensen, & Kristbergsson, 2002). Introduced by the Tas-
manian Food Research Division (Bremner, 1985), QIM
attributes demerit points (from 0 to 3) adjusted to the
species being evaluated (Guillerm-Regost et al., 2006).
Scores closer to 0 indicate freshness, and scores closer to
3 indicate an advanced state of decay (Sveinsdottir et al.,
2002), denoting the appearance of fish parameters previ-
ously selected, directly related to sale and consumption
(Vaz-Pires & Seixas, 2006).
The development of the quality index (QI), an overall
sensory score, occurs in three stages (Figure 1), two steps
of training for the assessors and one validation step (Ritter
et al., 2016). In the first training step, the assessors monitor
the decay process and describe fish parameters that have
changed during storage (Ritter et al., 2016). The changes
are listed in a preliminary QI protocol, and each set is
punctuated from 0 to 3 (Guillerm-Regost et al., 2006). The
second training step is performed to confirm the listed
observations and to propose changes in the preliminary QI
protocol (Sant’Ana et al., 2011). The third step is the val-
idation of the QI protocol (Borges, Conte-Junior, Franco,
& Freitas, 2013). The main advantage of this method is
to provide a linear relationship between the freshness of
the evaluated species in relation to the time of ice stor-
age (Ritter et al., 2016), so that the minimum differences
attributed by the assessors to the same characteristic are
not able to influence the final result (Martinsdóttir, Sveins-
dóttir, Luten, Schelvis-Smit, & Hyldig, 2001). Moreover,
distinct protocols should be developed for different species
(Table 1), as each one has a specific quality standard.
The efficiency of QIM depends on several factors, such
as (i) the selection of the sensory parameters that will com-
pose the protocol, (ii) the sampling size (Marshall, 1996),
(iii) the species specificity (Lanzarin et al., 2016), (iv) the
storage conditions of the samples (Sant’Ana et al., 2011), (v)
the experience of the assessors (Ozogul, Ozyurt, Ozogul,
QIM—A COMPREHENSIVE REVIEW. . .
F I G U R E 1 The development of the 3 steps of QIM
Note. The main factors affecting the efficiency and reproducibility of the QIM were listed from i to vi. The alternative artificial methods were
listed from a to d. Abbreviations: AQI: artificial quality index; CSA: colorimetric sensor array; MVS: machine vision system; QIM: quality index
method
Kuley, & Polat, 2005), and (vi) the bacteriological and
chemical validation of the results (Nielsen & Green, 2007;
Sveinsdottir et al., 2002). These factors usually represent
high costs and especially compromise the reproducibility
of the QIM, resulting in controversial results even for sim-
ilar species, preventing its widespread use as an official
method for freshness assessment. Also, considering the
expected large world population, scientific advances in the
prediction of fish quality could overcome the limitations
of the QIM and thus optimize and protect food systems for
the future.
3 QIM’S WEAKNESSES
3.1 Gaps in the QI protocol
The parameters considered to compose the QI protocol
depend on the species to be evaluated and the information
obtained during the observation of the sensory changes in
the first and second steps (Bogdanović, Šimat, Frka-Roić,
& Marković, 2012). Through the QI protocol, it is possi-
ble to proceed to the third stage of determination. How-
ever, this protocol may present differences that generate
contradictory results. The first protocol evaluated for cut-
tlefish (Sepia officinalis) was described by Vaz-Pires and
Seixas (2006). These authors related that the decay state-
ment progressed according to the ice storage time through
the observation of nine parameters. The rejection of the
cuttlefish occurred on the 10th day of storage when demerit
2659
points totalized 17 (Vaz-Pires & Seixas, 2006). On the other
hand, Sykes et al. (2009) evaluated the QIM for cuttlefish
and related that the rejection occurred in the eighth day
of ice storage, with 22 demerit points. These controversial
results for the same species can be explained by the differ-
ent methodologies applied by each author. The QIM con-
ducted by Vaz-Pires and Seixas (2006) does not consider
the two training steps proposed before the protocol vali-
dation according Martinsdóttir et al. (2001). Thus, some
parameters, such as odor and color of the mantle cavity,
were not observed in the protocol. Moreover, the disagree-
ment between the two protocols demonstrates that results
obtained by the QIM are subject to the observation of the
assessors and to the choice of nonstandardized parameters
that will compose the final protocol.
3.2 Sampling size
QIM is classified as a qualitative methodology consider-
ing the training process of the assessors and the determi-
nation of the parameters to be evaluated. Moreover, the
procedure requires a large number of samples, as well as
a flexible and interactive experimental design (Marshall,
1996). In this way, the results obtained for freshness and
shelf life may present controversies due to sampling size
adopted by the authors. The QIM described by Vaz-Pires
and Seixas (2006) utilized 39 specimens of cuttlefish for the
entire procedure and obtained final scores between 0 and
17. On the other hand, for the same species, Sykes et al.
2660 QIM—A COMPREHENSIVE REVIEW. . .

TA B L E 1 QIM schemes main characteristics developed for fish species between 2017 and 2020
Estimated
shelf life
Species Product Storage conditions QI (days) References
Atlantic Cod (Gadus Raw, fillet, wild Chilled in ice (0 to 2 ◦ C) 0 to 14 10 Roiha, Jónsson, Backi,
morhua) Lunestad, & Karlsdóttir
(2017)
Black Tiger Shrimp Raw, whole, farmed Chilled in ice (0 ◦ C) 0 to 18 8 Le, Doan, Nguyen Ba, and
(Penaeus monodon) Tran (2017)
Carapeba (Eucinostomus Raw, whole, wild Chilled in ice (0 ± 0.1 ◦ C) 0 to 19 10 Gonçalves and Soares
gula) (2017)
Cobia (Rachycentron Raw, whole, farmed Chilled in ice (0 ± 1 ◦ C) 0 to 23 15 Fogaça et al. (2017)
canadum)
Tambaqui (Colossoma Raw, gutted, farmed Chilled in ice (0 ± 1 ◦ C) 0 to 34 22 Araújo et al. (2017)
macropomum)
Turbot (Scophthalmus Raw, gutted Chilled at 4 ◦ C 0 to 20 15 Li et al. (2017)
maximus)
Goldlined Seabream Raw, whole, wild Chilled in ice (0 ◦ C) 0 to 34 9 Ahmadi Shalhe et al.
(Rhabdosargus sarba) (2018)
Rainbow Trout Raw, whole and Chilled at 2 ◦ C 0 to 30 12 (whole) Diler and Genç (2018)
(Oncorhyncus mykiss) gutted, farmed (whole)
0 to 15 14 (gutted)
(gutted)
Greater Amberjack Raw, whole, farmed Chilled in ice (0 ± 1 ◦ C) 0 to 25 11 Freitas, Vaz-Pires, and
(Seriola dumerili) Câmara (2019)
Greenback Gray Mullet Raw, whole, wild Chilled at 4 ◦ C 0 to 34 12 Ghani Kuvei et al. (2019)
(Chelon subviridis)
Shrimp (Metapenaeus Raw, whole, wild Chilled in ice (0 ◦ C) 0 to 18 9 Khodanazary (2019)
affinis)
Nile Tilapia (Oreochromis Raw, whole, farmed Chilled in ice (1 ± 0.5 ◦ C) 0 to 19 11 Vázquez-Sánchez et al.
niloticus) (2020)
Note. The QIM references between 2000 and 2012, see table 1 in Bernardi et al. (2013). The QIM references between 2013 and 2016, see table 1 at Ndraha (2017).

(2009) utilized 60 samples in each step of the QIM, totaliz-
ing 180 samples. Consequently, a more extensive range of
parameters was observed and chosen to compose the QI
protocol, resulting in a more elaborate protocol, ranging
from 0 to 29 (Sykes et al., 2009). Nonetheless, when the
sampling size is the same, the protocol becomes similar
even for different species. Lanzarin et al. (2016) employed
105 specimens of Amazonian pintado (Pseudoplatystoma
fasciatum × Leiarius marmoratus), and the final QI pro-
tocol ranged from 0 to 18, with 11 sensory parameters
assessed. The same sampling size was adopted by Ritter
et al. (2016) by determining the QIM of tambatinga (Colos-
soma macropomum × Piaractus brachypomum), evaluat-
ing 10 sensory parameters of 105 specimens, and the final
QI protocol also featured a range from 0 to 18. Addition-
ally, the procedure to obtain the QI protocol was the same
in both studies, including storage temperature (0 ◦ C), sam-
pling size (105 samples), number of assessors (12), and the
training step (12 sessions of 30 min, totalizing 10 hr; Lan-
zarin et al., 2016; Ritter et al., 2016). Furthermore, the two
species are hybrids and originate from native species of
Amazonian rivers, justifying similar results too.
3.3 Species specificities
The protocol developed by Sant’Ana et al. (2011) for
blackspot seabream (Pagellus bogaraveo) presented 14
parameters, totalizing 30 demerit points. On the other
hand, Ritter et al. (2016) described a protocol for tambat-
inga containing 10 parameters and totalizing 18 demerit
points. These differences arise due to blackspot seabream
that comes from seawater, while tambatinga comes from
freshwater. The metabolic and microbial activities that
generate the sensory changes occur in different ways,
depending on the specificities of the fish (Liu et al., 2016).
Likewise, Borges et al. (2013) have reported a protocol
with 16 quality parameters for pacu (Piaractus mesopotam-
icus), totalizing 32 demerit points, which is different from
the results obtained for tambatinga (Ritter et al., 2016).
QIM—A COMPREHENSIVE REVIEW. . .
However, pacu and tambatinga are similar because both
are round fishes. The round fish group includes pacu,
tambaqui (Colossoma macropomum), pirapitinga (Piar-
actus brachypomus), their hybrids (such as tambatinga),
and other species of family Serrasalmidae (Hashimoto
et al., 2011; Ortí, Sivasundar, Dietz, & Jégu, 2008). Also,
their juvenile stages are morphologically indistinguishable
(Hashimoto et al., 2011). Therefore, a specific sensory pro-
tocol is required even for similar species, due to physical
changes and chemical reactions that appear in each species
due to the action of enzymes and microorganisms (Borges
et al., 2013). In this way, one of the basic principles of QIM
(species specificities) seems to be actually a disadvantage,
since it makes the procedure limited to qualifying only the
species to which it is applied, not allowing to generalize the
results. Thus, the procedure appears to be time consuming
and costly.
3.4 Storage conditions
In the general development of QIM, the storage of fish
samples occurs at refrigeration temperature, 0 ◦ C to 4 ◦ C
(Martinsdóttir et al., 2001). Differently, changes in the stor-
age temperature alter the shelf life of the fish, modifying
the final results. Campus et al. (2011) appraised the fresh-
ness of gilthead seabream (Sparus aurata) stored at 4 ◦ C
inside modified atmosphere packaging (MAP). The max-
imum storage period was 13 days. On the other hand, at
higher temperatures (8 ◦ C), the QI score rapidly increased.
This fast increment can be explained by the decreased sol-
ubility of CO2 in the MAP (Campus et al., 2011). The use
of very low temperatures (2 ◦ C) does not improve the sen-
sory parameters compared to storage at 4 ◦ C (Campus
et al., 2011) so that the temperature reduction from 4 ◦ C
to 2 ◦ C is not enough to reduce the microbial metabolism
and endogenous enzymes activities. On the other hand,
the temperature near the freezing point is able to extend
the shelf life, prolonging the QIM development. Baixas-
Nogueras et al. (2003) assessed the freshness of Mediter-
ranean hake (Merluccius merluccius) stored at flaked ice (0
◦ C) and inside a refrigerator set at 4 ◦ C. The sample accep-
tance does not surpass the eighth day of storage. For frozen
hake (M. capensis), the shelf life may reach months since
the samples are kept at temperatures below −10 ◦ C (Her-
rero, Huidobro, & Careche, 2003). Therefore, the develop-
ment of QIM from frozen fish can be considered slow, due
to the time required to obtain the final score, and destruc-
tive, as it involves the thawing of samples (Herrero et al.,
2003). In this way, the use of food plastic trays to pre-
vent fish from coming in contact with thawing liquids is
necessary (López-García, Ramil-Novo, Vázquez-Odériz, &
Romero-Rodríguez, 2014).
2661
4 QIM PANELS VERSUS SENSORY
DESCRIPTIVE ANALYSIS
Some of the weaknesses listed above, although numerous,
are manageable, such as the sampling size and the storage
conditions, by standardizing the number of samples and
the ideal storage conditions to establish QIM. However, as
presented in Figure 2, the sensory analysis procedure does
not start at the same point as QIM. For this purpose, the
incorrect construction of the panel group could be the pri-
mary source of bias for these analyses.
4.1 Assessors experience
The panel of trained assessors provides unique informa-
tion about the sensory characteristics (tastes, odors, and
textures) of the target product and is also widely used to
perform analytical tasks, mainly due to its sensory acuity
(Ares & Varela, 2017). Nonetheless, several challenges
affect sensory analysis, such as the correctness of training
of the assessors and the panel size. Borges et al. (2013)
developed the QIM for pacu (Piaractus mesopotamicus),
and the visual, olfactive, and textural analysis showed dif-
ferences for the protocol reported for tambacu (Colossoma
macropomum × Piaractus mesopotamicus) by Borges,
Conte-Junior, Franco, Mársico, and Freitas (2014). The
flesh firmness, eyes shape, and gills odor presented dis-
tinct demerit points at the same stage of storage. These
disparities can be justified due to the incorrect training and
low comparability between the assessors (Papadopoulou,
Panagou, Mohareb, & Nychas, 2013), or due to the dif-
ferent species specificities. However, both fish belong to
the round fish group, showing morphological similarities
(Ortí et al., 2008). Thus, the training procedure seems to be
the main reason of these variations. The panel group coor-
dinated by Borges et al. (2014) utilized two fishes for each
storage period in the first training step, totalizing 16 train-
ing sessions. On the other hand, Borges et al. (2013) utilized
one fish for each training session, totalizing 10 training
sessions. Moreover, the general guidelines for selection,
training, and monitoring of selected and expert sensory
assessors are currently described by the ISO 8586 (ISO,
2012). The international standard requires that a desirable
panel has at least 10 selected assessors, and at least two or
three times the number of assessors should be recruited for
screening before the final panel establishment. In this way,
the incorrect or insufficient training and the low number
of assessors may be responsible to affect the sensory
analysis, since the species present microbiological and
physical–chemical similarities (Borges et al., 2013, 2014).
Therefore, throughout the last two decades, novel sensory
descriptive methodologies have been applied in the sense
2662 QIM—A COMPREHENSIVE REVIEW. . .

F I G U R E 2 A macroscopic view of the development of QIM according to ISO 8586 (ISO, 2012)
Note. The panel leader is responsible for recruiting naive assessors, who have never participated in sensory analysis (a). The naive assessors are
presented with sensory analysis (b), and then a minor group is selected to compose the final panel (c). The selected panel goes on to training,
which corresponds to the first step of QIM (d). Throughout the development of QIM, the image data obtained during storage and the final
protocol can later be used by untrained assessors to perform WA and CATA methods, respectively. Moreover, the selected assessors work is
monitored by the panel leader (e), and at the end of the process they can become expert sensory assessors (f). Abbreviations: CATA: check-all-
that-apply; QIM: Quality Index Method; WA: word association.

to overcome the needing of a trained group of panelists,
such as the check-all-that-apply (CATA) and the word
association (WA) methods.
4.2 QIM sensory-related methods
CATA is described as an easy and quick methodology,
in which untrained assessors select from a list of all
the descriptors that they consider present in the product
according to their perception (Dooley, Lee, & Meullenet,
2010). WA is a method based on presenting stimuli to
untrained advisors, that should write the first association
that comes to their mind (Szczesniak & Skinner, 1973).
As described in Figure 2, these two methodologies can
be used combined with QIM. The changes related by the
trained assessors through the QI development and the
image data of fish freshness during the storage period
both could be used to build the CATA list and the WA
stimuli, respectively. Recently, Godoy, Veneziano, Cunha
Rodrigues, Schoffen Enke, and Lapa-Guimarães (2019)
employed both QIM, CATA and WA, to assess the qual-
ity of flathead gray mullet (Mugil cephalus) during ice stor-
age. The results indicated that both CATA and WA are use-
ful to evaluate fish quality, obtaining similar responses to
QIM. Since CATA uses the same protocol obtained from
QIM, similar results mean that using an elaborated QI
protocol, even untrained assessors can reach the results
for fish quality as a group of selected assessors. On the
other hand, a good correlation with WA could indicate
that, through visual stimuli, even untrained assessors can
achieve the same results as selected assessors. Since QIM
depends on an extended process, including recruitment,
familiarization, selection, and training of the assessors,
these results are contradictory, making it necessary to vali-
date the outcomes of QIM. Therefore, to evaluate the influ-
ence of the different analyses conducted by the assessors
and confirm the QIM results and correlate sensory rejec-
tion with predicted shelf life, effective statistical models
should be employed, mainly multivariate analysis, focus-
ing on describing QIM’s performance and understanding
the outcomes. In addition, some authors have also applied
diverse chemical and bacteriological analyses in order to
validate the results (Ahmadi Shalhe et al., 2018; Alasalvar
et al., 2002; Bogdanović et al., 2012; Borges et al., 2013, 2014;
Khodanazary, 2019; Li et al., 2017).
QIM—A COMPREHENSIVE REVIEW. . .
5 STATISTICAL MODELS FOR QIM
PERFORMANCE EVALUATION
One of the principles of QIM is to predict a linear rela-
tionship between the quality of the evaluated fish species
and the refrigeration storage time, composing the QIM
calibration curve, which allows estimating the remaining
shelf life of the samples (QIM Eurofish, 2013). However,
as noted above, the experience of the assessors and sam-
pling size are factors that generate uncertainty predictions.
Moreover, some parameters evaluated by the assessors dur-
ing storage seem to establish a greater influence on the
final score than others. In order to determine the uncer-
tainty associated with QIM prediction and the most impor-
tant sensory attributes for its development, the partial least
squares (PLS) regression was applied (Table 2). PLS, as
described by Wold, Sjöström, and Eriksson (2001), is a mul-
tiple linear regression that can analyze data with strongly
collinear and numerous X variables, and simultaneously
model several response variables (Y).
Most studies using PLS regression to determine QIM
prediction uncertainty (Table 2) had a high coefficient of
determination (>0.79), showing that scores assigned by
assessors during storage days significantly explain shelf-
life prediction proposed by the QIM. Moreover, the vari-
ables with importance to the projection (VIP) were deter-
mined in some of these studies. Gills odor, spot on pupil,
abdominal odor, eye color, iris color, gills color, eye shape,
abdominal color, pupil, eye transparency, and surface
appearance appear to be the most important variables to
describe fish sensory freshness during storage (Araújo, De
Lima, Peixoto Joele, & Lourenço, 2017; Borges et al., 2013,
2014; Lanzarin et al., 2016; Ritter et al., 2016; Vázquez-
Sánchez, García, Galvão, & Oetterer, 2020). The standard
errors, differently from the R2 , presented a wide range,
from 0.34 to 6.25. These results point out that, contradicto-
rily, despite a high R2 , some regressions tend to have shelf-
life prediction errors of almost 1 week (Ahmadi Shalhe
et al., 2018).
6 CHEMICAL VALIDATION
After harvesting, a series of biochemical changes occur
in fish body (Wu et al., 2019), including (i) the break-
down pathway of ATP, immediately after slaughter; (ii) the
production of undesirable protein derivates; and (iii) the
degradation of the lipid content (lipid oxidation). Three of
the most common chemical analysis used for determining
fish quality during storage, such as K value, total volatile
basic-nitrogen (TVB-N), and thiobarbituric acid-reactive
substances (TBARS) were performed by the authors as a
criterion to validate the QIM score and sensory rejection.
2663
6.1 K value
The K value is described as a chemical quality and fresh-
ness index for fish determined by nucleotide degradation
(Cheng, Sun, Pu, & Zhu, 2015a). This value is obtained
by quantifying ATP (adenosine triphosphate) and its
degradation product series, including adenosine diphos-
phate (ADP), adenosine monophosphate (AMP), inosine
monophosphate (IMP), inosine (HxR), and hypoxanthine
(Hx; Rahman, Kondo, Ogawa, Suzuki, & Kanamori, 2016).
In this way, HxR and Hx are correlated with loss of
fish freshness, and their accumulation indicates the start
of autolysis and bacterial spoilage (Canizales-Rodríguez
et al., 2015). The calculation of this index was first
described by Saito, Arai, and Matsuyoshi (1959), as the
percentage rate of HxR and Hx (nonphosphorylated ATP
breakdown products) to the sum of ATP and related degra-
dation products (ADP, AMP, IMP, HxR, and Hx; Rahman
et al., 2016). Alasalvar et al. (2002) determined the K value
and QIM for both cultured and wild sea bass (Dicentrar-
chus labrax) stored at 4 ◦ C for 22 days. The K value at the
sensory rejection time (18th day of storage) was about 50%
for cultured and 70% for wild sea bass. Therefore, QIM
seems to be underestimating the K value for cultured sea
bass, since the rejection range for aquatic products is above
60% (Cai, Cao, Bai, & Li, 2015). However, the different K
values obtained to cultured and wild sea bass can be justi-
fied by the different conditions of capture, handling, and
transport, factors that alter the rate of nucleotide degra-
dation (Vázquez-Ortiz, Pacheco-Aguilar, Lugo-Sanchez, &
Villegas-Ozuna, 1997). Recently, Li et al. (2017) developed
a QIM for turbot (Scophtalmus maximus), stored at 4 ◦ C
for 18 days. The turbot samples were rejected by the pan-
elists on the 15th day of storage. Nonetheless, the K value
had reached 60% around the 10th day of storage. There-
fore, QIM results overestimate the turbot shelf life. These
results showed that the sensory evaluation proposed by the
sensory panel does not correspond to the K value rejection
range.
6.2 TVB-N
TVB-N is a term used for describing some undesirable
products generated during the fish protein degradation,
more specifically originated from trimethylamine oxide
(TMAO), such as trimethylamine (TMA), dimethylamine
(DMA), and ammonia (Cheng, Sun, Zeng, & Liu, 2015b).
As described by EC (2005), the upper limits for TVB-N are
around 25 to 35 mg N/100 g. Gonçalves, De Lima, and De
Paula (2015) performed the QIM for spiny lobster (Pan-
ulirus argus) stored at 1 ◦ C for 18 days. The TVB-N val-
ues ranged from 5.23 to 20.31 mg N/100 g, and the lobster
2664 QIM—A COMPREHENSIVE REVIEW. . .

TA B L E 2 QIM’s multivariate statistical descriptors

Standard
Specie R2 error (days) VIP References
Atlantic Herring (Clupea harengus) 0.8 1.91 - Mai et al. (2009)
Cuttlefish (Sepia officinalis) 0.98 0.98 - Sykes et al. (2009)
Blackspot Seabram (Boops boops, L.) 0.98 0.95 - Bogdanović et al. (2012)
Pacu (Piaractus mesopotamicus) 0.95 1.18 Gill odor Borges et al. (2013)
Spot on pupil
Abdominal odor
Eye color
Hybrid Tambacu (Colossoma macropomum x 0.96 1.05 Iris color Borges et al. (2014)
Piaractus mesopotamicus)
Gills color
Eye shape
Spot on pupil
Amazonian Pintado (Pseudoplatystoma fasciatum 0.84 1.01 Abdominal odor Lanzarin et al. (2016)
x Leiarius marmoratus)
Gills odor
Abdominal color
Pupil
Hybrid Tambatinga (Colossoma macropomum x 0.79 1.19 Pupil Ritter et al. (2016)
Piaractus brachypomum)
Abdominal odor
Abdominal color
Gills color
Tambaqui Colossoma macropomum 0.98 2.94 Surface aspect Araújo et al. (2017)
Gills color
Abdominal odor
Eye transparency
Carapeba (Eucinostomus gula) 0.95 1.75 - Gonçalves and Soares (2017)
Cobia (Rachycentron canadum) 0.99 0.5 Skin appearance Fogaça et al. (2017)
Cornea
Gills mucus
Abdomen elasticity
Goldlined Seabream (Rhabdosargus sarba) 0.95 6.25 - Ahmadi Shalhe et al. (2018)
Greater Amberjack (Seriola dumerili) 0.99 0.54 Odor Freitas et al. (2019)
Gills odor
Eye color
Eye shape
Greenback Gray Mullet (Chelon subviridis) 0.96 4.8 - Ghani Kuvei et al. (2019)
Shrimp (Metapenaeus affinis) 0.96 1.15 - Khodanazary (2019)
Nile Tilapia (Oreochromis niloticus) 0.99 0.43 Gills odor Vázquez-Sánchez et al. (2020)
Skin brightness
Meat firmness
Pupil
Abbreviations: R2 : coefficient of determination; VIP: variables of importance to the projection.
QIM—A COMPREHENSIVE REVIEW. . .
samples were rejected on the 10th day of storage, when the
TVB-N value obtained was 15.5. Thus, QIM could under-
estimate the shelf life of spiny lobster since the TVB-N
value was below the acceptable limit on the 10th day. On
the other hand, another recent study on monitoring crus-
tacean shelf life showed that TVB-N levels increased up
to 25 mg N/100 g after 10 days of storage, as described by
Khodanazary (2019). TVB-N presented levels above 34 mg
N/100 g in the ninth day of storage for shrimp (Metape-
naeus affinis), as this index well correlated with the QIM
results, since the sensory panel rejected the samples at
the same day (Khodanazary, 2019). Moreover, the correla-
tion of QIM with the TVB-N values becomes problematic
when considering freshwater species, due to the absence of
TMAO in vivo. Acceptance levels for freshwater species are
lower in certain places, such as China, where the TVB-N
content cannot exceed 15 mg N/100 g (Cheng et al., 2015a).
This knowledge may justify the results of QIM assessed by
some authors, that determined TVB-N levels of around 10
to 18 mg N/100 g at the sensory rejection (Araújo et al., 2017;
Borges et al., 2013, 2014; Vázquez-Sánchez et al., 2020).
6.3 TBARS
TBARS is an index generally used to determine secondary
oxidative products, and thus interpret the degree of lipid
oxidation (Cheng et al., 2015b). This parameter is strongly
related to fish degradation due to the high levels of unsat-
urated fatty acids in this matrix (Rodrigues et al., 2017).
Its increase during storage is associated with the action
of lipoxygenase enzyme and other pro-oxidizing agents
(Monteiro et al., 2018). The acceptable limit for meat is 2 mg
MDA/kg. However, for fresh fish, the limits of malonalde-
hyde (oxidative damage indicator) remain not established
(Lanzarin et al., 2016). Bogdanović et al. (2012) described
the QIM for bogue (Boops boops, L.) and suggested limits of
5 to 8 mg MDA/kg for TBARS. These results are supported
by those described by Sykes et al. (2009). At the time of sen-
sory rejection (10th day of storage), the TBARS increased
up to around 5 mg MDA/kg. However, as described by
Sykes et al. (2009), this index is not a consistent method to
evaluate freshness in cuttlefish, since the cephalopod man-
tle composition has a small percentage of lipids. Moreover,
recent studies have shown that at the sensory rejection
day, the TBARS values are below 2 mg MDA/kg (Ahmadi
Shalhe et al., 2018; Araújo et al., 2017; Lanzarin et al., 2016;
Vázquez-Sánchez et al., 2020). In this way, there seems
to be no consent about the acceptable limits of TBARS
and the well correlation among this index and sensory
evaluation.
2665
7 BACTERIOLOGICAL VALIDATION
To validate the results obtained by the QIM, some authors
applied microbial growth as a parameter (Table 3). The
microbial growth may manifest as spoilage in foods, lead-
ing to sensory changes in the matrix (Gram & Dal-
gaard, 2002). The specific spoilage organisms are different
according to the seafood product evaluated but are gener-
ally described as Gram-negative, nonfermenting, and psy-
chrotrophic bacteria (Gram & Huss, 1996). Nonetheless,
there is no agreement about which bacteria should be mon-
itored for fish quality assessment (Fogarty et al., 2019). On
the other hand, it has been suggested that specific spoilage
bacteria, such as Pseudomonas spp., lactic acid bacteria
(LAB), hydrogen sulfide producing bacteria (HSPB), Bro-
chothrix termosphacta and Photobacterium spp. are the
main spoilage organisms for chilled fish (Fogarty et al.,
2019). The growth of these microorganisms is related to
their capacity to produce metabolic spoilage activity (Gram
& Dalgaard, 2002; Sant’Ana et al., 2011) as well as ammo-
niacal and sulfur odors (off-odors), increasing the demerit
points of fish assessed by QIM.
Ahmadi Shalhe et al. (2018) validated the QIM of
goldlined seabream (Rhabdosargus sarba) stored at 4
◦ C, monitoring the populational changes in mesophilic,
psychrotrophic, and Enterobacteriaceae bacteria. The
panelists rejected fish samples on the ninth day of storage
according to the sensory characteristics. On the same day,
Enterobacteriaceae populations were above 6 log CFU/g
and mesophilic and psychrotrophic populations were
above 7 log CFU/g, both higher than the maximum rec-
ommended limit (ICMSF, 1986). In this way, these results
were supported by the validation performed by Araújo
et al. (2017). According to the authors, the rejection of tam-
baqui (Colossoma macropomum) samples stored at 0 ◦ C
occurred on the 22nd day of storage, being well correlated
with the growth of mesophilic bacteria, that reached their
maximum allowable limit on the same day (ICMSF, 2005).
On the other hand, Vázquez-Sánchez et al. (2020) reported
that mesophilic and psychrotrophic populations on tilapia
(Oreochromis niloticus) stored at 1 ◦ C did not even reach 4
log CFU/g at the sensory rejection point (13th day). These
divergences indicate that the QIM may underestimate
the microbiological analysis, or that the microbial groups
previously related are not the best spoilage indicators in
fish. Besides, the population of HSPB was measured by
Cyprian et al. (2014a), which established the QIM of tilapia
fillets (Oreochromis niloticus) stored at 1 ◦ C, suggesting
that 6 log CFU/g is the maximum acceptable limit for
these bacteria at rejection point. However, as reported by
Fogarty et al. (2019), Pseudomonas spp. is one of the best
2666 QIM—A COMPREHENSIVE REVIEW. . .

TA B L E 3 Bacterial rejection count performed for QIM scheme validation

Specie Bacterial group Population at rejection References
Blackspot Seabream (Pagellus bogaraveo) TVC >7 log CFU/cm2 Sant’Ana et al. (2011)
HSPB >6 log CFU/cm2
Pseudomonas spp. >7 log CFU/cm2
Pacu (Piaractus mesopotamicus) Mesophilic >7 log CFU/g Borges et al. (2013)
Psychrothrophic >8 log CFU/g
Hybrid Tambacu (Colossoma macropomum x Mesophilic >7 log CFU/g Borges et al. (2014)
Piaractus mesopotamicus)
Psychrotrophic >7 log CFU/g
Tilapia (Oreochromis niloticus) fillets TVC 7 log CFU/g Cyprian, Sveinsdóttir,
Magnússon, and
Martinsdóttir (2014b)
HSPB 6 log CFU/g
Spiny Lobster (Panulirus argus) Mesophilic >4 log CFU/g Gonçalves, de Lima, and de
Paula (2015)
Psychrotrophic >4 log CFU/g
Amazonian Pintado (Pseudoplatystoma fasciatum Mesophilic 6 log CFU/g Lanzarin et al. (2016)
x Leiarius marmoratus)
Psychrotrophic >7 log CFU/g
Hybrid Tambatinga (Colossoma macropomum x Mesophilic >7 log CFU/g Ritter et al. (2016)
Piaractus brachypomum)
Psychrotrophic >9 log CFU/g
Atlantic Cod (Gadus morhua) TVC >7 log CFU/g Roiha et al. (2017)
HSPB >6 log CFU/g
Carapeba (Eucinostomus gula) Mesophilic >3 log CFU/g Gonçalves and Soares (2017)
Psychrotrophic >4 log CFU/g
Cobia (Rachycentron canadum) Mesophilic >3 log CFU/g Fogaça et al. (2017)
Psychrotrophic >3 log CFU/g
Enterobacteriaceae >3 log CFU/g
HSPB >2 log CFU/g
Pseudomonas spp. >5 log CFU/g
Goldlined Seabream (Rhabdosargus sarba) Mesophilic >7 log CFU/g Ahmadi Shalhe et al. (2018)
Psychrotrophic >7 log CFU/g
Enterobacteriaceae >6 log CFU/g
Greater Amberjack (Seriola dumerili) TVC >7 log CFU/g Freitas et al. (2019)
HSPB >7 log CFU/g
Greenback Grey Mullet (Chelon subviridis) Mesophilic 7 log CFU/g Ghani Kuvei et al. (2019)
Psychrotrophic 7 log CFU/g
Shrimp (Metapenaeus affinis) Mesophilic >7 log CFU/g Khodanazary (2019)
Psychrotrophic >6 log CFU/g
Nile Tilapia (Oreochromis niloticus) Mesophilic >3 log CFU/g Vázquez-Sánchez et al. (2020)
Psychrotrophic >3 log CFU/g
Abbreviations: CFU: colony forming units; HSPB: hydrogen sulfide producing bacteria; TVC: total viable count.

spoilage indicators in fresh fish, rather than mesophilic, et al. (2011). After the fourth day of ice storage, the popu-
psychrotrophic, and HSPB. lation exceeded 4 log CFU/cmš, reaching 7 log CFU/cmš
The count of Pseudomonas spp. in raw blackspot on the 12th day, which would indicate the rejection
seabream (Pagellus bogaraveo) was performed by Sant’Ana (Sant’Ana et al., 2011), as the maximum acceptable limit for
QIM—A COMPREHENSIVE REVIEW. . .
Pseudomonas spp. is 7 log CFU/g (Koutsoumanis, 2001).
Nonetheless, according to the QIM results, this fish could
be consumed in up to 11 days of storage (Sant’Ana et al.,
2011). These results demonstrate that the sensory analy-
sis of the QIM underestimates the microbiological anal-
ysis, leading to discarding fish that is able for consump-
tion. Inversely, Khodanazary (2019) assessed the freshness
of shrimp (Metapenaeus affinis). These authors found that
the QIM indicates that the shelf life in ice stored was 9
days and the total mesophilic count of Metapenaeus affinis
reached 7 log CFU/g before the ninth day (Khodanazary,
2019), which is higher than the maximal recommended
(ICMSF, 1986). In this way, QI may overestimate the real
bacteriological shelf life of fish, leading to the consump-
tion of improper food. Moreover, these results show the
need for novel methodologies for fish quality assessment
that can mimic the human senses without being subject to
possible sensory errors.
8 ARTIFICIAL QUALITY INDEX (AQI)
The use of artificial instruments for the evaluation of color
and odor allows the construction of an AQI, a less destruc-
tive, low cost, and easy-to-perform practice (Macagnano
et al., 2005). Despite the development of several studies
of AQI, published reviews on the use of these artificial
instruments for fish freshness assessment are still limited.
Cheng et al. (2015b) published a review discussing a vari-
ety of approaches for determining fish quality, including
artificial instruments. Recently, another study has been
classified the AQI instruments as Sensory Bionic Tech-
nologies (SBT), able to overcome the subjectivity and poor
repeatability of sensory methods (Wu et al., 2019). SBT
application is based on the artificial senses of smell, taste,
and vision (Shi et al., 2018), and comprises (i) electronic
noses (Loutfi, Coradeschi, Mani, Shankar, & Rayappan,
2015; Zaukuu, Bazar, Gillay, & Kovacs, 2019), (ii) electronic
tongues (Jiang, Zhang, Bhandari, & Adhikari, 2018; Peris &
Escuder-Gilabert, 2009; Zaukuu et al., 2019), (iii) computer
vision techniques (Wu et al., 2019), and (iv) colorimetric
sensor arrays (CSAs; Huang, Xin, & Zhao, 2011).
8.1 Electronic nose
The practical application of the human nose as a qual-
ity assessment instrument is severely limited by the fact
that our sense of smell gets tired easily (Di Natale et al.,
1998). Moreover, it has to be noted that the communica-
tion of olfactive experiences, contrary to those related to
sight or hearing, is quite vague (Di Natale et al., 1998;
Loutfi et al., 2015). This means that to develop QI, the
2667
use of human olfaction can generate errors since the
sensory analysis by a trained panel is a costly process,
requires relatively long periods, and the human response to
odors is subjective (Peris & Escuder-Gilabert, 2009). There-
fore, the need of a rapid detection (Mai, Martinsdóttir,
Sveinsdóttir, Olafsdóttir, & Arason, 2009), nondestructive
(Macagnano et al., 2005), sensitive (Haugen et al., 2006),
cost-effective (Macagnano et al., 2005), and easy-to-build
(Peris & Escuder-Gilabert, 2009) instrument made the use
of electronic noses more common. The electronic nose (e-
nose) is an instrument that comprises an array of heteroge-
neous electrochemical gas sensors with partial specificity
and a pattern recognition system (Persaud & Dodd, 1982).
E-nose provides a quantitative representation or signature
of a gas. The gas sensor can be divided into metal oxide,
electrochemical, conductive polymer, and photoionization
(Wu et al., 2019).
Studies on the use of e-noses in fish quality determi-
nation include their use as a sensor for the detection
of degradation biomarkers such as volatile compounds
(Table 4; Macagnano et al., 2005; Mai et al., 2009; Olafs-
dottir et al., 2004), since it presents high sensitivity to
small variations of these compounds (Mai et al., 2009).
In addition, as described by Mai et al. (2009), QIM and
e-nose are well correlated, since QI odor descriptor results
are closely related to the e-nose gas measured responses
(NH3 , H2 S, SO2 , and CO), according to a PCA biplot.
Moreover, Gholam Hosseini, Luo, Xu, Liu, and Benjamin
(2008) related that e-nose could be employed for freshness
assessment of different species. However, at the early
ice storage days, it is not sensitive enough to estimate
freshness, as its accuracy increases above a certain level
of volatile compounds (Mai et al., 2009). Guohua, Lvye,
Yanhong, and Lingxia (2012) developed an e-nose com-
posed by a sensor with eight metal oxide semiconductors
to predict shelf life of grass carp (Ctenopharyngodon
idella). The intensity of the response increased with the
storage time of the samples, which were divided into
three groups (fresh, medium, and aged). The response of
the sensors corresponds to the influence of volatile gases
produced by the samples on their electrical characteristics.
Sensor 8 (MQ-9, methane, carbon monoxide) showed high
responsiveness to the volatile gases. However, all sensors
showed voltammetric variations in 2.5 s. The accuracy of
the quality prediction was 87.5% (Guohua et al., 2012). On
the other hand, the conducting polymer e-nose applied
by Wilson, Oberle, and Oberle (2013) for detect off-flavor
in catfish (Ictalarus puncatus) presents an accuracy over
90%, due to the 32 sensor array.
These results indicate that e-nose is a promising technol-
ogy for food quality assessment (Wojnowski, Majchrzak,
Dymerski, Gębicki, & Namieśnik, 2017), that allows to
estimate the rate of degradation (Loutfi et al., 2015), the
 2668

TA B L E 4 Bionic sensor technologies application on fish quality assessment

Sensor Statistical
Specie Bionic sensor model Detection target Sensor type no. analyze R2 References
Atlantic Herring (Clupea harengus) Electronic nose Volatile compounds (CO, Electrochemical gas 4 PLS - Mai et al. (2009)
SO2 , NH3 , H2 S) sensor
Grass Carp (Ctenopharyngodon idellus) Electronic nose Volatile compounds Metal oxide 8 SNR 0.993 Guohua et al. (2012)
semiconductors
Pontic Shad (Alosa pontica) Electronic tongue TVB-N and BAs (cadaverine Polypyrrole doped 3 PLS 0.948 to 0.971 Apetrei et al. (2013)
and histamine) electrodes
Gilthead Seabream (Sparus aurata) Machine vision Gills and eyes color changes - - ANN 0.961 to 0.995 Dowlati et al. (2013)
Cod (Gadus morhua) Electronic tongue TVB-N Metallic electrodes 8 PLS 0.795 Ruiz-Rico et al. (2013)
Catfish (Ictalurus puncatus) Electronic nose Flavor Conductin polymer 32 ANN - Wilson et al. (2013)
Jumbo Squid (Dosidicus gigas) Colorimetric sensor Mesophilic, psychrotrophic Dyes 8 PLS - Zaragozá et al. (2015)
and H2 S producing
bacteria
Atlantic Salmon (Salmo salar) Colorimetric sensor TVB-N and BAs (cadaverine Dyes 16 PLS 0.730 Morsy et al. (2016)
and putrescine)
Tilapia (Oreochromis niloticus) Machine vision Gills and pupils color changes - - LSD 0.989 to 0.999 Shi et al. (2018)
Abbreviations: ANN: artificial neural network; BAs: biogenic amines; HSPB: hydrogen sulfide producing bacteria; LSD: least significant difference; PLS: partial least squares; R2 : coefficient of determination; SNR:
signal-to-noise ratio; TVB-N: total volatile basic nitrogen.
QIM—A COMPREHENSIVE REVIEW. . .
QIM—A COMPREHENSIVE REVIEW. . .
freshness (Gholam Hosseini et al., 2008; Macagnano et al.,
2005), and detect spoilage (Mai et al., 2009), producing sim-
ilar results to those of a trained panel (Macagnano et al.,
2005), being quickly, nondestructive, and cost effective.
8.2 Electronic tongue
The application principle of electronic tongues (e-tongues)
is the same as the e-noses. Nonetheless, the gas sen-
sor array is adapted to a liquid sensor array. Recently,
Ghasemi-Varnamkhasti, Apetrei, Lozano, and Anyogu
(2018) published a review on the use of e-tongues as a
system for spoilage examination in foods and described
its physical structure, that comprises three fundamen-
tal components: automatic sampler, array of sensors, and
chemometric approaches. Moreover, the most often used
e-tongues are based on potentiometric sensors (potentio-
metric, voltammetric, amperometric, impedimetric, con-
ductimetric; Ghasemi-Varnamkhasti et al., 2018). Gong
et al. (2016) combined a commercial e-tongue and sensory
descriptions to detect the key umami-related compounds
of Yangtze Coilia ectenes. Na+ showed the lowest umami
score when analyzed by the e-tongue, and was the most
identified compound by the sensory panel in the omission
test (used to evaluate the impact of each substance on the
umami taste; Gong et al., 2016). In this way, e-tongues are
a promising technology for detecting the main compounds
related to fish flavor, since they seem to be well correlated
with descriptive panels.
Apetrei, Rodriguez-Mendez, Apetrei, and de Saja (2013)
developed an electrochemical e-tongue based on voltam-
metry measurements to determine biogenic amines (BAs)
of pontic shad (Alosa pontica) during storage at 4 ◦ C
(Table 4). A multisensory system composed of electrodes
modified with polypyrrole doped with different doping
agents was employed to monitor fish spoilage (Apetrei
et al., 2013). These authors found that an increase of the
signal currents associated with the BAs was observed while
increasing storage days. Likewise, Ruiz-Rico et al. (2013)
employed a system with eight metallic electrodes grouped
in two voltammetric e-tongues. The first e-tongue was
composed by four noble metals (iridium, rhodium, plat-
inum, and gold) and the second by four nonnoble metals
(silver, cobalt, copper, and nickel). The system was able
to discriminate fresh fish (days 0 and 1) and spoiled fish
(fourth day), and the statistical models obtained with the
e-tongue measurements successfully predicted mesophilic
bacteria (Ruiz-Rico et al., 2013). Therefore, e-tongues also
demonstrate potential as an alternative method for esti-
mating fish shelf life.
2669
8.3 Machine vision system (MVS)
Color is one of the most important food quality param-
eters and has a direct effect on consumer buying inten-
tion (Shi et al., 2018). On the other hand, this matrix is
highly susceptible to color changes due to decay process
(Shi et al., 2018), in which the discoloration is caused by
the formation of metmyoglobin (Chaijan, Benjakul, Vises-
sanguan, & Faustman, 2005). QI as a tool for color assess-
ment is an expensive and time-consumption procedure
(Dowlati, de la Guardia, Dowlati, & Mohtasebi, 2012).
Moreover, the color measured by a panel is a subjective
result, which is difficult to convert to reproducible numer-
ical values (Hong, Yang, You, & Cheng, 2014). Therefore,
other fast and noninvasive methods have been developed
for a continuous fish evaluation, such as the MVS (Dowlati
et al., 2012; Shi et al., 2018). MVS is an emerging tech-
nology employed to recognize objects, extract, and ana-
lyze quantitative information from digital images (Hong
et al., 2014). The images are acquired by a system com-
posed of camera, illumination device, frame grabber, and
computer, and processed by pretreatment, segmentation,
and feature extraction (Hong et al., 2014). The results for
color obtained are expressed as multiple regression mod-
els, with high correlation coefficients (Shi et al., 2018),
so that MVS can represent an alternative tool to human
eyes.
Shi et al. (2018) developed an MVS to predict the fresh-
ness of tilapia (Oreochromis niloticus). The MVS utilized
the color changes presented by the pupils and the gills of
the fish and compared them with the biochemical (TVB-N
and TBARS) and bacteriological (total viable count [TVC])
indicators (Shi et al., 2018). These authors showed that
by using the MVS, it is possible to predict the values of
these freshness indicators in tilapia stored at 4 ◦ C (Table 4).
These data are supported by Dowlati et al. (2012), that uti-
lized an MVS to assess the freshness of gilthead seabream
(Sparus aurata) by images of gills and pupils. The color
changes presented by the gills reflect better the quality
and freshness of the fish than the changes in the eyes
(Dowlati et al., 2012), as the R2 for this factor is closer to 1
(Table 4). Moreover, the use of MVS seems to obtain bet-
ter color results than the use of colorimeters, since the
color obtained is much closer to the actual color of the
fish, with distinct total color differences (ΔE) among the
two devices (Yagiz, Balaban, Kristinsson, Welt, & Marshall,
2009). On the other hand, different from the previous two
methods, there are no studies about the use of MVS and
sensory analysis together to express fish freshness during
storage.
2670
8.4 CSA
CSA, also called optoelectric sensor, is an olfaction–
visualization technology based on color changes due to
chemical bonds between chromogenic agents and gases
through metal, hydrogen bonds, or covalent bonds (Wu
et al., 2019). Zaragozá et al. (2015) utilized a CSA to
evaluate the freshness of jumbo squid (Dosidicus gigas)
stored at 4 ◦ C. The CSA was composed of six sensory
materials obtained by mixing an aluminum oxide or sil-
ica gel suspension with the corresponding dye and an
appropriate solvent. All sensors changed color and inten-
sity during storage and PLS models were performed. The
chromogenic data successfully predicted concentrations of
mesophilic, psychrotrophic, and hydrogen sulfide produc-
ing bacteria (Zaragozá et al., 2015).
Morsy et al. (2016) monitored the freshness of Atlantic
salmon (Salmo salar) using a colorimetric sensor com-
posed of 16 substances sensitive to spoilage compounds
(TMA, DMA, cadaverine, and putrescine). Fish spoilage
was evaluated by TVC during 9 days and the color
changes obtained by CSA were well correlated with micro-
bial growth (Morsy et al., 2016). Recently, Zhong et al.
(2018) proposed a CSA composed of gold nanoparticles,
graphene oxide, hydrogel silicon, and pH-sensitive dyes
to detect eight different gaseous BAs. Furthermore, a
poly (ortho-phenylenediamine-co-aniline) copolymer col-
orimetric sensor based was developed by Domínguez-
Aragón, Olmedo-Martínez, and Zaragoza-Contreras (2018)
to assess the freshness of tilapia fillets stored at 10 ◦ C. The
evaluation performed by these authors consisted in the
detection of color changes in the copolymer due to pH vari-
ations produced by the total volatile bases (TVB) generated
after the initial freshness phase. In addition, the bacterio-
logical analysis showed that the Pseudomonas spp. count
reached the maximum limit within 2 days, similar to the
maximum TVB levels (close to 25 mg/100 g) detected by
CSA (Domínguez-Aragón et al., 2018). The results obtained
by the application of CSA demonstrate that this bionic sen-
sor can be applied to assess fresh fish quality.
8.5 Challenges in the application of AQI
The SBT, although fast and objective, reflects more the
state of spoilage than the state of freshness, as they detect
chemical and microbiological changes during the late
stages of storage (Cléach et al., 2019). Moreover, these novel
technologies still have structural (physical) and method-
ological (chemical) limitations that make their use defiant.
E-nose and e-tongue sensors sensitivity are highly suscep-
tible to environmental conditions (e.g., oxidation; Holmin,
Krantz-Rülcker, Lundström, & Winquist, 2001), resulting
in an aging process described as sensor drift, responsible to
QIM—A COMPREHENSIVE REVIEW. . .
weaken their sensitivity (Zaukuu et al., 2019). In the e-nose
measurements, in particular, the speed at which volatile
compounds are taken from the sample to the electronic
nose sensor chamber (headspace generation time) should
be considered to establish their application method, as this
may influence signal strength (González-Martín, Pérez-
Pavón, González-Pérez, Hernández-Méndez, & Álvarez-
García, 2000). In this way, the development of a device
able to overcome the influences of airflow and modulate
the temperature to maintain a steady environment could
be an alternative to improve the e-nose responses (Li, Lei,
Zhang, Shao, & Xie, 2015). Also, as the e-tongue device only
evaluates liquids, samples in solid state, as fish and fish by-
products, require transformations before the instrumental
assessment. Therefore, the use of protocols where there
is a minimum of biochemical changes, such as extraction
and microfiltration (García et al., 2017; Han, Huang, Teye
& Gu, 2015) could be adopted. However, there is no con-
sent on which type of extraction method presents the most
representative results (Zaukuu et al., 2019). In addition,
the use of MVS to assess the quality of fresh fish also has
its limitations, since, for the capture of the gills images,
Shi et al. (2018) needed to remove them from the sam-
ples, making the method time consuming and destructive.
At least, CSA signal responses reach a plateau before the
10th day of storage, suggesting an early sensor saturation
(Morsy et al., 2016). Thus, as well as QIM, the emerging
instrumental methods previously described also have their
weaknesses. In this role, alternative technologies, such as
molecular approaches and mitochondrial activity monitor-
ing have been developed (Cléach et al., 2019; Costa et al.,
2019).
8.6 State of the art of instrumental
methods for fish quality monitoring
Li et al. (2017) applied QIM associated with proteomic
approaches to evaluate the quality of turbot (Scophthalmus
maximus). QIM results showed that turbot stored at 4 ◦ C
are not suitable for consumption at the fifteenth day of
storage. On the proteomic analysis, seven proteins of inter-
est were excised from two-dimensional gel electrophoresis
(2-DE), digested with trypsin and identified by matrix-
assisted laser desorption/ionization time-of-flight/time-
of-flight (MALDI-TOF-TOF) mass spectrometer (Li et al.,
2017). The changes in these muscle proteins were signifi-
cantly correlated with the QIM results, and actin was the
protein that showed the greatest intensity variation during
the storage. These results indicate that actin can be applied
as a new early indicator of fish freshness (Costa et al., 2019).
Nonetheless, this method may be considered destructive
and high cost, since the turbot muscle is ground in liquid
nitrogen and depends on robust equipment (Li et al., 2017).
QIM—A COMPREHENSIVE REVIEW. . .
A practical methodology is necessary for field use rep-
resents another difficulty for the determination of quality
in fresh fish, and the methods currently employed present
laboratory demand. Hasanah et al. (2019) employed an
optical pH sensor based on the immobilization of chro-
moionophore by a membrane of pectin for fish fresh-
ness monitoring at 4 ◦ C. During the storage, the pH of
the samples decreased in the first days due to glycogen
degradation and lactic acid formation (Fogarty et al., 2019).
From the seventh day, the pH increased up to 8, due to bac-
terial enzymatic activity, resulting in alkalinity conditions
(Fogarty et al., 2019). However, as the sensory and instru-
mental methods, the results reflect the state of deteriora-
tion rather than freshness. Moreover, fish microbiome is
influenced by fish trophic level (Liu et al., 2016), which can
lead to variations in pH, preventing its use as a standard
method.
Cléach et al. (2019) evaluated the postmortem changes in
mitochondrial structure and function to determinate fish
freshness. Mitochondria plays a key role in the mecha-
nisms involving cell death, such as necrosis and apopto-
sis (Parsons & Green, 2010). The mitochondria of gilthead
seabream (Sparus aurata) stored at 4 ◦ C was isolated and
analyzed for oxygen consumption and membrane poten-
tial (Cléach et al., 2019). The mitochondrial structure was
altered during storage, due to the reduction in respiratory
activity and membrane potential disrupt. However until
the fourth day of storage, respiratory activity remained sig-
nificant (Cléach et al., 2019). These results indicate that
mitochondria may be applied as a target to evaluate fish
freshness (Cléach et al., 2019). On the other hand, the
structural and physiological changes of the mitochondria
that influence the perception of the consumer remain not
elucidated.
9 CONCLUSION
QIM is a nondestructive fish sensory evaluation tool widely
applied in research and industry. However, QIM presents
some limitations that are difficult for its widespread use
as an official quality assessment method. Fish freshness
state depends on the storage temperature and QIM can be
considered a destructive methodology for frozen fish. In
addition, the scheme of training of the assessors can lead
to erroneous sensory analysis. Thus, the subjective results
may often be contradictory to bacteriological and chemical
analysis. In this way, methodologies such as e-nose, e-
tongue, MVS, and CSA have been employed as a potential
alternative to overcome the QIM limitations, and emerg-
ing techniques such as proteomic analysis, pH optical
sensor, and mitochondrial changes monitoring have been
developed as alternatives for an authentic determination
2671
of the freshness state of this matrix. Although low cost (pH
optical) and fast, some of these methodologies still have
limitations, such as the destruction of the sample and the
absence of correlation with the sensorial analysis. There-
fore, further studies are necessary for the development
of novel quality control methodologies and understand-
ing of the technologies already proposed, allowing
their use as a public health instrument for freshness
assessment.
AC K N OW L E D G M E N T S
This study was financed in part by the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior—Brazil
(CAPES)—Finance Code001. Fundação de Amparo à
Pesquisa do Estado do Rio de Janeiro—Brazil (FAPERJ)—
grant number [E-26/200.195/2020, E-26/203.049/2017, E-
26/010.000148/2020] and Conselho Nacional de Desen-
volvimento Científico e Tecnológico (CNPq) grant number
[311422/2016-0, 140947/2019-1].
AU T H O R CO N T R I B U T I O N S
Yago A. A. Bernardo developed the idea of the article,
compilated the literature, and wrote the article. Denes K.
A. Rosário participated in the writing, making substantial
contributions, and reviewed the article. Isabella F. Delgado
and Carlos A. Conte-Junior reviewed the final article.
CONFLICTS OF INTEREST
Authors declare no conflicts of interest.
ORCID
Yago A. A. Bernardo https://orcid.org/0000-0001-8778-
3236
Denes K. A. Rosario https://orcid.org/0000-0001-8565-
2021
Carlos A. Conte-Junior https://orcid.org/0000-0001-
6133-5080
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How to cite this article: Bernardo YAA, Rosario
DKA, Delgado IF, Conte-Junior CA. Fish Quality
Index Method: Principles, weaknesses, validation
and alternatives – a review. Compr Rev Food Sci
Food Saf. 2020;19:2657–2676.
https://doi.org/10.1111/1541-4337.12600